The predicted secretomes of Monosiga brevicollis and Capsaspora owczarzaki, close unicellular relatives of metazoans, reveal new insights into the evolution of the metazoan extracellular matrix

Matrix Biology

Volumn 37, Issue , 2014, Pages 60-68

  Williams, Frederike ^a   Tew, Hannah A ^a   Paul, Catherine E ^a   Adams, Josephine C ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Adhesion; Choanoflagellate; Extracellular matrix; Filasterea; Metazoa; Multicellularity

Indexed keywords

FIBRONECTIN; GLYCOSAMINOGLYCAN; GLYCOSIDASE; INTEGRIN; LAMININ; PEPTIDES AND PROTEINS; SECRETOME; THROMBOSPONDIN; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; SCLEROPROTEIN;

ARTICLE; BINDING AFFINITY; CAPSASPORA OWCZARZAKI; EUKARYOTE; EXTRACELLULAR MATRIX; MONOSIGA BREVICOLLIS; NONHUMAN; PREDICTIVE VALUE; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; CHOANOFLAGELLATE; EVOLUTION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SECRETION (PROCESS); SEQUENCE ALIGNMENT; SPECIES DIFFERENCE;

AMINO ACID SEQUENCE; BIOLOGICAL EVOLUTION; CHOANOFLAGELLATA; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EID: 84908322799     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2014.02.002     Document Type: Article

References (53)

