Skip to main content
SpringerLink
Log in

Thrombospondin as a mediator of cancer cell adhesion in metastasis

  • Published:
Cancer and Metastasis Reviews Aims and scope Submit manuscript

Summary

Thrombospondin (TSP) is a 450 kDa adhesive glycoprotein. It is present in high concentrations in the platelet α-granule and can readily be secreted following platelet activation where local concentrations can be increased by 3–4 orders of magnitude. TSP is also synthesized by a variety of other cells and is incorporated into their extracellular matrix. TSP is a homotrimer with a number of functional domains, at least four of which might serve as receptor recognizing regions. The amino-terminal heparin binding domain interacts with heparin, other glycosaminoglycans and glycolipids and likely recognizes specific cell surface proteoglycans. The central disulfide cross-linked region, 210 kDa non-reduced and 70 kDa reduced, contains a peptide motif CSVTCG which is apparently responsible for binding to glycoprotein IV (CD36) with high affinity. Immediately adjacent to the calcium binding region of TSP, which undergoes considerable molecular relaxation in the absence of calcium, is an RGDA sequence. TSP has been demonstrated to bind to integrins of the αvβ3 and αIIbβ3 class. The carboxy-terminal region of TSP also contains at least one binding epitope for a cell receptor. There are 2 well characterized genes for TSP and truncated forms of TSP have been detected which have inhibitory effects on angiogenesis. Finally, TSP can interact with fibrinogen and fibronectin, perhaps on cellular surfaces, which might serve as secondary receptor-like mechanisms for TSP binding and subsequent mediation of cell adhesion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. HoltJC, NiewiarowskiS: Biochemistry of platelet α-granule proteins. Semin Hematol 22: 151–163, 1985

    PubMed  Google Scholar 

  2. LawlerJ: The structural and functional properties of thrombospondin. Blood 67: 1197–1209, 1986

    PubMed  Google Scholar 

  3. MajackRA, BornsteinP: Thrombospondin, a multi-functional extracellular matrix glycoprotein. In: ElsonE, FrazierWA, GlasorL (eds) Cell Membranes, Methods and Reviews. Plenum Publishing, New York, 1987, pp 55–77

    Google Scholar 

  4. FrazierWA: Thrombospondin: a modular adhesive glycoprotein of platelets and nucleated cells. J Cell Biol 105: 625–632, 1987

    PubMed  Google Scholar 

  5. AschAS, NachmanRL: Thrombospondin: phenomenology to function. Prog Hemost Thromb 9: 157–176, 1989

    PubMed  Google Scholar 

  6. MosherDF: Physiology of thrombospondin. Ann Rev Med 41: 85–97, 1990

    PubMed  Google Scholar 

  7. FrazierWA: Thrombospondins. Current Opinion in Cell Biology 3: 792–799, 1991

    PubMed  Google Scholar 

  8. BaenzigerNL, BrodieGN, MajerusPW: Thrombin-sensitive protein of human platelet membranes. Proc Natl Acad Sci USA 68: 240–243, 1971

    PubMed  Google Scholar 

  9. GartnerTK, GerrardJM, WhiteJG, WilliamsDC: The endogenous lectin of human platelets is an alpha-granule component. Blood 58: 153–157, 1981

    PubMed  Google Scholar 

  10. TuszynskiGP, KowalskaMA: Thrombospondin-induced adhesion of human platelets. J Clin Invest 87: 1387–1394, 1991

    PubMed  Google Scholar 

  11. TuszynskiGP, RothmanVL, MurphyA, SieglerK, KnudsenKA: Thrombospondin promotes platelet aggregation. Blood 72: 109–115, 1988

    PubMed  Google Scholar 

  12. LeungLLK: Role of thrombospondin in platelet aggregation. J Clin Invest 74: 1764–1772, 1984

    PubMed  Google Scholar 

  13. HaverstickDM, DixitVM, GrantGA, FrazierWA, SantoroSA: Localization of the hemagglutinating activity of platelet thrombospondin to a 140,000 dalton thermolytic fragment. Biochemistry 23: 5597–5603, 1984

