The evolution of metazoan extracellular matrix

Journal of Cell Biology

Volumn 196, Issue 6, 2012, Pages 671-679

  Hynes, Richard O ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; DYSTROGLYCAN; FIBRONECTIN; GLYCOPROTEIN; INTEGRIN; LAMININ BINDING PROTEIN; MEMBRANE PROTEIN; PERLECAN; PROTEOGLYCAN; SYNDECAN;

BASEMENT MEMBRANE; CARCINOGENESIS; CELL MIGRATION; CELL STRUCTURE; DROSOPHILA MELANOGASTER; ENZYME MECHANISM; EXON; EXTRACELLULAR MATRIX; GENE DUPLICATION; GENOME ANALYSIS; HYDRA MAGNIPAPILLATA; LIFE CYCLE STAGE; METAZOON; MOLECULAR EVOLUTION; NEMATOSTELLA VECTENSIS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SEQUENCE ANALYSIS;

ANIMALS; EVOLUTION, MOLECULAR; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; GENOME; INVERTEBRATES; VERTEBRATES;

METAZOA; VERTEBRATA;

EID: 84860293184     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201109041     Document Type: Review

References (55)

1. Adams, J.C., and J. Lawler. 2011. The thrombospondins. Cold Spring Harb. Perspect. Biol. 3:a009712. http://dx.doi.org/10.1101/cshperspect.a009712
2. Aouacheria, A., C. Geourjon, N. Aghajari, V. Navratil, G. Deléage, C. Lethias, and J.-Y. Exposito. 2006. 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. 23:2288-2302. http://dx.doi.org/10.1093/molbev/msl100
3. Ball, E.E., D.C. Hayward, R. Saint, and D.J. Miller. 2004. A simple plan- cnidarians and the origins of developmental mechanisms. Nat. Rev. Genet. 5:567-577. http://dx.doi.org/10.1038/nrg1402
4. Barros, C.S., S.J. Franco, and U. Müller. 2011. Extracellular matrix: functions in the nervous system. Cold Spring Harb. Perspect. Biol. 3:a005108. http://dx.doi.org/10.1101/cshperspect.a005108
5. Bentley, A.A., and J.C. Adams. 2010. The evolution of thrombospondins and their ligand-binding activities. Mol. Biol. Evol. 27:2187-2197. http://dx.doi.org/10.1093/molbev/msq107
6. Bergmeier, W., and R.O. Hynes. 2012. Extracellular matrix proteins in hemostasis and thrombosis. Cold Spring Harb. Perspect. Biol. 4:a005132. http://dx.doi.org/10.1101/cshperspect.a005132
7. Boute, N., J.Y. Exposito, N. Boury-Esnault, J. Vacelet, N. Noro, K. Miyazaki, K. Yoshizato, and R. Garrone. 1996. Type IV collagen in sponges, the missing link in basement membrane ubiquity. Biol. Cell. 88:37-44. http://dx.doi.org/10.1016/S0248-4900(97)86829-3
8. Chapman, J.A., E.F. Kirkness, O. Simakov, S.E. Hampson, T. Mitros, T. Weinmaier, T. Rattei, P.G. Balasubramanian, J. Borman, D. Busam, et al. 2010. The dynamic genome of Hydra. Nature. 464:592-596. http://dx.doi.org/10.1038/nature08830
9. Chiquet-Ehrismann, R., and R.P. Tucker. 2011. Tenascins and the importance of adhesion modulation. Cold Spring Harb. Perspect. Biol. 3:a004960. http://dx.doi.org/10.1101/cshperspect.a004960
10. Couchman, J.R. 2010. Transmembrane signaling proteoglycans. Annu. Rev. Cell Dev. Biol. 26:89-114. http://dx.doi.org/10.1146/annurev-cellbio-100109-104126
11. Dehal, P., Y. Satou, R.K. Campbell, J. Chapman, B. Degnan, A. De Tomaso, B. Davidson, A. Di Gregorio, M. Gelpke, D.M. Goodstein, et al. 2002. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science. 298:2157-2167. http://dx.doi.org/10.1126/science.1080049
