Comprehensive analysis of the HEPN superfamily: identification of novel roles in intra-genomic conflicts, defense, pathogenesis and RNA processing View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2013-12

AUTHORS

Vivek Anantharaman, Kira S Makarova, A Maxwell Burroughs, Eugene V Koonin, L Aravind

ABSTRACT

BACKGROUND: The major role of enzymatic toxins that target nucleic acids in biological conflicts at all levels has become increasingly apparent thanks in large part to the advances of comparative genomics. Typically, toxins evolve rapidly hampering the identification of these proteins by sequence analysis. Here we analyze an unexpectedly widespread superfamily of toxin domains most of which possess RNase activity. RESULTS: The HEPN superfamily is comprised of all α-helical domains that were first identified as being associated with DNA polymerase β-type nucleotidyltransferases in prokaryotes and animal Sacsin proteins. Using sensitive sequence and structure comparison methods, we vastly extend the HEPN superfamily by identifying numerous novel families and by detecting diverged HEPN domains in several known protein families. The new HEPN families include the RNase LS and LsoA catalytic domains, KEN domains (e.g. RNaseL and Ire1) and the RNase domains of RloC and PrrC. The majority of HEPN domains contain conserved motifs that constitute a metal-independent endoRNase active site. Some HEPN domains lacking this motif probably function as non-catalytic RNA-binding domains, such as in the case of the mannitol repressor MtlR. Our analysis shows that HEPN domains function as toxins that are shared by numerous systems implicated in intra-genomic, inter-genomic and intra-organismal conflicts across the three domains of cellular life. In prokaryotes HEPN domains are essential components of numerous toxin-antitoxin (TA) and abortive infection (Abi) systems and in addition are tightly associated with many restriction-modification (R-M) and CRISPR-Cas systems, and occasionally with other defense systems such as Pgl and Ter. We present evidence of multiple modes of action of HEPN domains in these systems, which include direct attack on viral RNAs (e.g. LsoA and RNase LS) in conjunction with other RNase domains (e.g. a novel RNase H fold domain, NamA), suicidal or dormancy-inducing attack on self RNAs (RM systems and possibly CRISPR-Cas systems), and suicidal attack coupled with direct interaction with phage components (Abi systems). These findings are compatible with the hypothesis on coupling of pathogen-targeting (immunity) and self-directed (programmed cell death and dormancy induction) responses in the evolution of robust antiviral strategies. We propose that altruistic cell suicide mediated by HEPN domains and other functionally similar RNases was essential for the evolution of kin and group selection and cell cooperation. HEPN domains were repeatedly acquired by eukaryotes and incorporated into several core functions such as endonucleolytic processing of the 5.8S-25S/28S rRNA precursor (Las1), a novel ER membrane-associated RNA degradation system (C6orf70), sensing of unprocessed transcripts at the nuclear periphery (Swt1). Multiple lines of evidence suggest that, similar to prokaryotes, HEPN proteins were recruited to antiviral, antitransposon, apoptotic systems or RNA-level response to unfolded proteins (Sacsin and KEN domains) in several groups of eukaryotes. CONCLUSIONS: Extensive sequence and structure comparisons reveal unexpectedly broad presence of the HEPN domain in an enormous variety of defense and stress response systems across the tree of life. In addition, HEPN domains have been recruited to perform essential functions, in particular in eukaryotic rRNA processing. These findings are expected to stimulate experiments that could shed light on diverse cellular processes across the three domains of life. REVIEWERS: This article was reviewed by Martijn Huynen, Igor Zhulin and Nick Grishin. More... »

PAGES

15

References to SciGraph publications

  • 2010-01. An overview on nucleases (DNase, RNase, and phosphodiesterase) in snake venoms in BIOCHEMISTRY (MOSCOW)
  • 2003-12. New connections in the prokaryotic toxin-antitoxin network: relationship with the eukaryotic nonsense-mediated RNA decay system in GENOME BIOLOGY
  • 2010-12. OST-HTH: a novel predicted RNA-binding domain in BIOLOGY DIRECT
  • 2010-12. Post-transcriptional control by bacteriophage T4: mRNA decay and inhibition of translation initiation in VIROLOGY JOURNAL
  • 2009-12. Prokaryotic homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements in BIOLOGY DIRECT
  • 2010-10. Structural basis for 16S ribosomal RNA cleavage by the cytotoxic domain of colicin E3 in NATURE STRUCTURAL & MOLECULAR BIOLOGY
  • 2005-09. Mobile genetic elements: the agents of open source evolution in NATURE REVIEWS MICROBIOLOGY
  • 2009-05. Microbial community structure and its functional implications in NATURE
  • 2012-12. Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics in BIOLOGY DIRECT
  • 2011-06. Evolution and classification of the CRISPR–Cas systems in NATURE REVIEWS MICROBIOLOGY
  • 2011-11. Regulation of growth and death in Escherichia coli by toxin–antitoxin systems in NATURE REVIEWS MICROBIOLOGY
  • 2010-12. Hidden Markov model speed heuristic and iterative HMM search procedure in BMC BIOINFORMATICS
  • 2009-01. The exosome contains domains with specific endoribonuclease, exoribonuclease and cytoplasmic mRNA decay activities in NATURE STRUCTURAL & MOLECULAR BIOLOGY
  • 2009. The Integron/Gene Cassette System: An Active Player in Bacterial Adaptation in HORIZONTAL GENE TRANSFER
  • 2013-09. Recent Advances in Plant–Virus Interaction with Emphasis on Small Interfering RNAs (siRNAs) in MOLECULAR BIOTECHNOLOGY
  • 2009-12. Comprehensive comparative-genomic analysis of Type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes in BIOLOGY DIRECT
  • 2011-12. Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems in BIOLOGY DIRECT
  • 2009-02-05. The unfolded protein response signals through high-order assembly of Ire1 in NATURE
  • 2008-12. MutL homologs in restriction-modification systems and the origin of eukaryotic MORC ATPases in BIOLOGY DIRECT
  • 2004-12. MUSCLE: a multiple sequence alignment method with reduced time and space complexity in BMC BIOINFORMATICS
  • 2004-09. Escherichia coli mazEF-mediated cell death as a defense mechanism that inhibits the spread of phage P1 in MOLECULAR GENETICS AND GENOMICS
  • 2011-12. Prevalence of SOS-mediated control of integron integrase expression as an adaptive trait of chromosomal and mobile integrons in MOBILE DNA
  • 2011. Characterizing Immune Receptors from New Genome Sequences in IMMUNE RECEPTORS
  • 2010-09. RNA-based antiviral immunity in NATURE REVIEWS IMMUNOLOGY
  • 2010-05. Bacteriophage resistance mechanisms in NATURE REVIEWS MICROBIOLOGY
  • 2012-12. Live virus-free or die: coupling of antivirus immunity and programmed suicide or dormancy in prokaryotes in BIOLOGY DIRECT
  • 2009-01. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells in NATURE STRUCTURAL & MOLECULAR BIOLOGY
  • 2000-06. Who's your neighbor? New computational approaches for functional genomics in NATURE BIOTECHNOLOGY
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1186/1745-6150-8-15

    DOI

    http://dx.doi.org/10.1186/1745-6150-8-15

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1034075663

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/23768067


    Indexing Status Check whether this publication has been indexed by Scopus and Web Of Science using the SN Indexing Status Tool
    Incoming Citations Browse incoming citations for this publication using opencitations.net

    JSON-LD is the canonical representation for SciGraph data.

    TIP: You can open this SciGraph record using an external JSON-LD service: JSON-LD Playground Google SDTT

