Conserved sequence motifs in human TMTC1, TMTC2, TMTC3, and TMTC4, new O-mannosyltransferases from the GT-C/PMT clan, are rationalized as ligand ... View Full Text


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Article Info

DATE

2021-01-12

AUTHORS

Birgit Eisenhaber, Swati Sinha, Chaitanya K. Jadalanki, Vladimir A. Shitov, Qiao Wen Tan, Fernanda L. Sirota, Frank Eisenhaber

ABSTRACT

BACKGROUND: The human proteins TMTC1, TMTC2, TMTC3 and TMTC4 have been experimentally shown to be components of a new O-mannosylation pathway. Their own mannosyl-transferase activity has been suspected but their actual enzymatic potential has not been demonstrated yet. So far, sequence analysis of TMTCs has been compromised by evolutionary sequence divergence within their membrane-embedded N-terminal region, sequence inaccuracies in the protein databases and the difficulty to interpret the large functional variety of known homologous proteins (mostly sugar transferases and some with known 3D structure). RESULTS: Evolutionary conserved molecular function among TMTCs is only possible with conserved membrane topology within their membrane-embedded N-terminal regions leading to the placement of homologous long intermittent loops at the same membrane side. Using this criterion, we demonstrate that all TMTCs have 11 transmembrane regions. The sequence segment homologous to Pfam model DUF1736 is actually just a loop between TM7 and TM8 that is located in the ER lumen and that contains a small hydrophobic, but not membrane-embedded helix. Not only do the membrane-embedded N-terminal regions of TMTCs share a common fold and 3D structural similarity with subgroups of GT-C sugar transferases. The conservation of residues critical for catalysis, for binding of a divalent metal ion and of the phosphate group of a lipid-linked sugar moiety throughout enzymatically and structurally well-studied GT-Cs and sequences of TMTCs indicates that TMTCs are actually sugar-transferring enzymes. We present credible 3D structural models of all four TMTCs (derived from their closest known homologues 5ezm/5f15) and find observed conserved sequence motifs rationalized as binding sites for a metal ion and for a dolichyl-phosphate-mannose moiety. CONCLUSIONS: With the results from both careful sequence analysis and structural modelling, we can conclusively say that the TMTCs are enzymatically active sugar transferases belonging to the GT-C/PMT superfamily. The DUF1736 segment, the loop between TM7 and TM8, is critical for catalysis and lipid-linked sugar moiety binding. Together with the available indirect experimental data, we conclude that the TMTCs are not only part of an O-mannosylation pathway in the endoplasmic reticulum of upper eukaryotes but, actually, they are the sought mannosyl-transferases. More... »

PAGES

4

References to SciGraph publications

  • 2017-07-24. Charged residues next to transmembrane regions revisited: “Positive-inside rule” is complemented by the “negative inside depletion/outside enrichment rule” in BMC BIOLOGY
  • 2020-05-06. Glycobiology and schizophrenia: a biological hypothesis emerging from genomic research in MOLECULAR PSYCHIATRY
  • 2009-10-30. Integrated Tools for Biomolecular Sequence-Based Function Prediction as Exemplified by the ANNOTATOR Software Environment in DATA MINING TECHNIQUES FOR THE LIFE SCIENCES
  • 2018-06-11. A multiethnic genome-wide association study of primary open-angle glaucoma identifies novel risk loci in NATURE COMMUNICATIONS
  • 2013-07-10. Expansive marker analysis replicating the association of glaucoma susceptibility with human chromosome loci 1q43 and 10p12.31 in EUROPEAN JOURNAL OF HUMAN GENETICS
  • 2017-10-23. Molecular basis of lipid-linked oligosaccharide recognition and processing by bacterial oligosaccharyltransferase in NATURE STRUCTURAL & MOLECULAR BIOLOGY
  • 2019-12-18. Genome-wide association study of morbid obesity in Han Chinese in BMC GENETICS
  • 2019-01-21. miRNAs and target genes in the blood as biomarkers for the early diagnosis of Parkinson’s disease in BMC SYSTEMS BIOLOGY
  • 2014-06-02. On the necessity of dissecting sequence similarity scores into segment-specific contributions for inferring protein homology, function prediction and annotation in BMC BIOINFORMATICS
  • 2016-04-27. The Recipe for Protein Sequence-Based Function Prediction and Its Implementation in the ANNOTATOR Software Environment in DATA MINING TECHNIQUES FOR THE LIFE SCIENCES
  • 2019-02-18. SignalP 5.0 improves signal peptide predictions using deep neural networks in NATURE BIOTECHNOLOGY
  • 2013-07-01. Crystal structure of the C-terminal globular domain of the third paralog of the Archaeoglobus fulgidus oligosaccharyltransferases in BMC MOLECULAR AND CELL BIOLOGY
  • 2019-04-15. Integrating transcriptome-wide association study and mRNA expression profiling identifies novel genes associated with bone mineral density in OSTEOPOROSIS INTERNATIONAL
  • 2011-10-25. Not all transmembrane helices are born equal: Towards the extension of the sequence homology concept to membrane proteins in BIOLOGY DIRECT
  • 2011-07-26. A follow-up study for left ventricular mass on chromosome 12p11 identifies potential candidate genes in BMC MEDICAL GENETICS
  • 2012-05-11. Docking performance of the glide program as evaluated on the Astex and DUD datasets: a complete set of glide SP results and selected results for a new scoring function integrating WaterMap and glide in JOURNAL OF COMPUTER-AIDED MOLECULAR DESIGN
  • 2015-08-01. dissectHMMER: a HMMER-based score dissection framework that statistically evaluates fold-critical sequence segments for domain fold similarity in BIOLOGY DIRECT
  • 2015-11-06. Meta-analysis identifies seven susceptibility loci involved in the atopic march in NATURE COMMUNICATIONS
  • 2019-07-08. Structure of the eukaryotic protein O-mannosyltransferase Pmt1–Pmt2 complex in NATURE STRUCTURAL & MOLECULAR BIOLOGY
  • 2017-11-17. Association of Inflammatory Bowel Disease with Arthritis: Evidence from In Silico Gene Expression Patterns and Network Topological Analysis in INTERDISCIPLINARY SCIENCES: COMPUTATIONAL LIFE SCIENCES
  • 2017-08-18. Erratum to: Charged residues next to transmembrane regions revisited: “Positive-inside rule” is complemented by the “negative inside depletion/outside enrichment rule” in BMC BIOLOGY
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  • Identifiers

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    http://scigraph.springernature.com/pub.10.1186/s13062-021-00291-w

    DOI

    http://dx.doi.org/10.1186/s13062-021-00291-w

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1134490967

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/33436046


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