The evolution of thrombospondins and their ligand-binding activities

Molecular Biology and Evolution

Volumn 27, Issue 9, 2010, Pages 2187-2197

  Bentley, Amber A ^a   Adams, Josephine C ^a,b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

coiled coil; collagen; extracellular matrix; integrins; thrombospondins

Indexed keywords

CD36 ANTIGEN; FIBRILLAR COLLAGEN; GLYCOSAMINOGLYCAN; HEPARAN; INTEGRIN; THROMBOSPONDIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; EXTRACELLULAR MATRIX; GENE DUPLICATION; GENE LOSS; LIGAND BINDING; METAZOON; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; TISSUE ENGINEERING;

ANIMALS; EVOLUTION, MOLECULAR; EXTRACELLULAR MATRIX; HUMANS; INTEGRINS; PHYLOGENY; THROMBOSPONDINS;

DEUTEROSTOMIA; MAMMALIA; METAZOA; PROTOSTOMIA; VERTEBRATA;

EID: 77955978745     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq107     Document Type: Article

References (84)

1. Adams JC. 2001. Thrombospondins: multifunctional regulators of cell interactions. Annu Rev Cell Dev Biol. 17:25-51
2. Adams JC. 2004. Functions of the conserved thrombospondin carboxy-terminal cassette in cell-extracellular matrix interactions and signaling. Int J Biochem Cell Biol. 36:1102-1114
3. Adams JC, Bentley AA, Kvansakul M, Hatherley D, Hohenester E. 2008. Extracellular matrix retention of thrombospondin 1 is controlled by its conserved C-terminal region. J Cell Sci. 121:784-795
4. Adams JC, Monk R, Taylor AL, Ozbek S, Fascetti N, Baumgartner S, Engel J. 2003. Characterisation of Drosophila thrombospondin defines an early origin of pentameric thrombospondins. J Mol Biol. 328:479-494
5. Adams MD, Celniker SE, Holt RA, et al. (195 co-authors). 2000. The genome sequence of Drosophila melanogaster. Science 287:2185-2195
6. Akimana C, Lafontaine ER. 2007. The Moraxella catarrhalis outer membrane protein CD contains two distinct domains specifying adherence to human lung cells. FEMS Microbiol Lett. 271:12-19
7. Anilkumar N, Annis DS, Mosher DF, Adams JC. 2002. Trimeric assembly of the C-terminal region of thrombospondin-1 or thrombospondin-2 is necessary for cell spreading and fascin spike organisation. J Cell Sci. 115:2357-2366
8. Asch AS, Silbiger S, Heimer E, Nachman RL. 1992. Thrombospondin sequence motif (CSVTCG) is responsible for CD36 binding. Biochem Biophys Res Commun. 182:1208-1217
9. Barclay AN, Brown MH. 2006. The SIRP family of receptors and immune regulation. Nat Rev Immunol. 6:457-464
10. Bauer DJ. 2007. The Daphnia Genomics Consortium Meeting: the genome biology of the model crustacean Daphnia pulex. Expert Rev Proteomics. 4:601-602
11. Bornstein P, Agah A, Kyriakides TR. 2004. The role of thrombo-spondins 1 and 2 in the regulation of cell-matrix interactions, collagen fibril formation, and the response to injury. Int J Biochem Cell Biol. 36:1115-1125
12. Calzada MJ, Zhou L, Sipes JM, Zhang J, Krutzsch HC, Iruela-Arispe ML, Annis DS, Mosher DF, Roberts DD. 2004. a4b1 integrin mediates selective endothelial cell responses to thrombospondins 1 and 2 in vitro and modulates angiogenesis in vivo. Circ Res. 94:462-470
13. Carlson CB, Bernstein DA, Annis DS, Misenheimer TM, Hannah BL, Mosher DF, Keck JL. 2005. Structure of the calcium-rich signature domain of human thrombospondin-2. Nat Struct Mol Biol. 12:910-914
14. Cássaro CM, Dietrich CP. 1977. Distribution of sulfated mucopolysaccharides in invertebrates. J Biol Chem. 252: 2254-2261
15. C. elegans Sequencing Consortium. 1998. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012-2018
16. Chakravarti R, Adams JC. 2006. Comparative genomics of the syndecans defines an ancestral genomic context associated with matrilins in vertebrates. BMC Genomics. 7:83.
