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PMID: 18697744 Published · ppublish English Journal Article

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.

The Journal of biological chemistry ·Vol. 283 ·No. 42 ·2008-10-17 ·Pages 28226-35

Exposito JY, Larroux C, Cluzel C, Valcourt U, Lethias C, Degnan BM

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.

MeSH Terms
Amino Acid Sequence Animals Collagen/chemistry Collagen Type V/chemistry Collagen Type XI/chemistry Evolution, Molecular Fibrillar Collagens/chemistry Genome Humans Models, Biological Molecular Sequence Data Phylogeny Porifera Sea Anemones/metabolism Sequence Homology, Amino Acid
Chemicals
Collagen Type V Collagen Type XI Fibrillar Collagens Collagen
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Exposito Jean-Yves
Institut de Biologie et Chimie des Protéines (IBCP), 7 passage du Vercors, Lyon, F69367, France, CNRS, UMR 5086. jy.exposito@ibcp.fr
Larroux Claire
Cluzel Caroline
Valcourt Ulrich
Lethias Claire
Degnan Bernard M
References (52)
52 references, click to expand
  1. A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses.
    Proc Natl Acad Sci U S A. 2006 Apr 25;103(17):6647-52 PMID: 16614065
  2. MRBAYES: Bayesian inference of phylogenetic trees.
    Bioinformatics. 2001 Aug;17(8):754-5 PMID: 11524383
  3. Molecular evolution of fibrillar collagen in chordates, with implications for the evolution of vertebrate skeletons and chordate phylogeny.
    Evol Dev. 2006 Jul-Aug;8(4):370-7 PMID: 16805901
  4. Axial structure of the heterotypic collagen fibrils of vitreous humour and cartilage.
    J Mol Biol. 2001 Mar 9;306(5):1011-22 PMID: 11237615
  5. Prediction of complete gene structures in human genomic DNA.
    J Mol Biol. 1997 Apr 25;268(1):78-94 PMID: 9149143
  6. Sponge paraphyly and the origin of Metazoa.
    J Evol Biol. 2001 Jan 8;14(1):171-179 PMID: 29280585
  7. Invertebrate data predict an early emergence of vertebrate fibrillar collagen clades and an anti-incest model.
    J Biol Chem. 2004 Nov 12;279(46):47711-9 PMID: 15358765
  8. PHYML Online--a web server for fast maximum likelihood-based phylogenetic inference.
    Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W557-9 PMID: 15980534
  9. Molecular, biochemical and functional analysis of a novel and developmentally important fibrillar collagen (Hcol-I) in hydra.
    Development. 2000 Nov;127(21):4669-80 PMID: 11023869
  10. Type XXVII collagen at the transition of cartilage to bone during skeletogenesis.
    Bone. 2007 Oct;41(4):535-42 PMID: 17693149
  11. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization.
    Science. 2007 Jul 6;317(5834):86-94 PMID: 17615350
  12. Co-expression and functional interaction of silicatein with galectin: matrix-guided formation of siliceous spicules in the marine demosponge Suberites domuncula.
    J Biol Chem. 2006 Apr 28;281(17):12001-9 PMID: 16495220
  13. The collagens of hydra provide insight into the evolution of metazoan extracellular matrices.
    J Biol Chem. 2007 Mar 2;282(9):6792-802 PMID: 17204477
  14. Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics.
    BMC Evol Biol. 2007 Mar 02;7:33 PMID: 17335570
  15. The complete intron/exon structure of Ephydatia mülleri fibrillar collagen gene suggests a mechanism for the evolution of an ancestral gene module.
    J Mol Evol. 1993 Sep;37(3):254-9 PMID: 8230249
  16. Type IV collagen in sponges, the missing link in basement membrane ubiquity.
    Biol Cell. 1996;88(1-2):37-44 PMID: 9175266
  17. Early evolution of animal cell signaling and adhesion genes.
    Proc Natl Acad Sci U S A. 2006 Aug 15;103(33):12451-6 PMID: 16891419
  18. RASCAL: rapid scanning and correction of multiple sequence alignments.
    Bioinformatics. 2003 Jun 12;19(9):1155-61 PMID: 12801878
  19. The fibril structure of type V collagen triple-helical domain.
    Micron. 2001 Apr;32(3):317-23 PMID: 11006511
  20. The NK homeobox gene cluster predates the origin of Hox genes.
    Curr Biol. 2007 Apr 17;17(8):706-10 PMID: 17379523
  21. Collagen XXVII is developmentally regulated and forms thin fibrillar structures distinct from those of classical vertebrate fibrillar collagens.
    J Biol Chem. 2007 Apr 27;282(17):12791-5 PMID: 17331945
  22. Sea urchin collagen evolutionarily homologous to vertebrate pro-alpha 2(I) collagen.
    J Biol Chem. 1992 Aug 5;267(22):15559-62 PMID: 1639795
  23. Cytological basis of photoresponsive behavior in a sponge larva.
    Biol Bull. 2001 Dec;201(3):323-38 PMID: 11751245
  24. Evolution and development of the chordates: collagen and pharyngeal cartilage.
    Mol Biol Evol. 2006 Mar;23(3):541-9 PMID: 16280542