12. Engel, J. 1996. Domain organizations of modular extracellular matrix proteins and their evolution. Matrix Biol. 15:295-299. http://dx.doi.org/10.1016/S0945-053X(96)90130-4
13. Ewan, R., J. Huxley-Jones, A.P. Mould, M.J. Humphries, D.L. Robertson, and R.P. Boot-Handford. 2005. The integrins of the urochordate Ciona intestinalis provide novel insights into the molecular evolution of the vertebrate integrin family. BMC Evol. Biol. 5:31. http://dx.doi.org/10.1186/1471-2148-5-31
14. Exposito, J.-Y., C. Larroux, C. Cluzel, U. Valcourt, C. Lethias, and B.M. Degnan. 2008. 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. J. Biol. Chem. 283:28226-28235. http://dx.doi.org/10.1074/jbc.M804573200
15. Exposito, J.-Y., U. Valcourt, C. Cluzel, and C. Lethias. 2010. The fibrillar collagen family. Int. J. Mol. Sci. 11:407-426. http://dx.doi.org/10.3390/ijms11020407
16. Fahey, B., and B.M. Degnan. 2010. Origin of animal epithelia: insights from the sponge genome. Evol. Dev. 12:601-617. http://dx.doi.org/10.1111/j.1525-142X.2010.00445.x
17. Gazave, E., P. Lapébie, E. Renard, J. Vacelet, C. Rocher, A.V. Ereskovsky, D.V. Lavrov, and C. Borchiellini. 2010. Molecular phylogeny restores the supra-generic subdivision of homoscleromorph sponges (Porifera, Homoscleromorpha). PLoS ONE. 5:e14290. http://dx.doi.org/10.1371/journal.pone.0014290
18. Heino, J., M. Huhtala, J. Käpylä, and M.S. Johnson. 2009. Evolution of collagen-based adhesion systems. Int. J. Biochem. Cell Biol. 41:341-348. http://dx.doi.org/10.1016/j.biocel.2008.08.021
19. Hohenester, E., and J. Engel. 2002. Domain structure and organisation in extracellular matrix proteins. Matrix Biol. 21:115-128. http://dx.doi.org/10.1016/S0945-053X(01)00191-3
20. Huhtala, M., J. Heino, D. Casciari, A. de Luise, and M.S. Johnson. 2005. Integrin evolution: insights from ascidian and teleost fish genomes. Matrix Biol. 24:83-95. http://dx.doi.org/10.1016/j.matbio.2005.01.003
21. Hutter, H., B.E. Vogel, J.D. Plenefisch, C.R. Norris, R.B. Proenca, J. Spieth, C. Guo, S. Mastwal, X. Zhu, J. Scheel, and E.M. Hedgecock. 2000. Conservation and novelty in the evolution of cell adhesion and extracellular matrix genes. Science. 287:989-994. http://dx.doi.org/10.1126/science.287.5455.989
22. Huxley-Jones, J., D.L. Robertson, and R.P. Boot-Handford. 2007. On the origins of the extracellular matrix in vertebrates. Matrix Biol. 26:2-11. http://dx.doi.org/10.1016/j.matbio.2006.09.008
23. Hynes, R.O. 1990. Fibronectins. Springer-Verlag, New York. 546 pp.
24. Hynes, R.O. 2009. The extracellular matrix: not just pretty fibrils. Science. 326:1216-1219. http://dx.doi.org/10.1126/science.1176009
25. Hynes, R.O., and A. Naba. 2011. Overview of the matrisome-an inventory of extracellular matrix constituents and functions. Cold Spring Harb. Perspect. Biol. 4:a004903. http://dx.doi.org/10.1101/cshperspect.a004903
26. Hynes, R.O., and Q. Zhao. 2000. The evolution of cell adhesion. J. Cell Biol. 150:F89-F96. http://dx.doi.org/10.1083/jcb.150.2.F89