17. Chanana B, Graf R, Koledachkina T, Pflanz R, Vorbrüggen G. 2007. AlphaPS2 integrin-mediated muscle attachment in Drosophila requires the ECM protein thrombospondin. Mech Dev. 124:463-475
18. Chen FH, Thomas AO, Hecht JT, Goldring MB, Lawler J. 2005. Cartilage oligomeric matrix protein/thrombospondin 5 supports chondrocyte attachment through interaction with integrins. J Biol Chem. 280:32655-32661
19. Chen JY, Oliveri P, Gao F, Dornbos SQ, Li CW, Bottjer DJ, Davidson EH. 2002. Precambrian animal life: probable developmental and adult cnidarian forms from Southwest China. Dev Biol. 248:182-196
20. Christensen A, Svensson K, Persson S, Jung J, Michalak M, Widell S, Sommarin M. 2008. Functional characterization of Arabidopsis calreticulin1a: a key alleviator of endoplasmic reticulum stress. Plant Cell Physiol. 49:912-924
21. Dehal P, Boore JL. 2005. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3:e314.
22. Dehal P, Satou Y, Campbell RK, et al. (87 co-authors). 2002. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157-2167
23. Delsuc F, Brinkmann H, Chourrout D, Philippe H. 2006. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965-968
24. Dereeper A, Guignon V, Blanc G, et al. (12 co-authors). 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36:W465-W469
25. Dodd RB, Drickamer K. 2001. Lectin-like proteins in model organisms: implications for evolution of carbohydrate-binding activity. Glycobiology 11:71R-9R.
26. Doolittle RF. 2009. Step-by-step evolution of vertebrate blood coagulation. Cold Spring Harb Symp Quant Biol. Advance Access published August 10, 2010, doi:10.1101/sqb.2009.74.001.
27. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797
28. Efimov VP, Lustig A, Engel J. 1994. The thrombospondin-like chains of cartilage oligomeric matrix protein are assembled by a fivestranded alpha-helical bundle between residues 20 and 83. FEBS Lett. 341:54-58
29. Eichinger L, Pachebat JA, Glöckner G, et al. (97 co-authors). 2005. The genome of the social amoeba Dictyostelium discoideum. Nature 435:43-57
30. Exposito JY, Larroux C, Cluzel C, Valcourt U, Lethias C, Degnan BM. 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
31. Fuentes-Prior P, Fujikawa K, Pratt KP. 2002. New insights into binding interfaces of coagulation factors V and VIII and their homologues lessons from high-resolution crystal structures. Curr Protein Pept Sci. 3:313-339
32. Hegedus D, Erlandson M, Gillott C, Toprak U. 2009. New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol. 54:285-302
33. Holden P, Meadows RS, Chapman KL, Grant ME, Kadler KE, Briggs MD. 2001. Cartilage oligomeric matrix protein interacts with type IX collagen, and disruptions to these interactions identify a pathogenetic mechanism in a bone dysplasia family. J Biol Chem. 276:6046-6055
34. Honeybee Genome Sequencing Consortium. 2006. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931-949
35. Hori I. 1991. Role of fixed parenchyma cells in blastema formation of the planarian Dugesia japonica. Int J Dev Biol. 35:101-118
36. Huhtala M, Heino J, Casciari D, de Luise A, Johnson MS. 2005. Integrin evolution: insights from ascidian and teleost fish genomes. Matrix Biol. 24:83-95
37. Gao AG, Lindberg FP, Dimitry JM, Brown EJ, Frazier WA. 1996. Integrin-associated protein is a receptor for the C-terminal domain of thrombospondin. J Biol Chem. 271:21-24
38. Goicoechea S, Orr AW, Pallero MA, Eggleton P, Murphy-Ullrich JE. 2000. Thrombospondin mediates focal adhesion disassembly through interactions with cell surface calreticulin. J Biol Chem. 275:36358-36368
39. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704
40. Guo NH, Krutzsch HC, Nègre E, Vogel T, Blake DA, Roberts DD. 1992. Heparin-and sulfatide-binding peptides from the type I repeats of human thrombospondin promote melanoma cell adhesion. Proc Natl Acad Sci\USA. 89:3040-3044