    [
      {
        "@context": "https://springernature.github.io/scigraph/jsonld/sgcontext.json", 
        "about": [
          {
            "id": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/0604", 
            "inDefinedTermSet": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/", 
            "name": "Genetics", 
            "type": "DefinedTerm"
          }, 
          {
            "id": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/06", 
            "inDefinedTermSet": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/", 
            "name": "Biological Sciences", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Genomics", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Prokaryotic Cells", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Protein Structure, Tertiary", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "RNA", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Ribonucleases", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Toxins, Biological", 
            "type": "DefinedTerm"
          }
        ], 
        "author": [
          {
            "affiliation": {
              "alternateName": "National Center for Biotechnology Information", 
              "id": "https://www.grid.ac/institutes/grid.419234.9", 
              "name": [
                "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, 20894, Bethesda, MD, USA"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Anantharaman", 
            "givenName": "Vivek", 
            "id": "sg:person.0673016603.16", 
            "sameAs": [
              "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.0673016603.16"
            ], 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "National Center for Biotechnology Information", 
              "id": "https://www.grid.ac/institutes/grid.419234.9", 
              "name": [
                "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, 20894, Bethesda, MD, USA"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Makarova", 
            "givenName": "Kira S", 
            "id": "sg:person.0676725351.01", 
            "sameAs": [
              "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.0676725351.01"
            ], 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "National Center for Biotechnology Information", 
              "id": "https://www.grid.ac/institutes/grid.419234.9", 
              "name": [
                "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, 20894, Bethesda, MD, USA"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Burroughs", 
            "givenName": "A Maxwell", 
            "id": "sg:person.010440663102.58", 
            "sameAs": [
              "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.010440663102.58"
            ], 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "National Center for Biotechnology Information", 
              "id": "https://www.grid.ac/institutes/grid.419234.9", 
              "name": [
                "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, 20894, Bethesda, MD, USA"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Koonin", 
            "givenName": "Eugene V", 
            "id": "sg:person.01017015051.78", 
            "sameAs": [
              "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01017015051.78"
            ], 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "National Center for Biotechnology Information", 
              "id": "https://www.grid.ac/institutes/grid.419234.9", 
              "name": [
                "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, 20894, Bethesda, MD, USA"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Aravind", 
            "givenName": "L", 
            "id": "sg:person.01106662166.38", 
            "sameAs": [
              "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01106662166.38"
            ], 
            "type": "Person"
          }
        ], 
        "citation": [
          {
            "id": "https://doi.org/10.1074/jbc.270.26.15551", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1000323840"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.4161/mge.18477", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1000847096"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1039/c1mb05061c", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1001437973"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1073/pnas.1100186108", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1001834054"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1002/prot.20921", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1002979620"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1074/jbc.m109.062679", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1003556956"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1074/jbc.m111.232884", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1004724011"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1002/prot.24183", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1004853624"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1365-2958.2011.07561.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1004893156"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1365-2958.1995.tb02255.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1005193342"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.3109/10409238.2011.600437", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1005505180"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gkl191", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1005626584"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1365-2958.2007.05688.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1005750486"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/aob/mcr179", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1005958449"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1371/journal.pgen.1001165", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1006159650"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1745-6150-3-8", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1006845773", 
              "https://doi.org/10.1186/1745-6150-3-8"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1365-2958.2010.07175.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1007216054"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1365-2958.2010.07175.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1007216054"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1074/jbc.274.8.4754", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1007274211"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1128/jb.185.12.3624-3635.2003", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1007472841"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/s0968-0004(03)00060-4", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1007596830"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/s0968-0004(03)00060-4", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1007596830"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gkr397", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1008346026"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1420-9101.2009.01876.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1008369175"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1420-9101.2009.01876.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1008369175"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1261/rna.030171.111", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1008705926"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gki408", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1010393487"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gks1086", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1010830910"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1743-422x-7-360", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1011404836", 
              "https://doi.org/10.1186/1743-422x-7-360"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/s0968-0004(98)01274-2", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1011500385"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/s0300-9084(02)01425-6", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1011573123"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gkm993", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1012339407"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gkm993", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1012339407"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.sbi.2006.12.002", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1012392121"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/76443", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1013118779", 
              "https://doi.org/10.1038/76443"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/76443", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1013118779", 
              "https://doi.org/10.1038/76443"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1146/annurev-genet-110410-132430", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1013432136"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nsmb.1896", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1013910559", 
              "https://doi.org/10.1038/nsmb.1896"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nsmb.1896", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1013910559", 
              "https://doi.org/10.1038/nsmb.1896"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1039/c2mb25239b", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1014727669"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/s00438-004-1048-y", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1014923543", 
              "https://doi.org/10.1007/s00438-004-1048-y"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nsmb.1528", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1015177099", 
              "https://doi.org/10.1038/nsmb.1528"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/bioinformatics/14.10.892", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1015350604"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1002/prot.10631", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1015670168"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1745-6150-4-29", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1015797830", 
              "https://doi.org/10.1186/1745-6150-4-29"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.gene.2009.07.006", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1016087100"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nature07661", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1016156713", 
              "https://doi.org/10.1038/nature07661"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gkp985", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1016317136"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/gb-2003-4-12-r81", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1016542336", 
              "https://doi.org/10.1186/gb-2003-4-12-r81"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.molcel.2009.09.020", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1016972851"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/s0092-8674(00)80369-4", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1017028265"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1420-9101.2011.02236.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1017078944"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1002/bies.20474", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1017414835"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/infdis/jis645", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1017566789"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gkr036", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1017746997"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1006/jmbi.2000.4315", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1018016237"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1574-6968.2002.tb11161.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1018579254"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1574-6968.2002.tb11161.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1018579254"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1146/annurev.micro.091208.073214", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1019793505"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1365-2958.2008.06319.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1019993303"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nsmb.1530", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1020229438", 
              "https://doi.org/10.1038/nsmb.1530"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nrmicro2577", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1020345829", 
              "https://doi.org/10.1038/nrmicro2577"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.jmb.2004.03.016", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1021467321"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/s12033-012-9615-7", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1021498571", 
              "https://doi.org/10.1007/s12033-012-9615-7"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1128/jb.05535-11", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1021594947"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nrmicro1235", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1021596942", 
              "https://doi.org/10.1038/nrmicro1235"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nrmicro1235", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1021596942", 
              "https://doi.org/10.1038/nrmicro1235"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1128/mmbr.65.1.44-79.2001", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1021785027"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/29.3.638", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1021901623"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1534/genetics.104.033290", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1022080215"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1534/genetics.104.033290", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1022080215"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1126/science.1192276", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1022616074"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/bioinformatics/btg008", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1023659156"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1101/gr.10.8.1204", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1024524090"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.tim.2009.01.003", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1024707369"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.jmb.2005.06.071", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1024784078"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/27.7.1609", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1025096472"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1745-6150-4-19", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1025245856", 
              "https://doi.org/10.1186/1745-6150-4-19"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.molcel.2010.04.001", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1025264270"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/s0968-0004(00)01577-2", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1025754251"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1073/pnas.0914231107", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1026260219"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.3389/fphys.2011.00048", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1026441424"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.mib.2005.06.006", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1026784324"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1365-2958.2008.06387.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1026965437"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1128/aem.02967-08", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1027449386"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.celrep.2012.11.018", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1028027785"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1371/journal.pbio.1000008", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1028047698"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nrmicro2651", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1028527851", 
              "https://doi.org/10.1038/nrmicro2651"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/dnares/dsq027", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1028590364"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/dnares/dsq027", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1028590364"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gks593", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1029265593"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gkl195", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1029887831"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1101/gad.203786.112", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1031514354"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.jmb.2011.06.016", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1031782751"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1126/science.1129631", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1032711097"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.jmb.2010.05.023", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1032753327"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.3389/fcimb.2012.00089", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1032935679"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/jxb/erg045", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1033992296"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/26.18.4205", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1034175495"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.cell.2007.10.057", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1034409085"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1759-8753-2-6", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1034482592", 