    PubMed  Google Scholar 

  14. HaverstickDM, DixitVM, GrantGA, FrazierWA, SantoroSA: Characterization of the platelet agglutinating activity of thrombospondin. Biochemistry 24: 3128–3134, 1985

    PubMed  Google Scholar 

  15. GartnerTK, WalzDA, AikenM, Starr-SpiresL, OgilvieML: Antibodies against a 23 kDa heparin binding fragment of thrombospondin inhibit platelet aggregation. Biochem Biophys Res Commun 15: 290–295, 1984

    Google Scholar 

  16. JaffeEA, LeungLLK, NachmanRL, LevinRI, MosherDF: Thrombospondin is the endogenous lectin of human platelets. Nature 295: 246–248, 1982

    PubMed  Google Scholar 

  17. McPhersonJH, SageH, BornsteinP: Isolation and characterization of a glycoprotein secreted by aortic endothelial cells in culture. J Biol Chem 265: 11330–11336, 1981

    Google Scholar 

  18. MosherDF, DoyleMJ, JaffeEA: Synthesis and secretion of thrombospondin by cultured human endothelial cells. J Cell Biol 93: 343–348, 1982

    PubMed  Google Scholar 

  19. AschAS, LeungLLK, ShapiroJ, NachmanRL: Human brain glial cells synthesize thrombospondin. Proc Natl Acad Sci USA 83: 2904–2908, 1986

    PubMed  Google Scholar 

  20. WiknerMD, DixitVM, FrazierWA, ClarkAF: Human keratinocytes synthesize and secrete the extracellular matrix protein, thrombospondin. J Invest Dermatol 88: 207–211, 1987

    PubMed  Google Scholar 

  21. JaffeEA, RuggieroJT, LeungLLK, DoyleMJ, McKeown-LongoPJ, MosherDF: Cultured human fibroblasts synthesize and secrete thrombospondin and incorporate it into extracellular matrix. Proc Natl Acad Sci USA 80: 998–1002, 1983

    PubMed  Google Scholar 

  22. JaffeEA, RuggieroJT, FalconeDJ: Monocytes and macrophages synthesize and secrete thrombospondin. Blood 65: 79–84, 1985

    PubMed  Google Scholar 

  23. SageH, FarinFH, StrikerGE, FischerAB: Granular pneumocytes in primary culture secrete several major components of the extracellular matrix. Biochemistry 22: 2148–2155, 1983

    PubMed  Google Scholar 

  24. MajackRA, CookSC, BornsteinP: Platelet-derived growth factor and heparin-like glycosaminoglycans regulate thrombospondin synthesis and deposition in the matrix by smooth muscle cells. J Cell Biol 101: 1059–1070, 1985

    PubMed  Google Scholar 

  25. MillerRR, McDevittCA: Thrombospondin is present in articular cartilage and is synthesized by articular chondrocytes. Biochem Biophys Res Commun 153: 708–714, 1988

    PubMed  Google Scholar 

  26. RaugiGJ, LovettDH: Thrombospondin secretion by cultured human glomerular mesangial cells. Am J Pathol 129: 364–372, 1987

    PubMed  Google Scholar 

  27. NeugebauerKM, EmmettCJ, VenstromKA, ReichardtLF: Vitronectin and thrombospondin promote retinal neurite outgrowth — Developmental regulation and role of integrins. Neuron 6: 345–358, 1991

    PubMed  Google Scholar 

  28. RobeyPG, YoungMF, FisherLW, McClainTD: Thrombospondin is an osteoblast-derived component of mineralized extracellular matrix. J Cell Biol 108: 719–727, 1989

    PubMed  Google Scholar 

  29. DawesJ, ClezardinP, PrattDA: Thrombospondin in milk, other breast secretions, and breast tissue. Semin Thromb Hemost 13: 378–388, 1987

    PubMed  Google Scholar 

  30. WatkinsSC, LynchGW, KaneLP, SlayterHS: Thrombospondin expression in traumatized skeletal muscle. Correlation of appearance with post-trauma regeneration. Cell Tissue Res 261: 73–84, 1990