41. Isenberg JS, Jia Y, Fukuyama J, Switzer CH, Wink DA, Roberts DD. 2007. Thrombospondin-1 inhibits nitric oxide signaling via CD36 by inhibiting myristic acid uptake. J Biol Chem. 282: 15404-15415
42. Isenberg JS, Ridnour LA, Dimitry J, Frazier WA, Wink DA, Roberts DD. 2006. CD47 is necessary for inhibition of nitric oxide-stimulated vascular cell responses by thrombospondin-1. J Biol Chem. 281:26069-26080
43. Kiedzierska A, Smietana K, Czepczynska H, Otlewski J. 2007. Structural similarities and functional diversity of eukaryotic discoidin-like domains. Biochim Biophys Acta. 1774:1069-1078
44. King N, Westbrook MJ, Young SL, et al. (36 co-authors). 2008. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoa. Nature 451:783-788
45. Kvansakul M, Adams JC, Hohenester E. 2004. Structure of a thrombospondin C-terminal fragment reveals a novel calcium core in the type 3 repeats. EMBO J. 23:1223-1233
46. Kyriakides TR, Zhu YH, Smith LT, et al. (12 co-authors). 1998. Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J Cell Biol. 140:419-430
47. Lapraz F, Röttinger E, Duboc V, et al. (16 co-authors). 2006. RTK and TGF-beta signaling pathways genes in the sea urchin genome. Dev Biol. 300:132-152
48. Lawler J, Hynes RO. 1989. An integrin receptor on normal and thrombasthenic platelets that binds thrombospondin. Blood 74:2022-2027
49. Lawler J, Sunday M, Thibert V, Duquette M, George EL, Rayburn H, Hynes RO. 1998. Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia. J Clin Invest. 101:982-992
50. Madeo F, Durchschlag M, Kepp O, Panaretakis T, Zitvogel L, Fröhlich KU, Kroemer G. 2009. Phylogenetic conservation of the preapoptotic calreticulin exposure pathway from yeast to mammals. Cell Cycle. 8:639-642
51. McKenzie P, Chadalavada SC, Bohrer J, Adams JC. 2006. Phyloge-nomic analysis of vertebrate thrombospondins reveals fish-specific paralogues, ancestral gene relationships and a tetrapod innovation. BMC Evol Biol. 6:33.
52. Merritt TM, Bick R, Poindexter BJ, Alcorn JL, Hecht JT. 2007. Unique matrix structure in the rough endoplasmic reticulum cisternae of pseudoachondroplasia chondrocytes. Am J Pathol. 170:293-300
53. Müller WE, Thakur NL, Ushijima H, et al. (11 co-authors). 2004. Matrix-mediated canal formation in primmorphs from the sponge Suberites domuncula involves the expression of a CD36 receptor-ligand system. J Cell Sci. 117:2579-2590
54. Notredame C, Higgins D, Heringa J. 2000. T-Coffee: a novel method for multiple sequence alignments. J Mol Biol. 302:205-217
55. Page AP, Johnstone IL. 2007. The cuticle. WormBook. 19:1-15
56. PongsomboonS,WongpanyaR,TangS,ChalorsrikulA,Tassanakajon A. 2008. Abundantly expressed transcripts in the lymphoid organ of the black tiger shrimp, Penaeus monodon, and their implication in immune function. Fish Shellfish Immunol. 25:485-493
57. Posey KL, Hankenson K, Veerisetty AC, Bornstein P, Lawler J, Hecht JT. 2008. Skeletal abnormalities in mice lacking extracellular matrix proteins, thrombospondin-1, thrombospondin-3, throm-bospondin-5, and type IX collagen. Am J Pathol. 172:1664-1674
58. Putnam NH, Butts T, Ferrier DE, et al. (37 co-authors). 2008. The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064-1071
59. Putnam NH, Srivastava M, Hellsten U, et al. (19 co-authors). 2007. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86-94
60. Ribeiro SM, Poczatek M, Schultz-Cherry S, Villain M, Murphy-Ullrich JE. 1999. The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta. J Biol Chem. 274:13586-13593
61. Rigden DJ, Galperin MY. 2004. The DxDxDG motif for calcium binding: multiple structural contexts and implications for evolution. J Mol Biol. 343:971-984