  25. A comprehensive study of the spatial and temporal expression of the col5a1 gene in mouse embryos: a clue for understanding collagen V function in developing connective tissues.
    Cell Tissue Res. 2007 Feb;327(2):323-32 PMID: 17024418
  26. Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods.
    Methods Enzymol. 1996;266:418-27 PMID: 8743697
  27. Type V collagen: heterotypic type I/V collagen interactions in the regulation of fibril assembly.
    Micron. 2001 Apr;32(3):223-37 PMID: 11006503
  28. Distinct maturations of N-propeptide domains in fibrillar procollagen molecules involved in the formation of heterotypic fibrils in adult sea urchin collagenous tissues.
    J Biol Chem. 2004 Mar 12;279(11):9811-7 PMID: 14665629
  29. EST analysis of the cnidarian Acropora millepora reveals extensive gene loss and rapid sequence divergence in the model invertebrates.
    Curr Biol. 2003 Dec 16;13(24):2190-5 PMID: 14680636
  30. Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity.
    Evol Dev. 2006 Mar-Apr;8(2):150-73 PMID: 16509894
  31. Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record.
    Proc Natl Acad Sci U S A. 2005 Jul 5;102(27):9547-52 PMID: 15983372
  32. Collagen XXIV, a vertebrate fibrillar collagen with structural features of invertebrate collagens: selective expression in developing cornea and bone.
    J Biol Chem. 2003 Oct 31;278(44):43236-44 PMID: 12874293
  33. MrBayes 3: Bayesian phylogenetic inference under mixed models.
    Bioinformatics. 2003 Aug 12;19(12):1572-4 PMID: 12912839
  34. Genesis and expansion of metazoan transcription factor gene classes.
    Mol Biol Evol. 2008 May;25(5):980-96 PMID: 18296413
  35. Genome-based identification and analysis of collagen-related structural motifs in bacterial and viral proteins.
    J Biol Chem. 2003 Aug 22;278(34):32313-6 PMID: 12788919
  36. Collagens, modifying enzymes and their mutations in humans, flies and worms.
    Trends Genet. 2004 Jan;20(1):33-43 PMID: 14698617
  37. A novel and highly conserved collagen (pro(alpha)1(XXVII)) with a unique expression pattern and unusual molecular characteristics establishes a new clade within the vertebrate fibrillar collagen family.
    J Biol Chem. 2003 Aug 15;278(33):31067-77 PMID: 12766169
  38. Identification, characterization and expression analysis of a new fibrillar collagen gene, COL27A1.
    Matrix Biol. 2003 Mar;22(1):3-14 PMID: 12714037
  39. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny.
    Comput Appl Biosci. 1996 Dec;12(6):543-8 PMID: 9021275
  40. Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution.
    Mol Phylogenet Evol. 2004 Sep;32(3):823-37 PMID: 15288059
  41. Evolution of collagens.
    Anat Rec. 2002 Nov 1;268(3):302-16 PMID: 12382326
  42. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  43. Characterization of a fibrillar collagen gene in sponges reveals the early evolutionary appearance of two collagen gene families.
    Proc Natl Acad Sci U S A. 1990 Sep;87(17):6669-73 PMID: 2395869
  44. Cloning of an annelid fibrillar-collagen gene and phylogenetic analysis of vertebrate and invertebrate collagens.
    Eur J Biochem. 1997 May 15;246(1):50-8 PMID: 9210465
  45. SMART, a simple modular architecture research tool: identification of signaling domains.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):5857-64 PMID: 9600884
  46. Tracing the evolution of vertebrate fibrillar collagens from an ancestral alpha chain.
    Matrix Biol. 2000 Jul;19(3):275-9 PMID: 10936452
  47. Variants in a novel epidermal collagen gene (COL29A1) are associated with atopic dermatitis.
    PLoS Biol. 2007 Sep;5(9):e242 PMID: 17850181
  48. Type V collagen controls the initiation of collagen fibril assembly.
    J Biol Chem. 2004 Dec 17;279(51):53331-7 PMID: 15383546
  49. Insights into early extracellular matrix evolution: spongin short chain collagen-related proteins are homologous to basement membrane type IV collagens and form a novel family widely distributed in invertebrates.
    Mol Biol Evol. 2006 Dec;23(12):2288-302 PMID: 16945979
  50. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans.
    Nature. 2008 Feb 14;451(7180):783-8 PMID: 18273011
  51. TreeView: an application to display phylogenetic trees on personal computers.
    Comput Appl Biosci. 1996 Aug;12(4):357-8 PMID: 8902363
  52. Collagen XXVIII, a novel von Willebrand factor A domain-containing protein with many imperfections in the collagenous domain.
    J Biol Chem. 2006 Feb 10;281(6):3494-504 PMID: 16330543
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
2008-10-17
Epub
2008-00-11
Pages
28226-35
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2661393
Subset
IM
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