    PubMed  Google Scholar 

  31. WightTN, RaugiGJ, MumbySM, BornsteinP: Light microscopic immunolocation of thrombospondin in human tissues. J Histochem Cytochem 33: 295–302, 1985

    PubMed  Google Scholar 

  32. WolffR, PlowEF, GinsbergMH: Interaction of thrombospondin with resting and stimulated human platelets. J Biol Chem 261: 6840–6846, 1986

    PubMed  Google Scholar 

  33. AikenML, GinsbergMH, PlowEF: Divalent cationdependent and independent surface expression of thrombospondin on thrombin-stimulated human platelets. Blood 69: 58–64, 1987

    PubMed  Google Scholar 

  34. LeungLLK, NachmanRL: Complex formation of platelet thrombospondin with fibrinogen. J Clin Invest 70: 542–549, 1982

    PubMed  Google Scholar 

  35. Bacon-BaguleyT, KudrykBJ, WalzDA: Thrombospondin interaction with fibrinogen. J Biol Chem 262: 1927–1930, 1987

    PubMed  Google Scholar 

  36. Bacon-BaguleyT, OgilvieML, GartnerTK, WalzDA: Thrombospondin binding to specific sequences within the Aα- and Bβ-chains of fibrinogen. J Biol Chem 265: 2317–2323, 1990

    PubMed  Google Scholar 

  37. TuszynskiGP, SrivastavaS, SwitalskaHI, HoltJC, CierniewskiCS, NiewiarowskiS: The interaction of human platelet thrombospondin with fibrinogen. J Biol Chem 260: 12240–12245, 1985

    PubMed  Google Scholar 

  38. BaleMD, WestrickLG, MosherDF: Incorporation of thrombospondin into fibrin clots. J Biol Chem 260: 7506–7508, 1985

    Google Scholar 

  39. LawlerJ, HynesRO: The structure of human thrombospondin, an adhesive glycoprotein with multiple calcium-binding sites and homologies with several different proteins. J Cell Biol 103: 1635–1648, 1987

    Google Scholar 

  40. LawlerJW, SlayterHS, ColiganJE: Isolation and characterization of a high molecular weight glycoprotein from human blood platelets. J Biol Chem 253: 8609–8616, 1978

    PubMed  Google Scholar 

  41. LawlerJ, SimonsER: Cooperative binding of calcium to thrombospondin: the effect of calcium on the circular dichroism and limited tryptic digestion of thrombospondin. J Biol Chem 258: 12098–12101, 1983

    PubMed  Google Scholar 

  42. LawlerJ, DerickLH, ConnollyJE, ChenJH, ChaoFC: The structure of human platelet thrombospondin. J Biol Chem 260: 3762–3772, 1985

    PubMed  Google Scholar 

  43. GalvinNJ, DixitVM, O'RourkeKM, SantoroSA, GrantGA, FrazierWA: Mapping of epitopes for monoclonal antibodies against human platelet thrombospondin with electron microscopy and high sensitivity amino acid sequencing. J Cell Biol 101: 1434–1441, 1985

    PubMed  Google Scholar 

  44. LawlerJ, ConnollyJE, FerroP, DerickLH: Thrombin and chymotrypsin interactions with thrombospondin. Ann NY Acad Sci 485: 273–287, 1986

    PubMed  Google Scholar 

  45. DardikR, LahavJ: The structure of endothelial cell thrombospondin. Characterization of the heparin-binding domains. Eur J Biochem 168: 347–355, 1987

    PubMed  Google Scholar 

  46. LahavJ, DardikR, SteinO: Endothelial cell thrombospondin and its possible role in cell adhesion. Semin Thromb Hemost 13: 352–360, 1987

    PubMed  Google Scholar 

  47. ClezardinP, BourdillonMC, HunterNR, McGregorJL: Cell attachment and fibrinogen binding properties of platelet and endothelial cell thrombospondin are not affected by structural differences in the 70 and 18 kDa protease-resistant domains. FEBS Lett 228: 215–218, 1988