              "https://doi.org/10.1186/1759-8753-2-6"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1002/9780470123089.ch2", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1035223982"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nrmicro2315", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1035378322", 
              "https://doi.org/10.1038/nrmicro2315"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nrmicro2315", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1035378322", 
              "https://doi.org/10.1038/nrmicro2315"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1745-6150-5-13", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1035652165", 
              "https://doi.org/10.1186/1745-6150-5-13"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/gkq1283", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1035831116"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1126/science.291.5507.1279", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1036053511"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1745-6150-6-38", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1036092892", 
              "https://doi.org/10.1186/1745-6150-6-38"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1101/gr.174302", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1036137080"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1073/pnas.0601708103", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1036418126"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1128/jb.06248-11", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1036476616"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1128/mmbr.00036-06", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1036908654"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1002/pro.85", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1037865434"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1134/s0006297910010013", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1038699984", 
              "https://doi.org/10.1134/s0006297910010013"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.febslet.2011.05.064", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1039182392"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1139/w2012-025", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1039271746"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.virol.2012.02.008", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1039490934"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1126/science.278.5338.631", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1039646901"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1110/ps.8.8.1714", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1039923607"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1745-6150-7-18", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1040385591", 
              "https://doi.org/10.1186/1745-6150-7-18"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1471-2105-5-113", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1040413794", 
              "https://doi.org/10.1186/1471-2105-5-113"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/s0968-0004(98)01293-6", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1040470540"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/28.18.3417", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1040509484"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1074/jbc.274.29.20688", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1040737580"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1046/j.1365-2958.1996.371896.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1041333589"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1098/rspb.2011.1465", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1041743914"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/bioinformatics/btq675", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1041937331"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1534/genetics.110.121798", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1042169203"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1534/genetics.110.121798", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1042169203"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/s0092-8674(02)01282-5", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1042837565"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1074/jbc.m501160200", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1043120716"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/s0079-6603(08)00812-x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1043248781"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/s0076-6879(01)41142-6", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1044149920"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/30.7.1427", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1044919398"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1101/gr.2596504", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1044936424"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/s0968-0004(00)89070-2", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1045528087"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1046/j.1365-2958.2002.02896.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1045718405"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1745-6150-7-40", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1046031735", 
              "https://doi.org/10.1186/1745-6150-7-40"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/j.1365-2958.2012.07975.x", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1046365007"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1128/mcb.06019-11", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1046678221"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/nar/25.17.3389", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1047265454"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1101/gr.10.8.1074", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1047615307"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.coi.2011.10.005", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1047661115"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nature08058", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1048444853", 
              "https://doi.org/10.1038/nature08058"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nature08058", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1048444853", 
              "https://doi.org/10.1038/nature08058"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1073/pnas.0914470107", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1048450700"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.mrfmmm.2011.02.001", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1049195291"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nri2824", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1049682044", 
              "https://doi.org/10.1038/nri2824"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nri2824", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1049682044", 
              "https://doi.org/10.1038/nri2824"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1038/emboj.2008.97", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1049768623"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.3389/fimmu.2012.00136", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1049775115"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1111/1574-6968.12074", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1050146911"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/978-1-61779-139-0_19", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1050221138", 
              "https://doi.org/10.1007/978-1-61779-139-0_19"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1261/rna.2172105", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1050412789"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1098/rspb.2002.2227", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1050471248"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1002/wrna.78", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1050736106"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1006/jmbi.2001.5378", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1050919613"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/0020-0190(89)90102-6", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1051569339"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/0020-0190(89)90102-6", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1051569339"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.4161/cc.22068", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1052062569"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.4161/cc.22068", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1052062569"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1093/bioinformatics/btn507", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1052701181"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1002/stem.1237", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1052840081"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1016/j.jmb.2004.08.023", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1052911194"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1471-2105-11-431", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1053037263", 
              "https://doi.org/10.1186/1471-2105-11-431"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/978-1-60327-853-9_6", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1053535104", 
              "https://doi.org/10.1007/978-1-60327-853-9_6"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/978-1-60327-853-9_6", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1053535104", 
              "https://doi.org/10.1007/978-1-60327-853-9_6"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1101/gr.133850.111", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1053660193"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1021/bi015687u", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1055194890"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1021/bi015687u", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1055194890"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1021/cb200231c", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1055226019"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1089/jir.2010.0120", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1059281241"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.1128/jb.177.16.4681-4689.1995", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1062724032"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.2174/1389557043403891", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1069182442"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.4161/rna.3.1.2548", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1072310312"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://doi.org/10.4161/rna.8.2.15196", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1072310657"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "https://app.dimensions.ai/details/publication/pub.1076761104", 
            "type": "CreativeWork"
          }
        ], 
        "datePublished": "2013-12", 
        "datePublishedReg": "2013-12-01", 
        "description": "BACKGROUND: The major role of enzymatic toxins that target nucleic acids in biological conflicts at all levels has become increasingly apparent thanks in large part to the advances of comparative genomics. Typically, toxins evolve rapidly hampering the identification of these proteins by sequence analysis. Here we analyze an unexpectedly widespread superfamily of toxin domains most of which possess RNase activity.\nRESULTS: The HEPN superfamily is comprised of all \u03b1-helical domains that were first identified as being associated with DNA polymerase \u03b2-type nucleotidyltransferases in prokaryotes and animal Sacsin proteins. Using sensitive sequence and structure comparison methods, we vastly extend the HEPN superfamily by identifying numerous novel families and by detecting diverged HEPN domains in several known protein families. The new HEPN families include the RNase LS and LsoA catalytic domains, KEN domains (e.g. RNaseL and Ire1) and the RNase domains of RloC and PrrC. The majority of HEPN domains contain conserved motifs that constitute a metal-independent endoRNase active site. Some HEPN domains lacking this motif probably function as non-catalytic RNA-binding domains, such as in the case of the mannitol repressor MtlR. Our analysis shows that HEPN domains function as toxins that are shared by numerous systems implicated in intra-genomic, inter-genomic and intra-organismal conflicts across the three domains of cellular life. In prokaryotes HEPN domains are essential components of numerous toxin-antitoxin (TA) and abortive infection (Abi) systems and in addition are tightly associated with many restriction-modification (R-M) and CRISPR-Cas systems, and occasionally with other defense systems such as Pgl and Ter. We present evidence of multiple modes of action of HEPN domains in these systems, which include direct attack on viral RNAs (e.g. LsoA and RNase LS) in conjunction with other RNase domains (e.g. a novel RNase H fold domain, NamA), suicidal or dormancy-inducing attack on self RNAs (RM systems and possibly CRISPR-Cas systems), and suicidal attack coupled with direct interaction with phage components (Abi systems). These findings are compatible with the hypothesis on coupling of pathogen-targeting (immunity) and self-directed (programmed cell death and dormancy induction) responses in the evolution of robust antiviral strategies. We propose that altruistic cell suicide mediated by HEPN domains and other functionally similar RNases was essential for the evolution of kin and group selection and cell cooperation. HEPN domains were repeatedly acquired by eukaryotes and incorporated into several core functions such as endonucleolytic processing of the 5.8S-25S/28S rRNA precursor (Las1), a novel ER membrane-associated RNA degradation system (C6orf70), sensing of unprocessed transcripts at the nuclear periphery (Swt1). Multiple lines of evidence suggest that, similar to prokaryotes, HEPN proteins were recruited to antiviral, antitransposon, apoptotic systems or RNA-level response to unfolded proteins (Sacsin and KEN domains) in several groups of eukaryotes.\nCONCLUSIONS: Extensive sequence and structure comparisons reveal unexpectedly broad presence of the HEPN domain in an enormous variety of defense and stress response systems across the tree of life. In addition, HEPN domains have been recruited to perform essential functions, in particular in eukaryotic rRNA processing. These findings are expected to stimulate experiments that could shed light on diverse cellular processes across the three domains of life.\nREVIEWERS: This article was reviewed by Martijn Huynen, Igor Zhulin and Nick Grishin.", 
        "genre": "research_article", 
        "id": "sg:pub.10.1186/1745-6150-8-15", 
        "inLanguage": [
          "en"
        ], 
        "isAccessibleForFree": true, 
        "isFundedItemOf": [
          {
            "id": "sg:grant.2726065", 
            "type": "MonetaryGrant"
          }, 
          {
            "id": "sg:grant.2726029", 
            "type": "MonetaryGrant"
          }
        ], 
        "isPartOf": [
          {
            "id": "sg:journal.1036001", 
            "issn": [
              "1745-6150"
            ], 
            "name": "Biology Direct", 
            "type": "Periodical"
          }, 
          {
            "issueNumber": "1", 
            "type": "PublicationIssue"
          }, 
          {
            "type": "PublicationVolume", 
            "volumeNumber": "8"
          }
        ], 
        "name": "Comprehensive analysis of the HEPN superfamily: identification of novel roles in intra-genomic conflicts, defense, pathogenesis and RNA processing", 
        "pagination": "15", 
        "productId": [
          {
            "name": "readcube_id", 
            "type": "PropertyValue", 
            "value": [
              "a253f351d1e48796041403cf7982f0e4e3e7efb25f055b1184750c94ff9e6632"
            ]
          }, 
          {
            "name": "pubmed_id", 
            "type": "PropertyValue", 
            "value": [
              "23768067"
            ]
          }, 
          {
            "name": "nlm_unique_id", 
            "type": "PropertyValue", 
            "value": [
              "101258412"
            ]
          }, 
          {
            "name": "doi", 
            "type": "PropertyValue", 
            "value": [
              "10.1186/1745-6150-8-15"
            ]
          }, 
          {
            "name": "dimensions_id", 
            "type": "PropertyValue", 
            "value": [
              "pub.1034075663"
            ]
          }
        ], 
        "sameAs": [
          "https://doi.org/10.1186/1745-6150-8-15", 
          "https://app.dimensions.ai/details/publication/pub.1034075663"
        ], 
        "sdDataset": "articles", 
        "sdDatePublished": "2019-04-10T23:24", 
        "sdLicense": "https://scigraph.springernature.com/explorer/license/", 
        "sdPublisher": {
          "name": "Springer Nature - SN SciGraph project", 
          "type": "Organization"
        }, 
        "sdSource": "s3://com-uberresearch-data-dimensions-target-20181106-alternative/cleanup/v134/2549eaecd7973599484d7c17b260dba0a4ecb94b/merge/v9/a6c9fde33151104705d4d7ff012ea9563521a3ce/jats-lookup/v90/0000000001_0000000264/records_8693_00000514.jsonl", 
        "type": "ScholarlyArticle", 
        "url": "http://link.springer.com/10.1186%2F1745-6150-8-15"
      }
    ]
     

