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Demosponge and Sea Anemone Fibrillar Collagen Diversity Reveals the Early Emergence of A/C Clades and the Maintenance of the Modular Structure of Type V/XI Collagens from Sponge to Human*S⃞

Identifieur interne : 000E68 ( Pmc/Curation ); précédent : 000E67; suivant : 000E69

Demosponge and Sea Anemone Fibrillar Collagen Diversity Reveals the Early Emergence of A/C Clades and the Maintenance of the Modular Structure of Type V/XI Collagens from Sponge to Human*S⃞

Auteurs : Jean-Yves Exposito ; Claire Larroux [Australie] ; Caroline Cluzel ; Ulrich Valcourt ; Claire Lethias ; Bernard M. Degnan [Australie]

Source :

RBID : PMC:2661393

Abstract

Collagens are often considered a metazoan hallmark, with the fibril-forming fibrillar collagens present from sponges to human. From evolutionary studies, three fibrillar collagen clades (named A, B, and C) have been defined and shown to be present in mammals, whereas the emergence of the A and B clades predates the protostome/deuterostome split. Moreover, several C clade fibrillar collagen chains are present in some invertebrate deuterostome genomes but not in protostomes whose genomes have been sequenced. The newly sequenced genomes of the choanoflagellate Monosiga brevicollis, the demosponge Amphimedon queenslandica, and the cnidarians Hydra magnipapillata (Hydra) and Nematostella vectensis (sea anemone) allow us to have a better understanding of the origin and evolution of fibrillar collagens. Analysis of these genomes suggests that an ancestral fibrillar collagen gene arose at the dawn of the Metazoa, before the divergence of sponge and eumetazoan lineages. The duplication events leading to the formation of the three fibrillar collagen clades (A, B, and C) occurred before the eumetazoan radiation. Interestingly, only the B clade fibrillar collagens preserved their characteristic modular structure from sponge to human. This observation is compatible with the suggested primordial function of type V/XI fibrillar collagens in the initiation of the formation of the collagen fibrils.


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DOI: 10.1074/jbc.M804573200
PubMed: 18697744
PubMed Central: 2661393

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Jean-Yves Exposito
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Caroline Cluzel
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<nlm:aff id="N0x200d390N0x4428fc0"> Institut de Biologie et Chimie des Protéines (IBCP), 7 passage du Vercors, Lyon, F69367, France, CNRS, UMR 5086; Université de Lyon, France, Université Lyon 1, France, IFR 128, Lyon, France, and the</nlm:aff>
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Ulrich Valcourt
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Claire Lethias
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<p>Collagens are often considered a metazoan hallmark, with the fibril-forming fibrillar collagens present from sponges to human. From evolutionary studies, three fibrillar collagen clades (named A, B, and C) have been defined and shown to be present in mammals, whereas the emergence of the A and B clades predates the protostome/deuterostome split. Moreover, several C clade fibrillar collagen chains are present in some invertebrate deuterostome genomes but not in protostomes whose genomes have been sequenced. The newly sequenced genomes of the choanoflagellate
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<italic>Amphimedon queenslandica</italic>
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School of Integrative Biology, University of Queensland, Brisbane, Queensland 4072, Australia</aff>
<author-notes>
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<p>To whom correspondence should be addressed. Tel.: 33-4-72-72-26-77; Fax: 33-4-72-72-26-04; E-mail:
<email>jy.exposito@ibcp.fr</email>
. </p>
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<day>16</day>
<month>6</month>
<year>2008</year>
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<date date-type="rev-recd">
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<abstract>
<p>Collagens are often considered a metazoan hallmark, with the fibril-forming fibrillar collagens present from sponges to human. From evolutionary studies, three fibrillar collagen clades (named A, B, and C) have been defined and shown to be present in mammals, whereas the emergence of the A and B clades predates the protostome/deuterostome split. Moreover, several C clade fibrillar collagen chains are present in some invertebrate deuterostome genomes but not in protostomes whose genomes have been sequenced. The newly sequenced genomes of the choanoflagellate
<italic>Monosiga brevicollis</italic>
, the demosponge
<italic>Amphimedon queenslandica</italic>
, and the cnidarians
<italic>Hydra magnipapillata</italic>
(Hydra) and
<italic>Nematostella vectensis</italic>
(sea anemone) allow us to have a better understanding of the origin and evolution of fibrillar collagens. Analysis of these genomes suggests that an ancestral fibrillar collagen gene arose at the dawn of the Metazoa, before the divergence of sponge and eumetazoan lineages. The duplication events leading to the formation of the three fibrillar collagen clades (A, B, and C) occurred before the eumetazoan radiation. Interestingly, only the B clade fibrillar collagens preserved their characteristic modular structure from sponge to human. This observation is compatible with the suggested primordial function of type V/XI fibrillar collagens in the initiation of the formation of the collagen fibrils.</p>
</abstract>
</article-meta>
<notes>
<fn-group>
<fn id="fn1">
<label>*</label>
<p>The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked “
<italic>advertisement</italic>
” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.</p>
</fn>
<fn id="fn2">
<label>S⃞</label>
<p>The on-line version of this article (available at
<ext-link ext-link-type="uri" xlink:href="http://www.jbc.org">http://www.jbc.org</ext-link>
) contains supplemental Figs. S1–S4.</p>
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