    PubMed  Google Scholar 

  48. ClezardinP, HunterNR, LawlerJ, DawesJ, McGregorJL: Production, characterization, and use of monoclonal antibodies directed against human blood platelet thrombospondin: immunologic comparison with human endothelial and fibroblast thrombospondins. Semin Thromb Hemost 13: 261–275, 1987

    PubMed  Google Scholar 

  49. NishimuraH, KawabataS, KisielW, HaseS, IkenakaT, TakaoT, ShimonishiY, IwanagaS: Identification of a disaccharide (xyl-glc) and a trisaccharide (xyl2-glc) O-glycosidically linked to a serine residue in the first epidermal growth factor-like domain of human factors VII and IX and protein Z and bovine protein Z. J Biol Chem 264: 20320–20325, 1989

    PubMed  Google Scholar 

  50. NishimuraH, YamashitaS, ZengZ, WalzDA, IwanagaS: Evidence for the existence of O-linked sugar chains (xylose-glucose and (xylose)2-glucose) in bovine thrombospondin. J Biochem 111: 460–464, 1992

    PubMed  Google Scholar 

  51. HennessySW, FrazierBA, KimDD, DeckwerthTL, BaumgartelDM, RotweinB, FrazierWA: Complete thrombospondin mRNA sequence includes potential regulatory sites in the 3′ untranslated region. J Cell Biol 108: 729–736, 1989

    PubMed  Google Scholar 

  52. LahertyCD, GiermanTM, DixitVM: Characterization of the promoter region of the human thrombospondin gene. J Biol Chem 264: 11222–11227, 1989

    PubMed  Google Scholar 

  53. JaffeE, BornsteinP, DistecheCM: Mapping of the thrombospondin gene to human chromosome 15 and mouse chromosome 2 byin situ hydridization. Genomics 7: 123–126, 1990

    PubMed  Google Scholar 

  54. WolfFW, EddyRL, ShowsTB, DixitVM: Structure and chromosomal localization of the human thrombospondin gene. Genomics 6: 685–691, 1990

    PubMed  Google Scholar 

  55. BornsteinP, AlfiD, DevarayaluL, FramsonP, LiP: Characterization of the mouse thrombospondin gene and evaluation of the role of the first intron in human gene expression. J Biol Chem 265: 16691–16698, 1990

    PubMed  Google Scholar 

  56. BornsteinP, O'RourkeK, WikstromK, WolfFW, KarzR, LiP, DixitVM: A second expressed thrombospondin gene [Thbs2] exists in the mouse genome. J Biol Chem 266: 12821–12829, 1991

    PubMed  Google Scholar 

  57. LawlerJ, DuquetteM, FerroP: Cloning and sequencing of chicken thrombospondin. J Biol Chem 266: 8039–8043, 1991

    PubMed  Google Scholar 

  58. DixitVM, HaverstickDM, O'RourkeKM, HennessySW, GrantGA, SantoroSA, FrazierWA: A monoclonal antibody against human thrombospondin inhibits platelet aggregation. Proc Natl Acad Sci USA 82: 3472–3476, 1985

    PubMed  Google Scholar 

  59. LawlerJ, HynesRO: An integrin receptor on normal and thrombasthenic platelets that binds thrombospondin. Blood 74: 2022–2027, 1989

    PubMed  Google Scholar 

  60. KarczewskiJ, KnudsenKA, SmithL, MurphyA, RothmanVL, TuszynskiGP: The interaction of thrombospondin with platelet glycoprotein GPIIb-IIIa. J Biol Chem 264: 21322–21326, 1989

    PubMed  Google Scholar 

  61. AschAS, LeungLLK, PollyMJ, NachmanRL: Platelet membrane topography: co-localization of thrombospondin and fibrinogen with the glycoprotein IIb-IIIa complex. Blood 66: 926–933, 1985

    PubMed  Google Scholar 

  62. BaleMD, MosherDF: Effects of thrombospondin on fibrin polymerization and structure. J Biol Chem 261: 862–868, 1986

    PubMed  Google Scholar 

  63. LynchGW, SlayterHS, MillerBE, McDonaghJ: Characterization of thrombospondin as a substrate for factor XIII transglutaminase. J Biol Chem 262: 1772–1778, 1987