    Download the RDF metadata as:  json-ld nt turtle xml License info

    HOW TO GET THIS DATA PROGRAMMATICALLY:

    JSON-LD is a popular format for linked data which is fully compatible with JSON.

    curl -H 'Accept: application/ld+json' 'https://scigraph.springernature.com/pub.10.1186/1745-6150-8-15'

    N-Triples is a line-based linked data format ideal for batch operations.

    curl -H 'Accept: application/n-triples' 'https://scigraph.springernature.com/pub.10.1186/1745-6150-8-15'

    Turtle is a human-readable linked data format.

    curl -H 'Accept: text/turtle' 'https://scigraph.springernature.com/pub.10.1186/1745-6150-8-15'

    RDF/XML is a standard XML format for linked data.

    curl -H 'Accept: application/rdf+xml' 'https://scigraph.springernature.com/pub.10.1186/1745-6150-8-15'


     

    This table displays all metadata directly associated to this object as RDF triples.

    628 TRIPLES      21 PREDICATES      194 URIs      27 LITERALS      15 BLANK NODES

    Subject Predicate Object
    1 sg:pub.10.1186/1745-6150-8-15 schema:about N0aa832e1515d4b80b9316cc85fd6d967
    2 N20d7c9ed08344e6192fbeab2281c04e0
    3 N235c1d4fb9e64f8f8ed47a0a3bfc8c79
    4 N5d471ee6e5934e08b38708e6891372d5
    5 N7c3a4fececb6407a9d67dccea048e6e4
    6 N9643a8e15a63419ab1fb90a35aadb558
    7 anzsrc-for:06
    8 anzsrc-for:0604
    9 schema:author N4ef9bcd03aa64e68bf6eba37f10415b7
    10 schema:citation sg:pub.10.1007/978-1-60327-853-9_6
    11 sg:pub.10.1007/978-1-61779-139-0_19
    12 sg:pub.10.1007/s00438-004-1048-y
    13 sg:pub.10.1007/s12033-012-9615-7
    14 sg:pub.10.1038/76443
    15 sg:pub.10.1038/nature07661
    16 sg:pub.10.1038/nature08058
    17 sg:pub.10.1038/nri2824
    18 sg:pub.10.1038/nrmicro1235
    19 sg:pub.10.1038/nrmicro2315
    20 sg:pub.10.1038/nrmicro2577
    21 sg:pub.10.1038/nrmicro2651
    22 sg:pub.10.1038/nsmb.1528
    23 sg:pub.10.1038/nsmb.1530
    24 sg:pub.10.1038/nsmb.1896
    25 sg:pub.10.1134/s0006297910010013
    26 sg:pub.10.1186/1471-2105-11-431
    27 sg:pub.10.1186/1471-2105-5-113
    28 sg:pub.10.1186/1743-422x-7-360
    29 sg:pub.10.1186/1745-6150-3-8
    30 sg:pub.10.1186/1745-6150-4-19
    31 sg:pub.10.1186/1745-6150-4-29
    32 sg:pub.10.1186/1745-6150-5-13
    33 sg:pub.10.1186/1745-6150-6-38
    34 sg:pub.10.1186/1745-6150-7-18
    35 sg:pub.10.1186/1745-6150-7-40
    36 sg:pub.10.1186/1759-8753-2-6
    37 sg:pub.10.1186/gb-2003-4-12-r81
    38 https://app.dimensions.ai/details/publication/pub.1076761104
    39 https://doi.org/10.1002/9780470123089.ch2
    40 https://doi.org/10.1002/bies.20474
    41 https://doi.org/10.1002/pro.85
    42 https://doi.org/10.1002/prot.10631
    43 https://doi.org/10.1002/prot.20921
    44 https://doi.org/10.1002/prot.24183
    45 https://doi.org/10.1002/stem.1237
    46 https://doi.org/10.1002/wrna.78
    47 https://doi.org/10.1006/jmbi.2000.4315
    48 https://doi.org/10.1006/jmbi.2001.5378
    49 https://doi.org/10.1016/0020-0190(89)90102-6
    50 https://doi.org/10.1016/j.cell.2007.10.057
    51 https://doi.org/10.1016/j.celrep.2012.11.018
    52 https://doi.org/10.1016/j.coi.2011.10.005
    53 https://doi.org/10.1016/j.febslet.2011.05.064
    54 https://doi.org/10.1016/j.gene.2009.07.006
    55 https://doi.org/10.1016/j.jmb.2004.03.016
    56 https://doi.org/10.1016/j.jmb.2004.08.023
    57 https://doi.org/10.1016/j.jmb.2005.06.071
    58 https://doi.org/10.1016/j.jmb.2010.05.023
    59 https://doi.org/10.1016/j.jmb.2011.06.016
    60 https://doi.org/10.1016/j.mib.2005.06.006
    61 https://doi.org/10.1016/j.molcel.2009.09.020
    62 https://doi.org/10.1016/j.molcel.2010.04.001
    63 https://doi.org/10.1016/j.mrfmmm.2011.02.001
    64 https://doi.org/10.1016/j.sbi.2006.12.002
    65 https://doi.org/10.1016/j.tim.2009.01.003
    66 https://doi.org/10.1016/j.virol.2012.02.008
    67 https://doi.org/10.1016/s0076-6879(01)41142-6
    68 https://doi.org/10.1016/s0079-6603(08)00812-x
    69 https://doi.org/10.1016/s0092-8674(00)80369-4
    70 https://doi.org/10.1016/s0092-8674(02)01282-5
    71 https://doi.org/10.1016/s0300-9084(02)01425-6
    72 https://doi.org/10.1016/s0968-0004(00)01577-2
    73 https://doi.org/10.1016/s0968-0004(00)89070-2
    74 https://doi.org/10.1016/s0968-0004(03)00060-4
    75 https://doi.org/10.1016/s0968-0004(98)01274-2
    76 https://doi.org/10.1016/s0968-0004(98)01293-6
    77 https://doi.org/10.1021/bi015687u
    78 https://doi.org/10.1021/cb200231c
    79 https://doi.org/10.1038/emboj.2008.97
    80 https://doi.org/10.1039/c1mb05061c
    81 https://doi.org/10.1039/c2mb25239b
    82 https://doi.org/10.1046/j.1365-2958.1996.371896.x
    83 https://doi.org/10.1046/j.1365-2958.2002.02896.x
    84 https://doi.org/10.1073/pnas.0601708103
    85 https://doi.org/10.1073/pnas.0914231107
    86 https://doi.org/10.1073/pnas.0914470107
    87 https://doi.org/10.1073/pnas.1100186108
    88 https://doi.org/10.1074/jbc.270.26.15551
    89 https://doi.org/10.1074/jbc.274.29.20688
    90 https://doi.org/10.1074/jbc.274.8.4754
    91 https://doi.org/10.1074/jbc.m109.062679
    92 https://doi.org/10.1074/jbc.m111.232884
    93 https://doi.org/10.1074/jbc.m501160200
    94 https://doi.org/10.1089/jir.2010.0120
    95 https://doi.org/10.1093/aob/mcr179
    96 https://doi.org/10.1093/bioinformatics/14.10.892
    97 https://doi.org/10.1093/bioinformatics/btg008
    98 https://doi.org/10.1093/bioinformatics/btn507
    99 https://doi.org/10.1093/bioinformatics/btq675
    100 https://doi.org/10.1093/dnares/dsq027
    101 https://doi.org/10.1093/infdis/jis645
    102 https://doi.org/10.1093/jxb/erg045
    103 https://doi.org/10.1093/nar/25.17.3389
    104 https://doi.org/10.1093/nar/26.18.4205
    105 https://doi.org/10.1093/nar/27.7.1609
    106 https://doi.org/10.1093/nar/28.18.3417
    107 https://doi.org/10.1093/nar/29.3.638
    108 https://doi.org/10.1093/nar/30.7.1427
    109 https://doi.org/10.1093/nar/gki408
    110 https://doi.org/10.1093/nar/gkl191
    111 https://doi.org/10.1093/nar/gkl195
    112 https://doi.org/10.1093/nar/gkm993
    113 https://doi.org/10.1093/nar/gkp985
    114 https://doi.org/10.1093/nar/gkq1283
    115 https://doi.org/10.1093/nar/gkr036
    116 https://doi.org/10.1093/nar/gkr397
    117 https://doi.org/10.1093/nar/gks1086
    118 https://doi.org/10.1093/nar/gks593
    119 https://doi.org/10.1098/rspb.2002.2227
    120 https://doi.org/10.1098/rspb.2011.1465
    121 https://doi.org/10.1101/gad.203786.112
    122 https://doi.org/10.1101/gr.10.8.1074
    123 https://doi.org/10.1101/gr.10.8.1204
    124 https://doi.org/10.1101/gr.133850.111
    125 https://doi.org/10.1101/gr.174302
    126 https://doi.org/10.1101/gr.2596504
    127 https://doi.org/10.1110/ps.8.8.1714
    128 https://doi.org/10.1111/1574-6968.12074
    129 https://doi.org/10.1111/j.1365-2958.1995.tb02255.x
    130 https://doi.org/10.1111/j.1365-2958.2007.05688.x
    131 https://doi.org/10.1111/j.1365-2958.2008.06319.x
    132 https://doi.org/10.1111/j.1365-2958.2008.06387.x
    133 https://doi.org/10.1111/j.1365-2958.2010.07175.x
    134 https://doi.org/10.1111/j.1365-2958.2011.07561.x
    135 https://doi.org/10.1111/j.1365-2958.2012.07975.x
    136 https://doi.org/10.1111/j.1420-9101.2009.01876.x
    137 https://doi.org/10.1111/j.1420-9101.2011.02236.x
    138 https://doi.org/10.1111/j.1574-6968.2002.tb11161.x
    139 https://doi.org/10.1126/science.1129631
    140 https://doi.org/10.1126/science.1192276
    141 https://doi.org/10.1126/science.278.5338.631
    142 https://doi.org/10.1126/science.291.5507.1279
    143 https://doi.org/10.1128/aem.02967-08
    144 https://doi.org/10.1128/jb.05535-11
    145 https://doi.org/10.1128/jb.06248-11
    146 https://doi.org/10.1128/jb.177.16.4681-4689.1995
    147 https://doi.org/10.1128/jb.185.12.3624-3635.2003
    148 https://doi.org/10.1128/mcb.06019-11
    149 https://doi.org/10.1128/mmbr.00036-06
    150 https://doi.org/10.1128/mmbr.65.1.44-79.2001
    151 https://doi.org/10.1139/w2012-025
    152 https://doi.org/10.1146/annurev-genet-110410-132430
    153 https://doi.org/10.1146/annurev.micro.091208.073214
    154 https://doi.org/10.1261/rna.030171.111
    155 https://doi.org/10.1261/rna.2172105
    156 https://doi.org/10.1371/journal.pbio.1000008
    157 https://doi.org/10.1371/journal.pgen.1001165
    158 https://doi.org/10.1534/genetics.104.033290
    159 https://doi.org/10.1534/genetics.110.121798
    160 https://doi.org/10.2174/1389557043403891
    161 https://doi.org/10.3109/10409238.2011.600437
    162 https://doi.org/10.3389/fcimb.2012.00089
    163 https://doi.org/10.3389/fimmu.2012.00136
    164 https://doi.org/10.3389/fphys.2011.00048
    165 https://doi.org/10.4161/cc.22068
    166 https://doi.org/10.4161/mge.18477
    167 https://doi.org/10.4161/rna.3.1.2548
    168 https://doi.org/10.4161/rna.8.2.15196
    169 schema:datePublished 2013-12
    170 schema:datePublishedReg 2013-12-01
