The collαgen III fibril has a “flexi-rod” structure of flexible sequences interspersed with rigid bioactive domains including two with hemostatic roles
Identifieur interne : 002837 ( Pmc/Curation ); précédent : 002836; suivant : 002838The collαgen III fibril has a “flexi-rod” structure of flexible sequences interspersed with rigid bioactive domains including two with hemostatic roles
Auteurs : J. Des Parkin [Australie] ; James D. San Antonio [États-Unis] ; Anton V. Persikov [États-Unis] ; Hayat Dagher [Australie] ; Raymond Dalgleish [Royaume-Uni] ; Shane T. Jensen [États-Unis] ; Xavier Jeunemaitre [France] ; Judy Savige [Australie]Source :
- PLoS ONE [ 1932-6203 ] ; 2017.
Abstract
Collagen III is critical to the integrity of blood vessels and distensible organs, and in hemostasis. Examination of the human collagen III interactome reveals a nearly identical structural arrangement and charge distribution pattern as for collagen I, with cell interaction domains, fibrillogenesis and enzyme cleavage domains, several major ligand-binding regions, and intermolecular crosslink sites at the same sites. These similarities allow heterotypic fibril formation with, and substitution by, collagen I in embryonic development and wound healing. The collagen III fibril assumes a “flexi-rod” structure with flexible zones interspersed with rod-like domains, which is consistent with the molecule’s prominence in young, pliable tissues and distensible organs. Collagen III has two major hemostasis domains, with binding motifs for von Willebrand factor, α2β1 integrin, platelet binding octapeptide and glycoprotein VI, consistent with the bleeding tendency observed with
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DOI: 10.1371/journal.pone.0175582
PubMed: 28704418
PubMed Central: 5509119
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Xavier Jeunemaitre<affiliation><nlm:aff id="aff006"><addr-line>INSERM U970 Paris Cardiovascular Research Centre, Paris France</addr-line></nlm:aff><wicri:noCountry code="subfield">Paris France</wicri:noCountry></affiliation><affiliation wicri:level="1"><nlm:aff id="aff007"><addr-line>University Paris Descartes, Paris Sorbonne Cite, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>University Paris Descartes, Paris Sorbonne Cite, Paris</wicri:regionArea></affiliation>Le document en format XML
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Des" last="Parkin">J. Des Parkin</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>From the University of Melbourne Department of Medicine (Northern Health), Melbourne, VIC, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>From the University of Melbourne Department of Medicine (Northern Health), Melbourne, VIC</wicri:regionArea></affiliation></author><author><name sortKey="San Antonio, James D" sort="San Antonio, James D" uniqKey="San Antonio J" first="James D." last="San Antonio">James D. San Antonio</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Operations, Stryker Global Quality and Operations, Malvern, PA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Operations, Stryker Global Quality and Operations, Malvern, PA</wicri:regionArea></affiliation></author><author><name sortKey="Persikov, Anton V" sort="Persikov, Anton V" uniqKey="Persikov A" first="Anton V." last="Persikov">Anton V. Persikov</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Lewis-Sigler Institute for Integrative Genomics, Princeton University, Carl Icahn Lab, Princeton, NJ, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Lewis-Sigler Institute for Integrative Genomics, Princeton University, Carl Icahn Lab, Princeton, NJ</wicri:regionArea></affiliation></author><author><name sortKey="Dagher, Hayat" sort="Dagher, Hayat" uniqKey="Dagher H" first="Hayat" last="Dagher">Hayat Dagher</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>From the University of Melbourne Department of Medicine (Northern Health), Melbourne, VIC, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>From the University of Melbourne Department of Medicine (Northern Health), Melbourne, VIC</wicri:regionArea></affiliation></author><author><name sortKey="Dalgleish, Raymond" sort="Dalgleish, Raymond" uniqKey="Dalgleish R" first="Raymond" last="Dalgleish">Raymond Dalgleish</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Department of Genetics, University of Leicester, Leicester, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Genetics, University of Leicester, Leicester</wicri:regionArea></affiliation></author><author><name sortKey="Jensen, Shane T" sort="Jensen, Shane T" uniqKey="Jensen S" first="Shane T." last="Jensen">Shane T. Jensen</name><affiliation wicri:level="1"><nlm:aff id="aff005"><addr-line>Wharton Business School, University of Pennsylvania, Philadelphia, PA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Wharton Business School, University of Pennsylvania, Philadelphia, PA</wicri:regionArea></affiliation></author><author><name sortKey="Jeunemaitre, Xavier" sort="Jeunemaitre, Xavier" uniqKey="Jeunemaitre X" first="Xavier" last="Jeunemaitre">Xavier Jeunemaitre</name><affiliation><nlm:aff id="aff006"><addr-line>INSERM U970 Paris Cardiovascular Research Centre, Paris