    PubMed  Google Scholar 

  64. BaleMD: Noncovalent and covalent interactions of thrombospondin with polymerizing fibrin. Semin Thromb Hemost 13: 326–334, 1987

    PubMed  Google Scholar 

  65. GoodDJ, PolveriniPJ, RastinejadF, LeBeauMM, LemonsRS, FrazierWA, BouckNP: A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc Natl Acad Sci USA 87: 6624–6628, 1990

    PubMed  Google Scholar 

  66. MajackRA, GoodmanLV, DixitVM: Cell surface thrombospondin is functionally essential for vascular smooth muscle cell proliferation. J Cell Biol 106: 415–422, 1988

    PubMed  Google Scholar 

  67. MajackRA, CookSC, BornsteinP: Regulation of smooth muscle cell growth by components of the extracellular matrix: an autocrine role for thrombospondin. Proc Natl Acad Sci USA 83: 9050–9054, 1986

    PubMed  Google Scholar 

  68. TarabolettiGD, RobertsDD, LiottaLA, GiavazziR: Platelet thrombospondin modulates endothelial cell adhesion, motility, and growth: a potential angiogenesis regulatory factor. J Cell Biol 111: 765–772, 1990

    PubMed  Google Scholar 

  69. Iruela-ArispeML, HasselaarP, SageH: Differential expression of extracellular proteins is correlated with angiogenesisin vitro. Lab Invest 64: 174–186, 1991

    PubMed  Google Scholar 

  70. Iruela-ArispeML, BornsteinP, SageH: Thrombospondin exerts an antiangiogenic effect on cord formation by endothelial cellsin vitro. Proc Natl Acad Sci USA 88: 5026–5030, 1991

    PubMed  Google Scholar 

  71. TarabolettiGD, RobertsDD, LiottaLA: Thrombospondin-induced tumor cell migration: haptotaxis and chemotaxis are mediated by different molecular domains. J Cell Biol 105: 2409–2415, 1987

    PubMed  Google Scholar 

  72. MansfieldPJ, BoxerLA, SuchardSJ: Thrombospondin stimulates motility of human neutrophils. J Cell Biol 111: 3077–3086, 1990

    PubMed  Google Scholar 

  73. Murphy-UllrichJE, HookM: Thrombospondin modulates focal adhesions in endothelial cells. J Cell Biol 109: 1309–1319, 1989

    PubMed  Google Scholar 

  74. BaenzigerNL, BrodieGN, MajerusPW: Isolation and properties of a thrombin-sensitive protein of human platelets. J Biol Chem 247: 2723–2731, 1972

    PubMed  Google Scholar 

  75. TakahashiK, AikenML, FentonJW, WalzDA: Thrombospondin fragmentation by α-thrombin and resistance to γ-thrombin. Biochem J 224: 673–676, 1984

    PubMed  Google Scholar 

  76. DanishefskyJ, AlexanderRJ, DetwilerTC: Formation of a stable complex of thrombin and the secreted platelet protein glycoprotein G (thrombin-sensitive protein, thrombospondin) by thiol-disulfide exchange. Biochemistry 23: 4984–4990, 1984

    PubMed  Google Scholar 

  77. SpezialeMV, DetwilerTC: Free thiols of platelet thrombospondin. J Biol Chem 265: 17859–17867, 1990

    PubMed  Google Scholar 

  78. SilversteinRL, LeungLLK, HarpelPC, NachmanRL: Complex formation of platelet thrombospondin with plasminogen. J Clin Invest 74: 1625–1633, 1984

    PubMed  Google Scholar 

  79. SilversteinRL, NachmanRL, LeungLLK, HarpelPC: Activation of immobilized plasminogen by tissue activator: multimolecular complex formation. J Biol Chem 260: 10346–10352, 1985

    PubMed  Google Scholar 

  80. DePoliP, Bacon-BaguleyT, Kendra-FranczakS, CederholmMT, WalzDA: Thrombospondin interaction with plasminogen. Evidence for binding to a specific region of the kringle structure of plasminogen. Blood 73: 976–982, 1989