    171 schema:description BACKGROUND: The major role of enzymatic toxins that target nucleic acids in biological conflicts at all levels has become increasingly apparent thanks in large part to the advances of comparative genomics. Typically, toxins evolve rapidly hampering the identification of these proteins by sequence analysis. Here we analyze an unexpectedly widespread superfamily of toxin domains most of which possess RNase activity. RESULTS: The HEPN superfamily is comprised of all α-helical domains that were first identified as being associated with DNA polymerase β-type nucleotidyltransferases in prokaryotes and animal Sacsin proteins. Using sensitive sequence and structure comparison methods, we vastly extend the HEPN superfamily by identifying numerous novel families and by detecting diverged HEPN domains in several known protein families. The new HEPN families include the RNase LS and LsoA catalytic domains, KEN domains (e.g. RNaseL and Ire1) and the RNase domains of RloC and PrrC. The majority of HEPN domains contain conserved motifs that constitute a metal-independent endoRNase active site. Some HEPN domains lacking this motif probably function as non-catalytic RNA-binding domains, such as in the case of the mannitol repressor MtlR. Our analysis shows that HEPN domains function as toxins that are shared by numerous systems implicated in intra-genomic, inter-genomic and intra-organismal conflicts across the three domains of cellular life. In prokaryotes HEPN domains are essential components of numerous toxin-antitoxin (TA) and abortive infection (Abi) systems and in addition are tightly associated with many restriction-modification (R-M) and CRISPR-Cas systems, and occasionally with other defense systems such as Pgl and Ter. We present evidence of multiple modes of action of HEPN domains in these systems, which include direct attack on viral RNAs (e.g. LsoA and RNase LS) in conjunction with other RNase domains (e.g. a novel RNase H fold domain, NamA), suicidal or dormancy-inducing attack on self RNAs (RM systems and possibly CRISPR-Cas systems), and suicidal attack coupled with direct interaction with phage components (Abi systems). These findings are compatible with the hypothesis on coupling of pathogen-targeting (immunity) and self-directed (programmed cell death and dormancy induction) responses in the evolution of robust antiviral strategies. We propose that altruistic cell suicide mediated by HEPN domains and other functionally similar RNases was essential for the evolution of kin and group selection and cell cooperation. HEPN domains were repeatedly acquired by eukaryotes and incorporated into several core functions such as endonucleolytic processing of the 5.8S-25S/28S rRNA precursor (Las1), a novel ER membrane-associated RNA degradation system (C6orf70), sensing of unprocessed transcripts at the nuclear periphery (Swt1). Multiple lines of evidence suggest that, similar to prokaryotes, HEPN proteins were recruited to antiviral, antitransposon, apoptotic systems or RNA-level response to unfolded proteins (Sacsin and KEN domains) in several groups of eukaryotes. CONCLUSIONS: Extensive sequence and structure comparisons reveal unexpectedly broad presence of the HEPN domain in an enormous variety of defense and stress response systems across the tree of life. In addition, HEPN domains have been recruited to perform essential functions, in particular in eukaryotic rRNA processing. These findings are expected to stimulate experiments that could shed light on diverse cellular processes across the three domains of life. REVIEWERS: This article was reviewed by Martijn Huynen, Igor Zhulin and Nick Grishin.
    172 schema:genre research_article
    173 schema:inLanguage en
    174 schema:isAccessibleForFree true
    175 schema:isPartOf N5e3b64bbc94f48ac877d99ab9954bd22
    176 Nd8cd2b20406b4f8ab1a580b1a4a74ad3
    177 sg:journal.1036001
    178 schema:name Comprehensive analysis of the HEPN superfamily: identification of novel roles in intra-genomic conflicts, defense, pathogenesis and RNA processing
    179 schema:pagination 15
    180 schema:productId N3568ee66c49d48daa7c579052a15d78e
    181 N8c1046ac5a9e478e941a8094eed3f7d6
    182 Na7fd5011bdfa42898819f7614b449310
    183 Nbdf3be43aafc480799321873cc18dd19
    184 Nd2d3a92cc76e457499dbdc0cf8a9c961
    185 schema:sameAs https://app.dimensions.ai/details/publication/pub.1034075663
    186 https://doi.org/10.1186/1745-6150-8-15
    187 schema:sdDatePublished 2019-04-10T23:24
    188 schema:sdLicense https://scigraph.springernature.com/explorer/license/
    189 schema:sdPublisher N89aa6a252d5b48e5996193fa34bd62e3
    190 schema:url http://link.springer.com/10.1186%2F1745-6150-8-15
    191 sgo:license sg:explorer/license/
    192 sgo:sdDataset articles
    193 rdf:type schema:ScholarlyArticle
    194 N0aa832e1515d4b80b9316cc85fd6d967 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    195 schema:name Toxins, Biological
    196 rdf:type schema:DefinedTerm
    197 N20d7c9ed08344e6192fbeab2281c04e0 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    198 schema:name Genomics
    199 rdf:type schema:DefinedTerm
    200 N2192c6f03a6d44d4ac728937784aeab0 rdf:first sg:person.01017015051.78
    201 rdf:rest N2ec8aa52f93f4251a4b4fbfbf7ea9ae0
    202 N235c1d4fb9e64f8f8ed47a0a3bfc8c79 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    203 schema:name Prokaryotic Cells
    204 rdf:type schema:DefinedTerm
    205 N2ec8aa52f93f4251a4b4fbfbf7ea9ae0 rdf:first sg:person.01106662166.38
    206 rdf:rest rdf:nil
    207 N3568ee66c49d48daa7c579052a15d78e schema:name pubmed_id
    208 schema:value 23768067
    209 rdf:type schema:PropertyValue
    210 N4ef9bcd03aa64e68bf6eba37f10415b7 rdf:first sg:person.0673016603.16
    211 rdf:rest Naf0ffaf0132345a0ab6c30b63a6e693c
    212 N5d471ee6e5934e08b38708e6891372d5 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    213 schema:name RNA
    214 rdf:type schema:DefinedTerm
    215 N5e3b64bbc94f48ac877d99ab9954bd22 schema:volumeNumber 8
    216 rdf:type schema:PublicationVolume
    217 N7c3a4fececb6407a9d67dccea048e6e4 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    218 schema:name Protein Structure, Tertiary
    219 rdf:type schema:DefinedTerm
    220 N89aa6a252d5b48e5996193fa34bd62e3 schema:name Springer Nature - SN SciGraph project
    221 rdf:type schema:Organization
    222 N8c1046ac5a9e478e941a8094eed3f7d6 schema:name dimensions_id
    223 schema:value pub.1034075663
    224 rdf:type schema:PropertyValue
    225 N9643a8e15a63419ab1fb90a35aadb558 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    226 schema:name Ribonucleases
    227 rdf:type schema:DefinedTerm
    228 Na7fd5011bdfa42898819f7614b449310 schema:name doi
    229 schema:value 10.1186/1745-6150-8-15
    230 rdf:type schema:PropertyValue
    231 Naf0ffaf0132345a0ab6c30b63a6e693c rdf:first sg:person.0676725351.01
    232 rdf:rest Necd745f1e7094187830cf49a384c5633
    233 Nbdf3be43aafc480799321873cc18dd19 schema:name readcube_id
    234 schema:value a253f351d1e48796041403cf7982f0e4e3e7efb25f055b1184750c94ff9e6632
    235 rdf:type schema:PropertyValue
    236 Nd2d3a92cc76e457499dbdc0cf8a9c961 schema:name nlm_unique_id
    237 schema:value 101258412
    238 rdf:type schema:PropertyValue
    239 Nd8cd2b20406b4f8ab1a580b1a4a74ad3 schema:issueNumber 1
    240 rdf:type schema:PublicationIssue
    241 Necd745f1e7094187830cf49a384c5633 rdf:first sg:person.010440663102.58
    242 rdf:rest N2192c6f03a6d44d4ac728937784aeab0
    243 anzsrc-for:06 schema:inDefinedTermSet anzsrc-for:
    244 schema:name Biological Sciences
    245 rdf:type schema:DefinedTerm
    246 anzsrc-for:0604 schema:inDefinedTermSet anzsrc-for:
    247 schema:name Genetics
    248 rdf:type schema:DefinedTerm
    249 sg:grant.2726029 http://pending.schema.org/fundedItem sg:pub.10.1186/1745-6150-8-15
    250 rdf:type schema:MonetaryGrant
    251 sg:grant.2726065 http://pending.schema.org/fundedItem sg:pub.10.1186/1745-6150-8-15
    252 rdf:type schema:MonetaryGrant
    253 sg:journal.1036001 schema:issn 1745-6150
    254 schema:name Biology Direct
    255 rdf:type schema:Periodical
    256 sg:person.01017015051.78 schema:affiliation https://www.grid.ac/institutes/grid.419234.9
    257 schema:familyName Koonin
    258 schema:givenName Eugene V
    259 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01017015051.78
    260 rdf:type schema:Person
    261 sg:person.010440663102.58 schema:affiliation https://www.grid.ac/institutes/grid.419234.9
    262 schema:familyName Burroughs
    263 schema:givenName A Maxwell
    264 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.010440663102.58
    265 rdf:type schema:Person
    266 sg:person.01106662166.38 schema:affiliation https://www.grid.ac/institutes/grid.419234.9
    267 schema:familyName Aravind
    268 schema:givenName L
    269 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01106662166.38
    270 rdf:type schema:Person
    271 sg:person.0673016603.16 schema:affiliation https://www.grid.ac/institutes/grid.419234.9
    272 schema:familyName Anantharaman
    273 schema:givenName Vivek