France</addr-line></nlm:aff><wicri:noCountry code="subfield">Paris France</wicri:noCountry></affiliation><affiliation wicri:level="1"><nlm:aff id="aff007"><addr-line>University Paris Descartes, Paris Sorbonne Cite, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>University Paris Descartes, Paris Sorbonne Cite, Paris</wicri:regionArea></affiliation></author><author><name sortKey="Savige, Judy" sort="Savige, Judy" uniqKey="Savige J" first="Judy" last="Savige">Judy Savige</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>From the University of Melbourne Department of Medicine (Northern Health), Melbourne, VIC, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>From the University of Melbourne Department of Medicine (Northern Health), Melbourne, VIC</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Collagen III is critical to the integrity of blood vessels and distensible organs, and in hemostasis. Examination of the human collagen III interactome reveals a nearly identical structural arrangement and charge distribution pattern as for collagen I, with cell interaction domains, fibrillogenesis and enzyme cleavage domains, several major ligand-binding regions, and intermolecular crosslink sites at the same sites. These similarities allow heterotypic fibril formation with, and substitution by, collagen I in embryonic development and wound healing. The collagen III fibril assumes a “flexi-rod” structure with flexible zones interspersed with rod-like domains, which is consistent with the molecule’s prominence in young, pliable tissues and distensible organs. Collagen III has two major hemostasis domains, with binding motifs for von Willebrand factor, α2β1 integrin, platelet binding octapeptide and glycoprotein VI, consistent with the bleeding tendency observed with <italic>COL3A1</italic> disease-causing sequence variants.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Ricard Blum, S" uniqKey="Ricard Blum S">S Ricard-Blum</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rich, A" uniqKey="Rich A">A Rich</name></author><author><name sortKey="Crick, Fh" uniqKey="Crick F">FH Crick</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Meek, Km" uniqKey="Meek K">KM Meek</name></author><author><name sortKey="Chapman, Ja" uniqKey="Chapman J">JA Chapman</name></author><author><name sortKey="Hardcastle, Ra" uniqKey="Hardcastle R">RA Hardcastle</name></author></analytic></biblStruct><biblStruct><analytic><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28704418</article-id><article-id pub-id-type="pmc">5509119</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0175582</article-id><article-id pub-id-type="publisher-id">PONE-D-17-00972</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Collagens</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Database and Informatics Methods</subject><subj-group><subject>Bioinformatics</subject><subj-group><subject>Sequence Analysis</subject><subj-group><subject>Sequence Motif Analysis</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Chemical Characterization</subject><subj-group><subject>Binding Analysis</subject><subj-group><subject>Cell Binding Assay</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Proteins</subject><subj-group><subject>Extracellular Matrix Proteins</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Chemical Characterization</subject><subj-group><subject>Binding Analysis</subject><subj-group><subject>Receptor-Ligand Binding Assay</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cell Adhesion</subject><subj-group><subject>Integrins</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Cell Biology</subject><subj-group><subject>Cellular Structures and Organelles</subject><subj-group><subject>Extracellular Matrix</subject><subj-group><subject>Integrins</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Glycobiology</subject><subj-group><subject>Glycoproteins</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Chemical Characterization</subject><subj-group><subject>Binding Analysis</subject></subj-group></subj-group></subj-group></article-categories><title-group><article-title>The collαgen III fibril has a “flexi-rod” structure of flexible sequences interspersed with rigid bioactive domains including two with hemostatic roles</article-title><alt-title alt-title-type="running-head">Collagen III interactome reveals structural and functional domain organization</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Parkin</surname><given-names>J. Des</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>San Antonio</surname><given-names>James D.</given-names></name><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Persikov</surname><given-names>Anton V.</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Dagher</surname><given-names>Hayat</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Dalgleish</surname><given-names>Raymond</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Jensen</surname><given-names>Shane T.