    PubMed  Google Scholar 

  81. HoggPJ, MosherDF: Thrombospondin is a slow tightbinding inhibitor of plasmin. Biochemistry 31: 265–269, 1992

    PubMed  Google Scholar 

  82. LawlerJ, HynesRO: Structural organization of the thrombospondin molecule. Semin Thromb Hemost 13: 245–254, 1987

    Google Scholar 

  83. DixitVM, GrantGA, SantoroSA, FrazierWA: Isolation and characterization of a heparin-binding domain from the amino terminus of platelet thrombospondin. J Biol Chem 259: 10100–10105, 1984

    PubMed  Google Scholar 

  84. AikenM, CiaglowskiRE, WalzDA: Isolation and identification of a 23,000 dalton heparin binding fragment from the amino terminus of bovine thrombospondin. Arch Biochem Biophys 250: 257–262, 1986

    PubMed  Google Scholar 

  85. RobertsDD, SherwoodJA, GinsburgV: Platelet thrombospondin mediates attachment and spreading of human melanoma cells. J Cell Biol 104: 131–139, 1987

    PubMed  Google Scholar 

  86. Murphy-UllrichJE, MosherDF: Interactions of thrombospondin with endothelial cells: receptor-mediated binding and degradation. J Cell Biol 105: 1603–1611, 1987

    PubMed  Google Scholar 

  87. GuoN-H, KrutzschHC, NegreE, VogelT, BlakeDA, RobertsDD: 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, 1992

    PubMed  Google Scholar 

  88. RobertsDD, HaverstickDM, DixitVM, FrazierWA, SantoroSA, GinsburgV: The platelet glycoprotein thrombospondin binds specifically to sulfated glycolipids. J Biol Chem 260: 9405–9411, 1985

    PubMed  Google Scholar 

  89. RobertsDD: Interactions of thrombospondin with sulfated glycolipids and proteoglycans of human melanoma cells. Cancer Res 48: 6785–6793, 1988

    PubMed  Google Scholar 

  90. ZabrenetzkyVS, KohnEC, RobertsDD: Suramin inhibits laminin- and thrombospondin-mediated melanoma cell adhesion and migration and binding of these adhesive proteins to sulfatide. Cancer Res. 50: 5937–5942, 1990

    PubMed  Google Scholar 

  91. KaesbergPR, ErshlerWB, EskoJD, MosherDF: Chinese hamster ovary cell adhesion to human platelet thrombospondin is dependent on cell surface heparin sulfate proteoglycan. J Clin Invest 83: 994–1001, 1989

    PubMed  Google Scholar 

  92. SunX, MosherDF, RapraegerA: Heparin sulfate-mediated binding of epithelial cell surface proteoglycan to thrombospondin. J Biol Chem 264: 2885–2889, 1989

    PubMed  Google Scholar 

  93. DardikR, LahavJ: Multiple domains are involved in the interaction of endothelial cell thrombospondin with fibronectin. Eur J Biochem 185: 581–588, 1989

    PubMed  Google Scholar 

  94. RapraegerA: Transforming growth factor (type β) promotes the addition of chondroitin sulfate chains to the cell surface proteoglycan (syndecan) of mouse mammary epithelia. J Cell Biol 109: 2509–2518, 1989

    PubMed  Google Scholar 

  95. LawlerJ, FerroP, DuquetteM: Expression and mutagenesis of thrombospondin. Biochemistry 31: 1173–1180, 1992

    PubMed  Google Scholar 

  96. RobsonKJH, HallJRS, JenningsMW, HarrisTJR, MarshK, NewboldCI, TateVE, WeatherallDJ: A highly conserved amino acid sequence in thrombospondin, properdin, and in proteins from sporozoites and blood stages of a human parasite. Nature 335: 79–82, 1988

    PubMed  Google Scholar 

  97. AschAS, BarnwellJ, SilversteinRL, NachmanRL: Isolation of the thrombospondin membrane receptor. J Clin Invest 79: 1054–1061, 1987