27. King, N., C.T. Hittinger, and S.B. Carroll. 2003. Evolution of key cell signaling and adhesion protein families predates animal origins. Science. 301:361-363. http://dx.doi.org/10.1126/science.1083853
28. King, N., M.J. Westbrook, S.L. Young, A. Kuo, M. Abedin, J. Chapman, S. Fairclough, U. Hellsten, Y. Isogai, I. Letunic, et al. 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature. 451:783-788. http://dx.doi.org/10.1038/nature06617
29. Knack, B.A., A. Iguchi, C. Shinzato, D.C. Hayward, E.E. Ball, and D.J. Miller. 2008. Unexpected diversity of cnidarian integrins: expression during coral gastrulation. BMC Evol. Biol. 8:136. http://dx.doi.org/10.1186/1471-2148-8-136
30. Martindale, M.Q., J.R. Finnerty, and J.Q. Henry. 2002. The Radiata and the evolutionary origins of the bilaterian body plan. Mol. Phylogenet. Evol. 24:358-365. http://dx.doi.org/10.1016/S1055-7903(02)00208-7
31. Merline, R., R.M. Schaefer, and L. Schaefer. 2009. The matricellular functions of small leucine-rich proteoglycans (SLRPs). J Cell Commun Signal. 3:323-335. http://dx.doi.org/10.1007/s12079-009-0066-2
32. Myllyharju, J., and K.I. Kivirikko. 2004. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20:33-43. http://dx.doi.org/10.1016/j.tig.2003.11.004
33. Naba, A., K.R. Clauser, S. Hoersch, H. Liu, S.A. Carr, and R.O. Hynes. 2011. The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Mol. Cell. Proteomics. http://dx.doi.org/10.1074/mcp.M111.014647
34. Ozbek, S., P.G. Balasubramanian, R. Chiquet-Ehrismann, R.P. Tucker, and J.C. Adams. 2010. The evolution of extracellular matrix. Mol. Biol. Cell. 21:4300-4305. http://dx.doi.org/10.1091/mbc.E10-03-0251
35. Patthy, L. 1999. Genome evolution and the evolution of exon-shuffling-a review. Gene. 238:103-114. http://dx.doi.org/10.1016/S0378-1119(99)00228-0
36. Philippe, H., N. Lartillot, and H. Brinkmann. 2005. Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. Mol. Biol. Evol. 22:1246-1253. http://dx.doi.org/10.1093/molbev/msi111
37. Philippe, H., R. Derelle, P. Lopez, K. Pick, C. Borchiellini, N. Boury-Esnault, J. Vacelet, E. Renard, E. Houliston, E. Quéinnec, et al. 2009. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19:706-712. http://dx.doi.org/10.1016/j.cub.2009.02.052
38. Pick, K.S., H. Philippe, F. Schreiber, D. Erpenbeck, D.J. Jackson, P. Wrede, M. Wiens, A. Alié, B. Morgenstern, M. Manuel, and G. Wörheide. 2010. Improved phylogenomic taxon sampling noticeably affects nonbilaterian relationships. Mol. Biol. Evol. 27:1983-1987. http://dx.doi.org/10.1093/molbev/msq089
39. Putnam, N.H., M. Srivastava, U. Hellsten, B. Dirks, J. Chapman, A. Salamov, A. Terry, H. Shapiro, E. Lindquist, V.V. Kapitonov, et al. 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science. 317:86-94. http://dx.doi.org/10.1126/science.1139158
40. Putnam, N.H., T. Butts, D.E.K. Ferrier, R.F. Furlong, U. Hellsten, T. Kawashima, M. Robinson-Rechavi, E. Shoguchi, A. Terry, J.-K. Yu, et al. 2008. The amphioxus genome and the evolution of the chordate karyotype. Nature. 453:1064-1071. http://dx.doi.org/10.1038/nature06967
41. Ricard-Blum, S. 2011. The collagen family. Cold Spring Harb. Perspect. Biol. 3:a004978. http://dx.doi.org/10.1101/cshperspect.a004978