    274 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.0673016603.16
    275 rdf:type schema:Person
    276 sg:person.0676725351.01 schema:affiliation https://www.grid.ac/institutes/grid.419234.9
    277 schema:familyName Makarova
    278 schema:givenName Kira S
    279 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.0676725351.01
    280 rdf:type schema:Person
    281 sg:pub.10.1007/978-1-60327-853-9_6 schema:sameAs https://app.dimensions.ai/details/publication/pub.1053535104
    282 https://doi.org/10.1007/978-1-60327-853-9_6
    283 rdf:type schema:CreativeWork
    284 sg:pub.10.1007/978-1-61779-139-0_19 schema:sameAs https://app.dimensions.ai/details/publication/pub.1050221138
    285 https://doi.org/10.1007/978-1-61779-139-0_19
    286 rdf:type schema:CreativeWork
    287 sg:pub.10.1007/s00438-004-1048-y schema:sameAs https://app.dimensions.ai/details/publication/pub.1014923543
    288 https://doi.org/10.1007/s00438-004-1048-y
    289 rdf:type schema:CreativeWork
    290 sg:pub.10.1007/s12033-012-9615-7 schema:sameAs https://app.dimensions.ai/details/publication/pub.1021498571
    291 https://doi.org/10.1007/s12033-012-9615-7
    292 rdf:type schema:CreativeWork
    293 sg:pub.10.1038/76443 schema:sameAs https://app.dimensions.ai/details/publication/pub.1013118779
    294 https://doi.org/10.1038/76443
    295 rdf:type schema:CreativeWork
    296 sg:pub.10.1038/nature07661 schema:sameAs https://app.dimensions.ai/details/publication/pub.1016156713
    297 https://doi.org/10.1038/nature07661
    298 rdf:type schema:CreativeWork
    299 sg:pub.10.1038/nature08058 schema:sameAs https://app.dimensions.ai/details/publication/pub.1048444853
    300 https://doi.org/10.1038/nature08058
    301 rdf:type schema:CreativeWork
    302 sg:pub.10.1038/nri2824 schema:sameAs https://app.dimensions.ai/details/publication/pub.1049682044
    303 https://doi.org/10.1038/nri2824
    304 rdf:type schema:CreativeWork
    305 sg:pub.10.1038/nrmicro1235 schema:sameAs https://app.dimensions.ai/details/publication/pub.1021596942
    306 https://doi.org/10.1038/nrmicro1235
    307 rdf:type schema:CreativeWork
    308 sg:pub.10.1038/nrmicro2315 schema:sameAs https://app.dimensions.ai/details/publication/pub.1035378322
    309 https://doi.org/10.1038/nrmicro2315
    310 rdf:type schema:CreativeWork
    311 sg:pub.10.1038/nrmicro2577 schema:sameAs https://app.dimensions.ai/details/publication/pub.1020345829
    312 https://doi.org/10.1038/nrmicro2577
    313 rdf:type schema:CreativeWork
    314 sg:pub.10.1038/nrmicro2651 schema:sameAs https://app.dimensions.ai/details/publication/pub.1028527851
    315 https://doi.org/10.1038/nrmicro2651
    316 rdf:type schema:CreativeWork
    317 sg:pub.10.1038/nsmb.1528 schema:sameAs https://app.dimensions.ai/details/publication/pub.1015177099
    318 https://doi.org/10.1038/nsmb.1528
    319 rdf:type schema:CreativeWork
    320 sg:pub.10.1038/nsmb.1530 schema:sameAs https://app.dimensions.ai/details/publication/pub.1020229438
    321 https://doi.org/10.1038/nsmb.1530
    322 rdf:type schema:CreativeWork
    323 sg:pub.10.1038/nsmb.1896 schema:sameAs https://app.dimensions.ai/details/publication/pub.1013910559
    324 https://doi.org/10.1038/nsmb.1896
    325 rdf:type schema:CreativeWork
    326 sg:pub.10.1134/s0006297910010013 schema:sameAs https://app.dimensions.ai/details/publication/pub.1038699984
    327 https://doi.org/10.1134/s0006297910010013
    328 rdf:type schema:CreativeWork
    329 sg:pub.10.1186/1471-2105-11-431 schema:sameAs https://app.dimensions.ai/details/publication/pub.1053037263
    330 https://doi.org/10.1186/1471-2105-11-431
    331 rdf:type schema:CreativeWork
    332 sg:pub.10.1186/1471-2105-5-113 schema:sameAs https://app.dimensions.ai/details/publication/pub.1040413794
    333 https://doi.org/10.1186/1471-2105-5-113
    334 rdf:type schema:CreativeWork
    335 sg:pub.10.1186/1743-422x-7-360 schema:sameAs https://app.dimensions.ai/details/publication/pub.1011404836
    336 https://doi.org/10.1186/1743-422x-7-360
    337 rdf:type schema:CreativeWork
    338 sg:pub.10.1186/1745-6150-3-8 schema:sameAs https://app.dimensions.ai/details/publication/pub.1006845773
    339 https://doi.org/10.1186/1745-6150-3-8
    340 rdf:type schema:CreativeWork
    341 sg:pub.10.1186/1745-6150-4-19 schema:sameAs https://app.dimensions.ai/details/publication/pub.1025245856
    342 https://doi.org/10.1186/1745-6150-4-19
    343 rdf:type schema:CreativeWork
    344 sg:pub.10.1186/1745-6150-4-29 schema:sameAs https://app.dimensions.ai/details/publication/pub.1015797830
    345 https://doi.org/10.1186/1745-6150-4-29
    346 rdf:type schema:CreativeWork
    347 sg:pub.10.1186/1745-6150-5-13 schema:sameAs https://app.dimensions.ai/details/publication/pub.1035652165
    348 https://doi.org/10.1186/1745-6150-5-13
    349 rdf:type schema:CreativeWork
    350 sg:pub.10.1186/1745-6150-6-38 schema:sameAs https://app.dimensions.ai/details/publication/pub.1036092892
    351 https://doi.org/10.1186/1745-6150-6-38
    352 rdf:type schema:CreativeWork
    353 sg:pub.10.1186/1745-6150-7-18 schema:sameAs https://app.dimensions.ai/details/publication/pub.1040385591
    354 https://doi.org/10.1186/1745-6150-7-18
    355 rdf:type schema:CreativeWork
    356 sg:pub.10.1186/1745-6150-7-40 schema:sameAs https://app.dimensions.ai/details/publication/pub.1046031735
    357 https://doi.org/10.1186/1745-6150-7-40
    358 rdf:type schema:CreativeWork
    359 sg:pub.10.1186/1759-8753-2-6 schema:sameAs https://app.dimensions.ai/details/publication/pub.1034482592
    360 https://doi.org/10.1186/1759-8753-2-6
    361 rdf:type schema:CreativeWork
    362 sg:pub.10.1186/gb-2003-4-12-r81 schema:sameAs https://app.dimensions.ai/details/publication/pub.1016542336
    363 https://doi.org/10.1186/gb-2003-4-12-r81
    364 rdf:type schema:CreativeWork
    365 https://app.dimensions.ai/details/publication/pub.1076761104 schema:CreativeWork
    366 https://doi.org/10.1002/9780470123089.ch2 schema:sameAs https://app.dimensions.ai/details/publication/pub.1035223982
    367 rdf:type schema:CreativeWork
    368 https://doi.org/10.1002/bies.20474 schema:sameAs https://app.dimensions.ai/details/publication/pub.1017414835
    369 rdf:type schema:CreativeWork
    370 https://doi.org/10.1002/pro.85 schema:sameAs https://app.dimensions.ai/details/publication/pub.1037865434
    371 rdf:type schema:CreativeWork
    372 https://doi.org/10.1002/prot.10631 schema:sameAs https://app.dimensions.ai/details/publication/pub.1015670168
    373 rdf:type schema:CreativeWork
    374 https://doi.org/10.1002/prot.20921 schema:sameAs https://app.dimensions.ai/details/publication/pub.1002979620
    375 rdf:type schema:CreativeWork
    376 https://doi.org/10.1002/prot.24183 schema:sameAs https://app.dimensions.ai/details/publication/pub.1004853624
    377 rdf:type schema:CreativeWork
    378 https://doi.org/10.1002/stem.1237 schema:sameAs https://app.dimensions.ai/details/publication/pub.1052840081
    379 rdf:type schema:CreativeWork
    380 https://doi.org/10.1002/wrna.78 schema:sameAs https://app.dimensions.ai/details/publication/pub.1050736106
    381 rdf:type schema:CreativeWork
    382 https://doi.org/10.1006/jmbi.2000.4315 schema:sameAs https://app.dimensions.ai/details/publication/pub.1018016237
    383 rdf:type schema:CreativeWork
    384 https://doi.org/10.1006/jmbi.2001.5378 schema:sameAs https://app.dimensions.ai/details/publication/pub.1050919613
    385 rdf:type schema:CreativeWork
    386 https://doi.org/10.1016/0020-0190(89)90102-6 schema:sameAs https://app.dimensions.ai/details/publication/pub.1051569339
    387 rdf:type schema:CreativeWork
    388 https://doi.org/10.1016/j.cell.2007.10.057 schema:sameAs https://app.dimensions.ai/details/publication/pub.1034409085
    389 rdf:type schema:CreativeWork
    390 https://doi.org/10.1016/j.celrep.2012.11.018 schema:sameAs https://app.dimensions.ai/details/publication/pub.1028027785
    391 rdf:type schema:CreativeWork
    392 https://doi.org/10.1016/j.coi.2011.10.005 schema:sameAs https://app.dimensions.ai/details/publication/pub.1047661115
    393 rdf:type schema:CreativeWork
    394 https://doi.org/10.1016/j.febslet.2011.05.064 schema:sameAs https://app.dimensions.ai/details/publication/pub.1039182392
    395 rdf:type schema:CreativeWork
    396 https://doi.org/10.1016/j.gene.2009.07.006 schema:sameAs https://app.dimensions.ai/details/publication/pub.1016087100
    397 rdf:type schema:CreativeWork
    398 https://doi.org/10.1016/j.jmb.2004.03.016 schema:sameAs https://app.dimensions.ai/details/publication/pub.1021467321
    399 rdf:type schema:CreativeWork
    400 https://doi.org/10.1016/j.jmb.2004.08.023 schema:sameAs https://app.dimensions.ai/details/publication/pub.1052911194
    401 rdf:type schema:CreativeWork
    402 https://doi.org/10.1016/j.jmb.2005.06.071 schema:sameAs https://app.dimensions.ai/details/publication/pub.1024784078
    403 rdf:type schema:CreativeWork