    PubMed  Google Scholar 

  98. SilversteinRL, AschAS, NachmanRL: Glycoprotein IV mediates thrombospondin-dependent platelet-monocyte and platelet-U937 cell adhesion. J Clin Invest 84: 546–552, 1989

    PubMed  Google Scholar 

  99. VaraniJ, NickoloffBJ, RiserBL, MitraRS, O'RourkeK, DixitVM: Thrombospondin-induced adhesion of human keratinocytes. J Clin Invest 81: 1537–1544, 1988

    PubMed  Google Scholar 

  100. ImamuraN, InadaT, MtasiwaDM, KuramotoA: Demonstration of thrombospondin (TSP) receptor on the cell surface of acute megakaryoblastic leukemia. Am J Hematol 31: 142–143, 1989

    PubMed  Google Scholar 

  101. VolpesR, van denOordJJ, DesmetVJ: Adhesive molecules in liver disease. Immunohistochemical distribution of thrombospondin receptors in chronic HBV infection. J Hepatol 10: 297–304, 1990

    PubMed  Google Scholar 

  102. KiefferN, BettaiebA, LegrandC, CoulombelL, VainchenkerW, EdelmanL, Brenton-GoriusJ: Developmentally regulated expression of a 78 kDa erythroblast membrane glycoprotein immunologically related to the platelet thrombospondin receptor. Biochem J 262: 835–842, 1989

    PubMed  Google Scholar 

  103. TuszynskiGP, RothmanVL, DeutchAH, HamiltonBK, EyalJ: Biological activities of peptides and peptide analogues derived from common sequences present in thrombospondin, properdin, and malarial proteins. J Cell Biol 116: 209–217, 1992

    PubMed  Google Scholar 

  104. AschAS, SilbigerS, HeimerE, NachmanRL: Thrombospondin sequence motif (CSVTCG) is responsible for CD36 binding. Biochem Biophys Res Commun 182: 1208–1217, 1992

    PubMed  Google Scholar 

  105. TuszynskiGP, GasicTB, RothmanVL, KnudsenKA, GasicGJ: Thrombospondin, a potentiator of tumor cell metastasis. Cancer Res 47: 4130–4133, 1987

    PubMed  Google Scholar 

  106. HynesRO: Integrins, a family of cell surface receptors. Cell 48: 549–555, 1987

    PubMed  Google Scholar 

  107. RuoslahtiE, PierschbacherMD: New perspectives in cell adhesion: RGD and integrins. Science 238: 491–497, 1987

    PubMed  Google Scholar 

  108. PhillipsDR, CharoIF, PariseLV, FitzgeraldLA: The platelet membrane glycoprotein IIb-IIIa complex. Blood 71: 831–843, 1988

    PubMed  Google Scholar 

  109. RybakME: Glycoproteins IIb and IIIa and platelet thrombospondin in a liposome model of platelet aggregation. Thromb Haemost 55: 240–245, 1986

    PubMed  Google Scholar 

  110. KnudsenKA, SmithL, SmithS, KarczewskiJ, TuszynskiGP: Role of IIb-IIIa-like glycoproteins in cell-substratum adhesion of human melanoma cells. J Cell Physiol 136: 471–478, 1988

    PubMed  Google Scholar 

  111. TuszynskiGP, KarczewskiJ, SmithL, MurphyA, RothmanVL, KnudsenKA: The GPIIb-IIIa-like complex may function as a human melanoma cell adhesion receptor for thrombospondin. Exp Cell Res 182: 473–481, 1989

    PubMed  Google Scholar 

  112. LawlerJ, WeinsteinR, HynesRO: Cell attachment to thrombospondin: the role of Arg-Gly-Asp, calcium, and integrin receptors. J Cell Biol 107: 2351–2361, 1988

    PubMed  Google Scholar 

  113. AschAS, TeplerJ, SilbigerS, NachmanRL: Cellular attachment to thrombospondin. J Biol Chem 266: 1740–1745, 1991

    PubMed  Google Scholar 

  114. LongMW, DixitVM: Thrombospondin functions as a cytoadhesion molecule for human hematopoietic progenitor cells. Blood 75: 2311–2318, 1990