42. Robertson, I., S. Jensen, and P. Handford. 2011. TB domain proteins: evolutionary insights into the multifaceted roles of fibrillins and LTBPs. Biochem. J. 433:263-276. http://dx.doi.org/10.1042/BJ20101320
43. Sadler, J.E. 2009. von Willebrand factor assembly and secretion. J. Thromb. Haemost. 7:24-27. http://dx.doi.org/10.1111/j.1538-7836.2009.03375.x
44. Schaefer, L., and R.M. Schaefer. 2010. Proteoglycans: from structural compounds to signaling molecules. Cell Tissue Res. 339:237-246. http://dx.doi.org/10.1007/s00441-009-0821-y
45. Schierwater, B., M. Eitel, W. Jakob, H.-J. Osigus, H. Hadrys, S.L. Dellaporta, S.-O. Kolokotronis, and R. Desalle. 2009. Concatenated analysis sheds light on early metazoan evolution and fuels a modern "urmetazoon"hypothesis. PLoS Biol. 7:e20. http://dx.doi.org/10.1371/journal.pbio.1000020
46. Sebé-Pedrós, A., A.J. Roger, F.B. Lang, N. King, and I. Ruiz-Trillo. 2010. Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc. Natl. Acad. Sci. USA. 107:10142-10147. http://dx.doi.org/10.1073/pnas.1002257107
47. Shalchian-Tabrizi, K., M.A. Minge, M. Espelund, R. Orr, T. Ruden, K.S. Jakobsen, and T. Cavalier-Smith. 2008. Multigene phylogeny of choanozoa and the origin of animals. PLoS ONE. 3:e2098. http://dx.doi.org/10.1371/journal.pone.0002098
48. Srivastava, M., E. Begovic, J. Chapman, N.H. Putnam, U. Hellsten, T. Kawashima, A. Kuo, T. Mitros, A. Salamov, M.L. Carpenter, et al. 2008. The Trichoplax genome and the nature of placozoans. Nature. 454:955-960. http://dx.doi.org/10.1038/nature07191
49. Srivastava, M., O. Simakov, J. Chapman, B. Fahey, M.E.A. Gauthier, T. Mitros, G.S. Richards, C. Conaco, M. Dacre, U. Hellsten, et al. 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature. 466:720-726. http://dx.doi.org/10.1038/nature09201
50. Tucker, R.P., and R. Chiquet-Ehrismann. 2009. Evidence for the evolution of tenascin and fibronectin early in the chordate lineage. Int. J. Biochem. Cell Biol. 41:424-434. http://dx.doi.org/10.1016/j.biocel.2008.08.003
51. Wada, H., M. Okuyama, N. Satoh, and S. Zhang. 2006. Molecular evolution of fibrillar collagen in chordates, with implications for the evolution of vertebrate skeletons and chordate phylogeny. Evol. Dev. 8:370-377. http://dx.doi.org/10.1111/j.1525-142X.2006.00109.x
52. Whittaker, C.A., and R.O. Hynes. 2002. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell. 13:3369-3387. http://dx.doi.org/10.1091/mbc.E02-05-0259
53. Whittaker, C.A., K.-F. Bergeron, J. Whittle, B.P. Brandhorst, R.D. Burke, and R.O. Hynes. 2006. The echinoderm adhesome. Dev. Biol. 300:252-266. http://dx.doi.org/10.1016/j.ydbio.2006.07.044
54. Yurchenco, P.D. 2011. Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb. Perspect. Biol. 3:a004911. http://dx.doi.org/10.1101/cshperspect.a004911
55. Zhang, X., R.P. Boot-Handford, J. Huxley-Jones, L.N. Forse, A.P. Mould, D.L. Robertson, Lili, M. Athiyal, and M.P. Sarras Jr. 2007. The collagens of hydra provide insight into the evolution of metazoan extracellular matrices. J. Biol. Chem. 282:6792-6802. http://dx.doi.org/10.1074/jbc.M607528200