    404 https://doi.org/10.1016/j.jmb.2010.05.023 schema:sameAs https://app.dimensions.ai/details/publication/pub.1032753327
    405 rdf:type schema:CreativeWork
    406 https://doi.org/10.1016/j.jmb.2011.06.016 schema:sameAs https://app.dimensions.ai/details/publication/pub.1031782751
    407 rdf:type schema:CreativeWork
    408 https://doi.org/10.1016/j.mib.2005.06.006 schema:sameAs https://app.dimensions.ai/details/publication/pub.1026784324
    409 rdf:type schema:CreativeWork
    410 https://doi.org/10.1016/j.molcel.2009.09.020 schema:sameAs https://app.dimensions.ai/details/publication/pub.1016972851
    411 rdf:type schema:CreativeWork
    412 https://doi.org/10.1016/j.molcel.2010.04.001 schema:sameAs https://app.dimensions.ai/details/publication/pub.1025264270
    413 rdf:type schema:CreativeWork
    414 https://doi.org/10.1016/j.mrfmmm.2011.02.001 schema:sameAs https://app.dimensions.ai/details/publication/pub.1049195291
    415 rdf:type schema:CreativeWork
    416 https://doi.org/10.1016/j.sbi.2006.12.002 schema:sameAs https://app.dimensions.ai/details/publication/pub.1012392121
    417 rdf:type schema:CreativeWork
    418 https://doi.org/10.1016/j.tim.2009.01.003 schema:sameAs https://app.dimensions.ai/details/publication/pub.1024707369
    419 rdf:type schema:CreativeWork
    420 https://doi.org/10.1016/j.virol.2012.02.008 schema:sameAs https://app.dimensions.ai/details/publication/pub.1039490934
    421 rdf:type schema:CreativeWork
    422 https://doi.org/10.1016/s0076-6879(01)41142-6 schema:sameAs https://app.dimensions.ai/details/publication/pub.1044149920
    423 rdf:type schema:CreativeWork
    424 https://doi.org/10.1016/s0079-6603(08)00812-x schema:sameAs https://app.dimensions.ai/details/publication/pub.1043248781
    425 rdf:type schema:CreativeWork
    426 https://doi.org/10.1016/s0092-8674(00)80369-4 schema:sameAs https://app.dimensions.ai/details/publication/pub.1017028265
    427 rdf:type schema:CreativeWork
    428 https://doi.org/10.1016/s0092-8674(02)01282-5 schema:sameAs https://app.dimensions.ai/details/publication/pub.1042837565
    429 rdf:type schema:CreativeWork
    430 https://doi.org/10.1016/s0300-9084(02)01425-6 schema:sameAs https://app.dimensions.ai/details/publication/pub.1011573123
    431 rdf:type schema:CreativeWork
    432 https://doi.org/10.1016/s0968-0004(00)01577-2 schema:sameAs https://app.dimensions.ai/details/publication/pub.1025754251
    433 rdf:type schema:CreativeWork
    434 https://doi.org/10.1016/s0968-0004(00)89070-2 schema:sameAs https://app.dimensions.ai/details/publication/pub.1045528087
    435 rdf:type schema:CreativeWork
    436 https://doi.org/10.1016/s0968-0004(03)00060-4 schema:sameAs https://app.dimensions.ai/details/publication/pub.1007596830
    437 rdf:type schema:CreativeWork
    438 https://doi.org/10.1016/s0968-0004(98)01274-2 schema:sameAs https://app.dimensions.ai/details/publication/pub.1011500385
    439 rdf:type schema:CreativeWork
    440 https://doi.org/10.1016/s0968-0004(98)01293-6 schema:sameAs https://app.dimensions.ai/details/publication/pub.1040470540
    441 rdf:type schema:CreativeWork
    442 https://doi.org/10.1021/bi015687u schema:sameAs https://app.dimensions.ai/details/publication/pub.1055194890
    443 rdf:type schema:CreativeWork
    444 https://doi.org/10.1021/cb200231c schema:sameAs https://app.dimensions.ai/details/publication/pub.1055226019
    445 rdf:type schema:CreativeWork
    446 https://doi.org/10.1038/emboj.2008.97 schema:sameAs https://app.dimensions.ai/details/publication/pub.1049768623
    447 rdf:type schema:CreativeWork
    448 https://doi.org/10.1039/c1mb05061c schema:sameAs https://app.dimensions.ai/details/publication/pub.1001437973
    449 rdf:type schema:CreativeWork
    450 https://doi.org/10.1039/c2mb25239b schema:sameAs https://app.dimensions.ai/details/publication/pub.1014727669
    451 rdf:type schema:CreativeWork
    452 https://doi.org/10.1046/j.1365-2958.1996.371896.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1041333589
    453 rdf:type schema:CreativeWork
    454 https://doi.org/10.1046/j.1365-2958.2002.02896.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1045718405
    455 rdf:type schema:CreativeWork
    456 https://doi.org/10.1073/pnas.0601708103 schema:sameAs https://app.dimensions.ai/details/publication/pub.1036418126
    457 rdf:type schema:CreativeWork
    458 https://doi.org/10.1073/pnas.0914231107 schema:sameAs https://app.dimensions.ai/details/publication/pub.1026260219
    459 rdf:type schema:CreativeWork
    460 https://doi.org/10.1073/pnas.0914470107 schema:sameAs https://app.dimensions.ai/details/publication/pub.1048450700
    461 rdf:type schema:CreativeWork
    462 https://doi.org/10.1073/pnas.1100186108 schema:sameAs https://app.dimensions.ai/details/publication/pub.1001834054
    463 rdf:type schema:CreativeWork
    464 https://doi.org/10.1074/jbc.270.26.15551 schema:sameAs https://app.dimensions.ai/details/publication/pub.1000323840
    465 rdf:type schema:CreativeWork
    466 https://doi.org/10.1074/jbc.274.29.20688 schema:sameAs https://app.dimensions.ai/details/publication/pub.1040737580
    467 rdf:type schema:CreativeWork
    468 https://doi.org/10.1074/jbc.274.8.4754 schema:sameAs https://app.dimensions.ai/details/publication/pub.1007274211
    469 rdf:type schema:CreativeWork
    470 https://doi.org/10.1074/jbc.m109.062679 schema:sameAs https://app.dimensions.ai/details/publication/pub.1003556956
    471 rdf:type schema:CreativeWork
    472 https://doi.org/10.1074/jbc.m111.232884 schema:sameAs https://app.dimensions.ai/details/publication/pub.1004724011
    473 rdf:type schema:CreativeWork
    474 https://doi.org/10.1074/jbc.m501160200 schema:sameAs https://app.dimensions.ai/details/publication/pub.1043120716
    475 rdf:type schema:CreativeWork
    476 https://doi.org/10.1089/jir.2010.0120 schema:sameAs https://app.dimensions.ai/details/publication/pub.1059281241
    477 rdf:type schema:CreativeWork
    478 https://doi.org/10.1093/aob/mcr179 schema:sameAs https://app.dimensions.ai/details/publication/pub.1005958449
    479 rdf:type schema:CreativeWork
    480 https://doi.org/10.1093/bioinformatics/14.10.892 schema:sameAs https://app.dimensions.ai/details/publication/pub.1015350604
    481 rdf:type schema:CreativeWork
    482 https://doi.org/10.1093/bioinformatics/btg008 schema:sameAs https://app.dimensions.ai/details/publication/pub.1023659156
    483 rdf:type schema:CreativeWork
    484 https://doi.org/10.1093/bioinformatics/btn507 schema:sameAs https://app.dimensions.ai/details/publication/pub.1052701181
    485 rdf:type schema:CreativeWork
    486 https://doi.org/10.1093/bioinformatics/btq675 schema:sameAs https://app.dimensions.ai/details/publication/pub.1041937331
    487 rdf:type schema:CreativeWork
    488 https://doi.org/10.1093/dnares/dsq027 schema:sameAs https://app.dimensions.ai/details/publication/pub.1028590364
    489 rdf:type schema:CreativeWork
    490 https://doi.org/10.1093/infdis/jis645 schema:sameAs https://app.dimensions.ai/details/publication/pub.1017566789
    491 rdf:type schema:CreativeWork
    492 https://doi.org/10.1093/jxb/erg045 schema:sameAs https://app.dimensions.ai/details/publication/pub.1033992296
    493 rdf:type schema:CreativeWork
    494 https://doi.org/10.1093/nar/25.17.3389 schema:sameAs https://app.dimensions.ai/details/publication/pub.1047265454
    495 rdf:type schema:CreativeWork
    496 https://doi.org/10.1093/nar/26.18.4205 schema:sameAs https://app.dimensions.ai/details/publication/pub.1034175495
    497 rdf:type schema:CreativeWork
    498 https://doi.org/10.1093/nar/27.7.1609 schema:sameAs https://app.dimensions.ai/details/publication/pub.1025096472
    499 rdf:type schema:CreativeWork
    500 https://doi.org/10.1093/nar/28.18.3417 schema:sameAs https://app.dimensions.ai/details/publication/pub.1040509484
    501 rdf:type schema:CreativeWork
    502 https://doi.org/10.1093/nar/29.3.638 schema:sameAs https://app.dimensions.ai/details/publication/pub.1021901623
    503 rdf:type schema:CreativeWork
    504 https://doi.org/10.1093/nar/30.7.1427 schema:sameAs https://app.dimensions.ai/details/publication/pub.1044919398
    505 rdf:type schema:CreativeWork
    506 https://doi.org/10.1093/nar/gki408 schema:sameAs https://app.dimensions.ai/details/publication/pub.1010393487
    507 rdf:type schema:CreativeWork
    508 https://doi.org/10.1093/nar/gkl191 schema:sameAs https://app.dimensions.ai/details/publication/pub.1005626584
    509 rdf:type schema:CreativeWork
    510 https://doi.org/10.1093/nar/gkl195 schema:sameAs https://app.dimensions.ai/details/publication/pub.1029887831
    511 rdf:type schema:CreativeWork
    512 https://doi.org/10.1093/nar/gkm993 schema:sameAs https://app.dimensions.ai/details/publication/pub.1012339407
    513 rdf:type schema:CreativeWork
    514 https://doi.org/10.1093/nar/gkp985 schema:sameAs https://app.dimensions.ai/details/publication/pub.1016317136
    515 rdf:type schema:CreativeWork
    516 https://doi.org/10.1093/nar/gkq1283 schema:sameAs https://app.dimensions.ai/details/publication/pub.1035831116