    PubMed  Google Scholar 

  115. YabkowitzR, DixitVM: Human carcinoma cells bind thrombospondin through a Mr 80,000/105,000 receptor. Cancer Res 51: 3648–3656, 1991

    PubMed  Google Scholar 

  116. VaraniJ, DixitVM, FligielSEG, McKeeverPE, CareyTE: Thrombospondin-induced attachment and spreading of human squamous carcinoma cells. Exp Cell Res 167: 376–390, 1986

    PubMed  Google Scholar 

  117. RiserBL, VaraniJ, O'RourkeK, DixitVM: Thrombospondin binding by human squamous carcinoma and melanoma cells: relationship to biological activity. Exp Cell Res 174: 319–329, 1988

    PubMed  Google Scholar 

  118. Zeng Z: Thrombospondin interactions with fibrinogen and platelets. Ph.D. Dissertation, Wayne State University, 1991

  119. Li Y: A monoclonal antibody against the central 70 kDa region of thrombospondin which blocks platelet aggregation. Ph.D. Dissertation. Wayne State University, 1992

  120. AliIV, HynesRO: Effects of LETS glycoprotein on cell motility. Cell 14: 439–446, 1978

    PubMed  Google Scholar 

  121. HayashiM, SchlesingerDH, KennedyDW, YamadaKM: Isolation and characterization of a heparin-binding domain of cellular fibronectin. J Biol Chem 255: 10017–10020, 1980

    PubMed  Google Scholar 

  122. SekiguchiK, HakomoriS: Functional domain structure of fibronectin. Proc Natl Acad Sci USA 77: 2661–2665, 1980

    PubMed  Google Scholar 

  123. YamadaKM, KennedyDW, KimataK, PrattRM: Characterization of fibronectin interactions with glycosaminoglycans and identification of active proteolytic fragments. J Biol Chem 255: 6055–6063, 1980

    PubMed  Google Scholar 

  124. SmithDE, FurchtTL: Localization of two unique heparin binding domains of human plasma fibronectin with monoclonal antibodies. J Biol Chem 257: 6518–6523, 1982

    PubMed  Google Scholar 

  125. WagnerDD, HynesRO: Topological arrangement of the major structural features of fibronectin. J Biol Chem 255: 4304–4312, 1980

    PubMed  Google Scholar 

  126. FurieMB, FreyAB, RifkinDB: Location of a gelatin-binding region of human plasma fibronectin. J Biol Chem 255: 4391–4394, 1980

    PubMed  Google Scholar 

  127. AlexanderSS, ColonnaG, EdelhockH: The structure and stability of human plasma cold-insoluble globulin. J Biol Chem 254: 1501–1505, 1979

    PubMed  Google Scholar 

  128. Zafar RS, Zeng Z, Walz DA: Localization of two binding domains for thrombospondin within fibronectin. Arch Biochem Biophys. In press

  129. LeungLLK, NachmanRL, HarpelPC: Complex formation of platelet thrombospondin with histidine-rich glycoprotein. J Clin Invest 73: 5–12, 1984

    PubMed  Google Scholar 

  130. De la Cadena RA, Wyshock EG, Walz DA, Colman RW: Structural determinants of the binding of human high molecular weight kininogen (HK) to platelet thrombospondin (TSP). Thromb Hemost 65: 699a, 1991

  131. ClezardinP, MalavalL, EhrenspergerAS, DelmasPD, DechavanneJL, McGregorJL: Complex formation of human thrombospondin with osteonectin. Eur J Biochem 175: 275–284, 1988

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology, Wayne State University School of Medicine, 540 E. Canfield, 48201, Detroit, MI, USA

    Daniel A. Walz

Authors
  1. Daniel A. Walz
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Walz, D.A. Thrombospondin as a mediator of cancer cell adhesion in metastasis. Cancer Metast Rev 11, 313–324 (1992). https://doi.org/10.1007/BF01307185

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01307185

Key words

Search

Navigation