62. Robb SM, Ross E, Sánchez Alvarado A. 2008. SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res. 36:D599-D606
63. Rokas A. 2008. The molecular origins of multicellular transitions. Curr Opin Genet Dev. 18:472-478
64. Satou Y, Yamada L, Mochizuki Y, et al. (14 co-authors). 2002. A cDNA resource from the basal chordate Ciona intestinalis. Genesis 33:153-154
65. Schéele S, Nyström A, Durbeej M, Talts JF, Ekblom M, Ekblom P. 2007. Laminin isoforms in development and disease. J Mol Med. 85:825-836
66. Schultz-Cherry S, Chen H, Mosher DF, Misenheimer TM, Krutzsch HC, Roberts DD, Murphy-Ullrich JE. 1995. Regulation of transforming growth factor-beta activation by discrete sequences of thrombospondin 1. J Biol Chem. 1270: 7304-7310
67. Sea Urchin Genome Sequencing Consortium. 2006. The genome of the sea urchin Strongylocentrotus purpuratus. Science 314: 941-952
68. Small KS, Brudno M, Hill MM, Sidow A. 2007. A haplome alignment and reference sequence of the highly polymorphic Ciona savignyi genome. Genome Biol. 8:R41.
69. Srivastava M, Begovic E, Chapman J, et al. (21 co-authors). 2008. The Trichoplax genome and the nature of placozoans. Nature 454:955-960
70. Stein LD, Bao Z, Blasiar D, et al. (36 co-authors). 2003. The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol. 1:E45.
71. Subramanian A, Wayburn B, Bunch T, Volk T. 2007. Thrombo-spondin-mediated adhesion is essential for the formation of the myotendinous junction in Drosophila. Development. 134: 1269-1278
72. Sun YD, Zhao XF, Kang CJ, Wang JX. 2006. Molecular cloning and characterization of Fc-TSP from the Chinese shrimp Fennerpe-naeus chinensis. Mol. Immunol. 43:1202-1210
73. Tan K, Duquette M, Joachimiak A, Lawler J. 2009. The crystal structure of the signature domain of cartilage oligomeric matrix protein: implications for collagen, glycosaminoglycan and integrin binding. FASEB J. 23:2490-2501
74. Tan K, Duquette M, Liu JH, Dong Y, Zhang R, Joachimiak A, Lawler J, Wang JH. 2002. Crystal structure of the TSP-1 type 1 repeats: a novel layered fold and its biological implication. J Cell Biol. 159:373-382
75. Tan K, Duquette M, Liu JH, Zhang R, Joachimiak A, Wang JH, Lawler J. 2006. The structures of the thrombospondin-1 N-terminal domain and its complex with a synthetic pentameric heparin. Structure 14:33-42
76. Tribolium Genome Sequencing Consortium. 2008. The genome of the model beetle and pest Tribolium castaneum. Nature 453:949-955
77. Tucker RP, Chiquet-Ehrismann R. 2009. Evidence for the evolution of tenascin and fibronectin early in the chordate lineage. Int J Biochem Cell Biol. 41:424-434
78. Vakonakis I, Campbell ID. 2007. Extracellular matrix: from atomic resolution to ultrastructure. Curr Opin Cell Biol. 19:578-583
79. Venkatesh B, Kirkness EF, Loh YH, et al. (12 co-authors). 2007. Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLoS Biol. 5:e101.
80. Voland C, Serre CM, Delmas P, Clezardin P. 2000. Platelet-osteosarcoma cell interaction is mediated through a specific fibrinogen-binding sequence located within the N-terminal domain of thrombospondin 1. J Bone Miner Res. 15:361-368
81. Whittaker CA, Bergeron KF, Whittle J, Brandhorst BP, Burke RD, Hynes RO. 2006. The echinoderm adhesome. Dev Biol. 300: 252-266
82. Yamano K, Qiu GF, Unuma T. 2004. Molecular cloning and ovarian expression profiles of thrombospondin, a major component of cortical rods in mature oocytes of penaeid shrimp, Marsupe-naeus japonicus. Biol Reprod. 70:1670-1678
83. Young GD, Murphy-Ullrich JE. 2004. The tryptophan-rich motifs of the thrombospondin type 1 repeats bind VLAL motifs in the latent transforming growth factor-beta complex. J Biol Chem. 279:47633-47642
84. Zhang X, Lawler J. 2007. Thrombospondin-based antiangiogenic therapy. Microvasc Res. 74:90-99