    517 rdf:type schema:CreativeWork
    518 https://doi.org/10.1093/nar/gkr036 schema:sameAs https://app.dimensions.ai/details/publication/pub.1017746997
    519 rdf:type schema:CreativeWork
    520 https://doi.org/10.1093/nar/gkr397 schema:sameAs https://app.dimensions.ai/details/publication/pub.1008346026
    521 rdf:type schema:CreativeWork
    522 https://doi.org/10.1093/nar/gks1086 schema:sameAs https://app.dimensions.ai/details/publication/pub.1010830910
    523 rdf:type schema:CreativeWork
    524 https://doi.org/10.1093/nar/gks593 schema:sameAs https://app.dimensions.ai/details/publication/pub.1029265593
    525 rdf:type schema:CreativeWork
    526 https://doi.org/10.1098/rspb.2002.2227 schema:sameAs https://app.dimensions.ai/details/publication/pub.1050471248
    527 rdf:type schema:CreativeWork
    528 https://doi.org/10.1098/rspb.2011.1465 schema:sameAs https://app.dimensions.ai/details/publication/pub.1041743914
    529 rdf:type schema:CreativeWork
    530 https://doi.org/10.1101/gad.203786.112 schema:sameAs https://app.dimensions.ai/details/publication/pub.1031514354
    531 rdf:type schema:CreativeWork
    532 https://doi.org/10.1101/gr.10.8.1074 schema:sameAs https://app.dimensions.ai/details/publication/pub.1047615307
    533 rdf:type schema:CreativeWork
    534 https://doi.org/10.1101/gr.10.8.1204 schema:sameAs https://app.dimensions.ai/details/publication/pub.1024524090
    535 rdf:type schema:CreativeWork
    536 https://doi.org/10.1101/gr.133850.111 schema:sameAs https://app.dimensions.ai/details/publication/pub.1053660193
    537 rdf:type schema:CreativeWork
    538 https://doi.org/10.1101/gr.174302 schema:sameAs https://app.dimensions.ai/details/publication/pub.1036137080
    539 rdf:type schema:CreativeWork
    540 https://doi.org/10.1101/gr.2596504 schema:sameAs https://app.dimensions.ai/details/publication/pub.1044936424
    541 rdf:type schema:CreativeWork
    542 https://doi.org/10.1110/ps.8.8.1714 schema:sameAs https://app.dimensions.ai/details/publication/pub.1039923607
    543 rdf:type schema:CreativeWork
    544 https://doi.org/10.1111/1574-6968.12074 schema:sameAs https://app.dimensions.ai/details/publication/pub.1050146911
    545 rdf:type schema:CreativeWork
    546 https://doi.org/10.1111/j.1365-2958.1995.tb02255.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1005193342
    547 rdf:type schema:CreativeWork
    548 https://doi.org/10.1111/j.1365-2958.2007.05688.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1005750486
    549 rdf:type schema:CreativeWork
    550 https://doi.org/10.1111/j.1365-2958.2008.06319.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1019993303
    551 rdf:type schema:CreativeWork
    552 https://doi.org/10.1111/j.1365-2958.2008.06387.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1026965437
    553 rdf:type schema:CreativeWork
    554 https://doi.org/10.1111/j.1365-2958.2010.07175.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1007216054
    555 rdf:type schema:CreativeWork
    556 https://doi.org/10.1111/j.1365-2958.2011.07561.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1004893156
    557 rdf:type schema:CreativeWork
    558 https://doi.org/10.1111/j.1365-2958.2012.07975.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1046365007
    559 rdf:type schema:CreativeWork
    560 https://doi.org/10.1111/j.1420-9101.2009.01876.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1008369175
    561 rdf:type schema:CreativeWork
    562 https://doi.org/10.1111/j.1420-9101.2011.02236.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1017078944
    563 rdf:type schema:CreativeWork
    564 https://doi.org/10.1111/j.1574-6968.2002.tb11161.x schema:sameAs https://app.dimensions.ai/details/publication/pub.1018579254
    565 rdf:type schema:CreativeWork
    566 https://doi.org/10.1126/science.1129631 schema:sameAs https://app.dimensions.ai/details/publication/pub.1032711097
    567 rdf:type schema:CreativeWork
    568 https://doi.org/10.1126/science.1192276 schema:sameAs https://app.dimensions.ai/details/publication/pub.1022616074
    569 rdf:type schema:CreativeWork
    570 https://doi.org/10.1126/science.278.5338.631 schema:sameAs https://app.dimensions.ai/details/publication/pub.1039646901
    571 rdf:type schema:CreativeWork
    572 https://doi.org/10.1126/science.291.5507.1279 schema:sameAs https://app.dimensions.ai/details/publication/pub.1036053511
    573 rdf:type schema:CreativeWork
    574 https://doi.org/10.1128/aem.02967-08 schema:sameAs https://app.dimensions.ai/details/publication/pub.1027449386
    575 rdf:type schema:CreativeWork
    576 https://doi.org/10.1128/jb.05535-11 schema:sameAs https://app.dimensions.ai/details/publication/pub.1021594947
    577 rdf:type schema:CreativeWork
    578 https://doi.org/10.1128/jb.06248-11 schema:sameAs https://app.dimensions.ai/details/publication/pub.1036476616
    579 rdf:type schema:CreativeWork
    580 https://doi.org/10.1128/jb.177.16.4681-4689.1995 schema:sameAs https://app.dimensions.ai/details/publication/pub.1062724032
    581 rdf:type schema:CreativeWork
    582 https://doi.org/10.1128/jb.185.12.3624-3635.2003 schema:sameAs https://app.dimensions.ai/details/publication/pub.1007472841
    583 rdf:type schema:CreativeWork
    584 https://doi.org/10.1128/mcb.06019-11 schema:sameAs https://app.dimensions.ai/details/publication/pub.1046678221
    585 rdf:type schema:CreativeWork
    586 https://doi.org/10.1128/mmbr.00036-06 schema:sameAs https://app.dimensions.ai/details/publication/pub.1036908654
    587 rdf:type schema:CreativeWork
    588 https://doi.org/10.1128/mmbr.65.1.44-79.2001 schema:sameAs https://app.dimensions.ai/details/publication/pub.1021785027
    589 rdf:type schema:CreativeWork
    590 https://doi.org/10.1139/w2012-025 schema:sameAs https://app.dimensions.ai/details/publication/pub.1039271746
    591 rdf:type schema:CreativeWork
    592 https://doi.org/10.1146/annurev-genet-110410-132430 schema:sameAs https://app.dimensions.ai/details/publication/pub.1013432136
    593 rdf:type schema:CreativeWork
    594 https://doi.org/10.1146/annurev.micro.091208.073214 schema:sameAs https://app.dimensions.ai/details/publication/pub.1019793505
    595 rdf:type schema:CreativeWork
    596 https://doi.org/10.1261/rna.030171.111 schema:sameAs https://app.dimensions.ai/details/publication/pub.1008705926
    597 rdf:type schema:CreativeWork
    598 https://doi.org/10.1261/rna.2172105 schema:sameAs https://app.dimensions.ai/details/publication/pub.1050412789
    599 rdf:type schema:CreativeWork
    600 https://doi.org/10.1371/journal.pbio.1000008 schema:sameAs https://app.dimensions.ai/details/publication/pub.1028047698
    601 rdf:type schema:CreativeWork
    602 https://doi.org/10.1371/journal.pgen.1001165 schema:sameAs https://app.dimensions.ai/details/publication/pub.1006159650
    603 rdf:type schema:CreativeWork
    604 https://doi.org/10.1534/genetics.104.033290 schema:sameAs https://app.dimensions.ai/details/publication/pub.1022080215
    605 rdf:type schema:CreativeWork
    606 https://doi.org/10.1534/genetics.110.121798 schema:sameAs https://app.dimensions.ai/details/publication/pub.1042169203
    607 rdf:type schema:CreativeWork
    608 https://doi.org/10.2174/1389557043403891 schema:sameAs https://app.dimensions.ai/details/publication/pub.1069182442
    609 rdf:type schema:CreativeWork
    610 https://doi.org/10.3109/10409238.2011.600437 schema:sameAs https://app.dimensions.ai/details/publication/pub.1005505180
    611 rdf:type schema:CreativeWork
    612 https://doi.org/10.3389/fcimb.2012.00089 schema:sameAs https://app.dimensions.ai/details/publication/pub.1032935679
    613 rdf:type schema:CreativeWork
    614 https://doi.org/10.3389/fimmu.2012.00136 schema:sameAs https://app.dimensions.ai/details/publication/pub.1049775115
    615 rdf:type schema:CreativeWork
    616 https://doi.org/10.3389/fphys.2011.00048 schema:sameAs https://app.dimensions.ai/details/publication/pub.1026441424
    617 rdf:type schema:CreativeWork
    618 https://doi.org/10.4161/cc.22068 schema:sameAs https://app.dimensions.ai/details/publication/pub.1052062569
    619 rdf:type schema:CreativeWork
    620 https://doi.org/10.4161/mge.18477 schema:sameAs https://app.dimensions.ai/details/publication/pub.1000847096
    621 rdf:type schema:CreativeWork
    622 https://doi.org/10.4161/rna.3.1.2548 schema:sameAs https://app.dimensions.ai/details/publication/pub.1072310312
    623 rdf:type schema:CreativeWork
    624 https://doi.org/10.4161/rna.8.2.15196 schema:sameAs https://app.dimensions.ai/details/publication/pub.1072310657
    625 rdf:type schema:CreativeWork
    626 https://www.grid.ac/institutes/grid.419234.9 schema:alternateName National Center for Biotechnology Information
    627 schema:name National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, 20894, Bethesda, MD, USA
    628 rdf:type schema:Organization
     




    Preview window. Press ESC to close (or click here)


    ...