An organelle-specific protein landscape identifies novel diseases and molecular mechanisms View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2016-05-13

AUTHORS

Karsten Boldt, Jeroen van Reeuwijk, Qianhao Lu, Konstantinos Koutroumpas, Thanh-Minh T. Nguyen, Yves Texier, Sylvia E. C. van Beersum, Nicola Horn, Jason R. Willer, Dorus A. Mans, Gerard Dougherty, Ideke J. C. Lamers, Karlien L. M. Coene, Heleen H. Arts, Matthew J. Betts, Tina Beyer, Emine Bolat, Christian Johannes Gloeckner, Khatera Haidari, Lisette Hetterschijt, Daniela Iaconis, Dagan Jenkins, Franziska Klose, Barbara Knapp, Brooke Latour, Stef J. F. Letteboer, Carlo L. Marcelis, Dragana Mitic, Manuela Morleo, Machteld M. Oud, Moniek Riemersma, Susan Rix, Paulien A. Terhal, Grischa Toedt, Teunis J. P. van Dam, Erik de Vrieze, Yasmin Wissinger, Ka Man Wu, Gordana Apic, Philip L. Beales, Oliver E. Blacque, Toby J. Gibson, Martijn A. Huynen, Nicholas Katsanis, Hannie Kremer, Heymut Omran, Erwin van Wijk, Uwe Wolfrum, François Kepes, Erica E. Davis, Brunella Franco, Rachel H. Giles, Marius Ueffing, Robert B. Russell, Ronald Roepman

ABSTRACT

Cellular organelles provide opportunities to relate biological mechanisms to disease. Here we use affinity proteomics, genetics and cell biology to interrogate cilia: poorly understood organelles, where defects cause genetic diseases. Two hundred and seventeen tagged human ciliary proteins create a final landscape of 1,319 proteins, 4,905 interactions and 52 complexes. Reverse tagging, repetition of purifications and statistical analyses, produce a high-resolution network that reveals organelle-specific interactions and complexes not apparent in larger studies, and links vesicle transport, the cytoskeleton, signalling and ubiquitination to ciliary signalling and proteostasis. We observe sub-complexes in exocyst and intraflagellar transport complexes, which we validate biochemically, and by probing structurally predicted, disruptive, genetic variants from ciliary disease patients. The landscape suggests other genetic diseases could be ciliary including 3M syndrome. We show that 3M genes are involved in ciliogenesis, and that patient fibroblasts lack cilia. Overall, this organelle-specific targeting strategy shows considerable promise for Systems Medicine. More... »

PAGES

11491

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  • Journal

    TITLE

    Nature Communications

    ISSUE

    1

    VOLUME

    7

    Author Affiliations

  • Medical Proteome Center, Institute for Ophthalmic Research, University of Tuebingen, 72074, Tuebingen, Germany
  • Department of Human Genetics and Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Geert Grooteplein Zuid 10, 6525 GA, Nijmegen, The Netherlands
  • Cell Networks, Bioquant, Ruprecht-Karl University of Heidelberg, Im Neuenheimer Feld 267, 69120, Heidelberg, Germany
  • Institute of Systems and Synthetic Biology, Genopole, CNRS, Université d’Evry, 91030, Evry, France
  • Department of Molecular Epigenetics, Helmholtz Center Munich, Center for Integrated Protein Science, 81377, Munich, Germany
  • Center for Human Disease Modeling, Duke University, 27701, Durham, North Carolina, USA
  • Department of General Pediatrics, University Children's Hospital Muenster, 48149, Muenster, Germany
  • German Center for Neurodegenerative Diseases (DZNE) within the Helmholz Association, Otfried-Müller Strasse 23, 72076, Tuebingen, Germany
  • Department of Nephrology and Hypertension, Regenerative Medicine Center, University Medical Center Utrecht, 3584 CT, Utrecht, The Netherlands
  • Department of Otorhinolaryngology and Donders Institute for Brain, Cognition and Behaviour, Radboud University Medical Center, Geert Grooteplein Zuid 10, 6525 GA, Nijmegen, The Netherlands
  • Telethon Institute of Genetics and Medicine, 80078, TIGEM, Italy
  • Molecular Medicine Unit and Birth Defects Research Centre, UCL Institute of Child Health, WC1N 1EH, London, UK
  • Cell and Matrix Biology, Inst. of Zoology, Johannes Gutenberg University of Mainz, 55122, Mainz, Germany
  • Cambridge Cell Networks Ltd, St John’s Innovation Centre, Cowley Road, CB4 0WS, Cambridge, UK
  • Department of Translational Medicine Federico II University, 80131, Naples, Italy
  • Department of Genetics, University Medical Center Utrecht, 3584 CX, Utrecht, The Netherlands
  • Structural and Computational Biology Unit, European Molecular Biology Laboratory, Meyerhofstrasse 1, 69117, Heidelberg, Germany
  • Centre for Molecular and Biomolecular Informatics and Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Geert Grooteplein Zuid 26-28, 6525 GA, Nijmegen, The Netherlands
  • School of Biomolecular & Biomed Science, Conway Institute, University College Dublin, 4, Dublin, Ireland
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1038/ncomms11491

    DOI

    http://dx.doi.org/10.1038/ncomms11491

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1011167377

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/27173435


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