1. Adams J.C. The evolution of extracellular matrix: an over-view. Chapter 1 of "Evolution of Extracellular Matrix" 2013, 1-25.
2. F.W. Keeley and R.P. Mecham (Eds.), Biology of Extracellular Matrix series. Publisher, Springer. doi:10.1007/978-3-642-36002-2.
3. Adams J.C., Engel J. Bioinformatic analysis of adhesion proteins. Methods Mol. Biol. 2007, 370:147-171.
4. Adams J.C., Lawler J. The thrombospondins. Cold Spring Harb. Perspect Biol. 2011, 3(10):a009712. 10.1101/cshperspect.a009712.
5. Adl S.M., Simpson A.G., Lane C.E., Lukeš J., Bass D., Bowser S.S., Brown M.W., Burki F., Dunthorn M., Hampl V., Heiss A., Hoppenrath M., Lara E., Le Gall L., Lynn D.H., McManus H., Mitchell E.A., Mozley-Stanridge S.E., Parfrey L.W., Pawlowski J., Rueckert S., Shadwick R.S., Schoch C.L., Smirnov A., Spiegel F.W. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 2012, 59:429-493.
6. Allinson T.M., Parkin E.T., Turner A.J., Hooper N.M. ADAMs family members as amyloid precursor protein alpha-secretases. J. Neurosci. Res. 2003, 74:342-352.
7. Asch A.S., Silbiger S., Heimer E., Nachman R.L. Thrombospondin sequence motif (CSVTCG) is responsible for CD36 binding. Biochem. Biophys. Res. Commun. 1992, 182:1208-1217.
8. Bradshaw A.D. Diverse biological functions of the SPARC family of proteins. Int. J. Biochem. Cell Biol. 2012, 44:480-488.
9. Carafoli F., Clout N.J., Hohenester E. Crystal structure of the LG1-3 region of the laminin alpha2 chain. J. Biol. Chem. 2009, 284:22786-22792.
10. Carr M., Leadbeater B.S., Hassan R., Nelson M., Baldauf S.L. Molecular phylogeny of choanoflagellates, the sister group to Metazoa. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16641-16646.
11. Chen C.C., Lau L.F. Functions and mechanisms of action of CCN matricellular proteins. Int. J. Biochem. Cell Biol. 2009, 41:771-783.
12. Couchman J.R. Transmembrane signaling proteoglycans. Annu. Rev. Cell Dev. Biol. 2010, 26:89-114.
13. Dehal P., Boore J.L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 2005, 3:e314.
14. De Arcangelis A., Georges-Labouesse E. Integrin and ECM functions: roles in vertebrate development. Trends Genet. 2000, 16:389-395.
15. Domogatskaya A., Rodin S., Tryggvason K. Functional diversity of laminins. Annu. Rev. Cell Dev. Biol. 2012, 28:523-553.
16. Doolittle R.F., McNamara K., Lin K. Correlating structure and function during the evolution of fibrinogen-related domains. Protein Sci. 2012, 21:1808-1823.
17. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
18. Exposito J.Y., Larroux C., Cluzel C., Valcourt U., Lethias C., Degnan B.M. 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. 2008, 283:28226-28235.
19. Fairclough S.R., Chen Z., Kramer E., Zeng Q., Young S., Robertson H.M., Begovic E., Richter D.J., Russ C., Westbrook M.J., Manning G., Lang B.F., Haas B., Nusbaum C., King N. Premetazoan genome evolution and the regulation of cell differentiation in the choanoflagellate Salpingoeca rosetta. Genome Biol. 2013, 14(2):R15.
20. Guindon S., Gascuel O. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
21. Guo N.H., Krutzsch H.C., Nègre E., Vogel T., Blake D.A., Roberts D.D. Heparin- and sulfatide-binding peptides from the type I repeats of human thrombospondin promote melanoma cell adhesion. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:3040-3044.
22. Harrison D., Hussain S.A., Combs A.C., Ervasti J.M., Yurchenco P.D., Hohenester E. Crystal structure and cell surface anchorage sites of laminin alpha1LG4-5. J. Biol. Chem. 2007, 282:11573-11581.
23. Hertel L.A., Bayne C.J., Loker E.S. The symbiont Capsaspora owczarzaki, nov. gen. nov. sp., isolated from three strains of the pulmonate snail Biomphalaria glabrata is related to members of the Mesomycetozoea. Int. J. Parasitol. 2002, 32:1183-1191.
24. Huxley-Jones J., Robertson D.L., Boot-Handford R.P. On the origins of the extracellular matrix in vertebrates. Matrix Biol. 2007, 26:2-11.
25. Hynes R.O., Naba A. Overview of the matrisome - an inventory of extracellular matrix constituents and functions. Cold Spring Harb. Perspect. Biol. 2012, 4(1):a004903.
26. King N., Westbrook M.J., Young S.L., Kuo A., Abedin M., Chapman J., Fairclough S., Hellsten U., Isogai Y., Letunic I., Marr M., Pincus D., Putnam N., Rokas A., Wright K.J., Zuzow R., Dirks W., Good M., Goodstein D., Lemons D., Li W., Lyons J.B., Morris A., Nichols S., Richter D.J., Salamov A., Sequencing J.G., Bork P., Lim W.A., Manning G., Miller W.T., McGinnis W., Shapiro H., Tjian R., Grigoriev I.V., Rokhsar D. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 2008, 451:783-788.
27. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
28. Letunic I., Doerks T., Bork P. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 2012, 10.1093/nar/gkr931.
29. Lu P., Takai K., Weaver V.M., Werb Z. Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb. Perspect. Biol. 2011, 3(12). (pii: a005058).
30. Marchler-Bauer A., Lu S., Anderson J.B., Chitsaz F., Derbyshire M.K., DeWeese-Scott C., Fong J.H., Geer L.Y., Geer R.C., Gonzales N.R., Gwadz M., Hurwitz D.I., Jackson J.D., Ke Z., Lanczycki C.J., Lu F., Marchler G.H., Mullokandov M., Omelchenko M.V., Robertson C.L., Song J.S., Thanki N., Yamashita R.A., Zhang D., Zhang N., Zheng C., Bryant S.H. CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 2011, 39:D225-D229.
31. McLysaght A., Hokamp K., Wolfe K.H. Extensive genomic duplication during early chordate evolution. Nat. Genet. 2002, 31:200-204.
32. Mosher D., Xu J. Fibronectin and other adhesive glycoproteins. Biology of Extracellular Matrix 2009, 41. 10.1007/978-3-642-16555-9_2. R.P. Mecham (Ed.).
33. Niklas K.J. The evolutionary-developmental origins of multicellularity. Am. J. Bot. 2014, 101:6-25.
34. Ortiz J.A., Castillo M., del Toro E.D., Mulet J., Gerber S., Valor L.M., Sala S., Sala F., Gutiérrez L.M., Criado M. The cysteine-rich with EGF-like domains 2 (CRELD2) protein interacts with the large cytoplasmic domain of human neuronal nicotinic acetylcholine receptor alpha4 and beta2 subunits. J. Neurochem. 2005, 95:1585-1596.
35. Özbek S., Balasubramainian P., Chiquet-Ehrismann R., Tucker R.P., Adams J.C. The evolution of extracellular matrix. Mol. Biol. Cell 2010, 21:4300-4306.
36. Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8:785-786.
37. Quevillon E., Silventoinen V., Pillai S., Harte N., Mulder N., Apweiler R., Lopez R. InterProScan: protein domains identifier. Nucleic Acids Res. 2005, 33:W116-W120.
38. Robertson I., Jensen S., Handford P. TB domain proteins: evolutionary insights into the multifaceted roles of fibrillins and LTBPs. Biochem. J. 2011, 433:263-276.
39. Schwarzbauer J.E., DeSimone D.W. Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harb. Perspect. Biol. 2011, 3(7).
40. Sebé-Pedrós A., Roger A.J., Lang F.B., King N., Ruiz-Trillo I. Ancient origin of the integrin-mediated adhesion and signaling machinery. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:10142-10147.
41. Sebé-Pedrós A., Irimia M., Del Campo J., Parra-Acero H., Russ C., Nusbaum C., Blencowe B.J., Ruiz-Trillo I. Regulated aggregative multicellularity in a close unicellular relative of metazoa. Elife 2013, 2:e01287. 10.7554/eLife.01287.
42. Segade F. Molecular evolution of the fibulins: implications on the functionality of the elastic fibulins. Gene 2010, 464:17-31.
43. Srivastava M., Simakov O., Chapman J., et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 2010, 466:720-726.
44. Suga H., Chen Z., de Mendoza A., Sebé-Pedrós A., Brown M.W., Kramer E., Carr M., Kerner P., Vervoort M., Sánchez-Pons N., Torruella G., Derelle R., Manning G., Lang B.F., Russ C., Haas B.J., Roger A.J., Nusbaum C., Ruiz-Trillo I. The Capsaspora genome reveals a complex unicellular prehistory of animals. Nat. Commun. 2013, 4:2325.
45. Tan K., Duquette M., Liu J.H., Dong Y., Zhang R., Joachimiak A., Lawler J., Wang J.H. Crystal structure of the TSP-1 type 1 repeats: a novel layered fold and its biological implication. J. Cell Biol. 2002, 159:373-382.
46. Tucker R.P. The thrombospondin type 1 repeat superfamily. Int. J. Biochem. Cell Biol. 2004, 36:969-974.
47. Tucker R.P., Adams J.C. Adhesion networks of Cnidaria: a post-genomic view. Int. Rev. Cell Mol. Biol. 2014, 308:323-377.
48. Wagstaff L., Kelwick R., Decock J., Edwards D.R. The roles of ADAMTS metalloproteinases in tumorigenesis and metastasis. Front Biosci. (Landmark Ed). 2011, 16:1861-1872.
49. Whittaker C.A., Hynes R.O. Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell 2002, 13:3369-3387.
50. Whittaker C.A., Bergeron K.F., Whittle J., Brandhorst B.P., Burke R.D., Hynes R.O. The echinoderm adhesome. Dev. Biol. 2006, 300:252-266.
51. Wouters M.A., Rigoutsos I., Chu C.K., Feng L.L., Sparrow D.B., Dunwoodie S.L. Evolution of distinct EGF domains with specific functions. Protein Sci. 2005, 14:1091-1103.
52. Ye F., Kim C., Ginsberg M.H. Reconstruction of integrin activation. Blood 2012, 119:26-33.
53. Zhang X., Boot-Handford R.P., Huxley-Jones J., Forse L.N., Mould A.P., Robertson D.L., Lili, Athiyal M., Sarras M.P. The collagens of hydra provide insight into the evolution of metazoan extracellular matrices. J. Biol. Chem. 2007, 282:6792-6802.