</given-names></name><xref ref-type="aff" rid="aff005"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Jeunemaitre</surname><given-names>Xavier</given-names></name><xref ref-type="aff" rid="aff006"><sup>6</sup></xref><xref ref-type="aff" rid="aff007"><sup>7</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-6813-0288</contrib-id><name><surname>Savige</surname><given-names>Judy</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>From the University of Melbourne Department of Medicine (Northern Health), Melbourne, VIC, Australia</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Operations, Stryker Global Quality and Operations, Malvern, PA, United States of America</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Lewis-Sigler Institute for Integrative Genomics, Princeton University, Carl Icahn Lab, Princeton, NJ, United States of America</addr-line></aff><aff id="aff004"><label>4</label><addr-line>Department of Genetics, University of Leicester, Leicester, United Kingdom</addr-line></aff><aff id="aff005"><label>5</label><addr-line>Wharton Business School, University of Pennsylvania, Philadelphia, PA, United States of America</addr-line></aff><aff id="aff006"><label>6</label><addr-line>INSERM U970 Paris Cardiovascular Research Centre, Paris France</addr-line></aff><aff id="aff007"><label>7</label><addr-line>University Paris Descartes, Paris Sorbonne Cite, Paris, France</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Zheng</surname><given-names>Jie</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>University of Akron, UNITED STATES</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>The employment of JSA in private industry (Stryker, Inc.) does not alter the authors’ adherence to PLOS ONE policies on sharing data and materials.</p></fn><fn fn-type="con"><p><list list-type="simple"><list-item><p><bold>Conceptualization:</bold> JDP JDS JAS.</p></list-item><list-item><p><bold>Data curation:</bold> JDP JDS AP HD RD STJ XJ JS.</p></list-item><list-item><p><bold>Formal analysis:</bold> JDP JDS AP STJ JS.</p></list-item><list-item><p><bold>Investigation:</bold> JDP JDS AP STJ JS.</p></list-item><list-item><p><bold>Methodology:</bold> JDP JDS AP STJ JS.</p></list-item><list-item><p><bold>Project administration:</bold> JDP JDS AP HD RD STJ XJ JS.</p></list-item><list-item><p><bold>Resources:</bold> JDP JDS AP RD STJ XJ JS.</p></list-item><list-item><p><bold>Software:</bold> STJ RD.</p></list-item><list-item><p><bold>Supervision:</bold> JDS JS.</p></list-item><list-item><p><bold>Validation:</bold> JDS JS JDP.</p></list-item><list-item><p><bold>Visualization:</bold> JDS JS JDP.</p></list-item><list-item><p><bold>Writing – original draft:</bold> JDS JS JDP.</p></list-item><list-item><p><bold>Writing – review & editing:</bold> JDP JDS AP HD RD STJ XJ JS.</p></list-item></list></p></fn><corresp id="cor001">* E-mail: <email>jasavige@unimelb.edu.au</email></corresp></author-notes><pub-date pub-type="epub"><day>13</day><month>7</month><year>2017</year></pub-date><pub-date pub-type="collection"><year>2017</year></pub-date><volume>12</volume><issue>7</issue><elocation-id>e0175582</elocation-id><history><date date-type="received"><day>9</day><month>1</month><year>2017</year></date><date date-type="accepted"><day>20</day><month>3</month><year>2017</year></date></history><permissions><copyright-statement>© 2017 Parkin et al</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>Parkin et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0175582.pdf"></self-uri><abstract><p>Collagen III is critical to the integrity of blood vessels and distensible organs, and in hemostasis. Examination of the human collagen III interactome reveals a nearly identical structural arrangement and charge distribution pattern as for collagen I, with cell interaction domains, fibrillogenesis and enzyme cleavage domains, several major ligand-binding regions, and intermolecular crosslink sites at the same sites. These similarities allow heterotypic fibril formation with, and substitution by, collagen I in embryonic development and wound healing. The collagen III fibril assumes a “flexi-rod” structure with flexible zones interspersed with rod-like domains, which is consistent with the molecule’s prominence in young, pliable tissues and distensible organs. Collagen III has two major hemostasis domains, with binding motifs for von Willebrand factor, α2β1 integrin, platelet binding octapeptide and glycoprotein VI, consistent with the bleeding tendency observed with <italic>COL3A1</italic> disease-causing sequence variants.</p></abstract><funding-group><funding-statement>This research did not receive any specific grant from funding agencies in the public, commercial or not-for profit sectors. The second author of this manuscript (JSA) is an employee of private industry, Stryker, Inc. Stryker provided salary support for JSA, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript and has no financial or proprietary interest in the research. The specific roles of JSA in this publication are articulated in the “author contributions’ section.</funding-statement></funding-group><counts><fig-count count="5"></fig-count><table-count count="1"></table-count><page-count count="24"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the paper and its Supporting Information files.</p></notes></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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