Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth

Journal of Cellular and Molecular Medicine

Volumn 6, Issue 1, 2002, Pages 1-12

  Lawler, Jack ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Angiogenesis; Matrix metalloproteinase; Neoplasia; Thrombospondin; Transforming growth factor

Indexed keywords

ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; ENZYME INHIBITOR; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA;

AMINO ACID SEQUENCE; ANGIOGENESIS; ANIMAL; BIOLOGICAL MODEL; CELL DIVISION; CHEMISTRY; DISEASE COURSE; GENETICS; METABOLISM; MOLECULAR GENETICS; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; REVIEW; VASCULARIZATION;

AMINO ACID SEQUENCE; ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; CELL DIVISION; DISEASE PROGRESSION; ENZYME INHIBITORS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA;

EID: 0036362236     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2002.tb00307.x     Document Type: Review

References (66)

1. Bale M.D., Westrick L.G., Mosher D.F., Incorporation of thrombospondin into fibrin clots, J. Biol. Chem., 260: 7502-8, 1985
2. Kyriakides T.R., Zhu Y.-H., Smith L.T., Bain S.D., Yang Z., Lin M.T., Danielson K.G, Iozzo R.V., LaMarca M., McKinney C.E., Ginns E.I., Bornstein P., Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density and a bleeding disorder, J. Cell Biol., 140: 419-430, 1998
3. Bornstein P., Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1, J. Cell. Biol., 130: 503-6, 1995
4. Chen H., Herndon M.E., Lawler J., The cell biology of thrombospondin-1, Matrix Biology, 19: 597-614, 2000
5. Brown L.F., Guidi A.J., Schnitt S.J., Van De Water L., Iruela-Arispe M.L., Yeo T.-K., Tognazzi K., Dvorak H.F., Vascular stroma formation in carcinoma of the breast, Clin. Cancer Res., 5: 1041-1056, 1999
6. Beckmann G., Hanke J., Bork P., Reich J.G., Merging extracellular domains: fold prediction for laminin G-like and amino-terminal thrombospondin-like modules based on homology to pentraxins, J. Mol. Biol., 275: 725-30, 1998
7. Chen H., Aeschlimann D., Nowlen J., Mosher D.F., Expression and initial characterization of recombinant mouse thrombospondin-1 and thrombospondin-3, F.E.B.S. Lett., 387: 36-41, 1996
8. Krutzsch H.C., Choe B.J., Sipes J.M., Guo N., Roberts D.D., Identification of an alpha(3)beta(1) integrin recognition sequence in thrombospondin-1, J. Biol. Chem., 274: 24080-6, 1999
9. Chandrasekaran S., Guo N.H., Rodrigues R.G., Kaiser J., Roberts D.D., Pro-adhesive and chemotactic activities of thrombospondin-1 for breast carcinoma cells are mediated by alpha(3)beta(1) integrin and regulated by insulin-like growth factor-1 and CD98, J. Biol. Chem., 274: 11408-16, 1999
10. Tolsma S.S., Volpert O.V., Good D.J., Frazier W.A., Polverini P.J., Bouck N., Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity. J. Cell Biol., 122: 497-511, 1993
11. Dawson D.W., Volpert O.V., Pearce S.F.A., Schneider A.J., Silverstein R.L., Henkin J., Bouck N.P., Three distinct D-amino acid substitutions confer potent antiangiogenic activity on an inactive peptide derived from a thrombospondin-1 type 1 repeat, Molec. Pharmacol., 55: 332-338, 1999
12. Venter J.C., Adams M.D., Myers E.W., Li P.W., Mural R.J., Sutton G.G., Smith H.O., Yandell M., Evans C.A., Holt R.A., Gocayne J.D., Amanatides P., Ballew R.M., Huson D.H., Wortman J.R., Zhang Q., Kodira C.D., Zheng X.H., Chen L., Skupski M., et al., The sequence of the human genome, Science, 291: 1304-51, 2001
13. Adams J.C., Tucker R.P., The thrombospondin type 1 repeat (TSR) superfamily: diverse proteins with related roles in neuronal development, Dev. Dyn., 218: 280-99, 2000
14. Lawler J., The functions of thrombospondin-1 and -2, Curr. Opin. Cell Biol., 12: 634-640, 2000
15. Murphy-Ullrich J.E., Poczatek M., Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology, Cytokine Growth Factor Rev., 11: 59-69, 2000
16. Schultz-Cherry S., Chen H., Mosher D.F., Misenheimer T.M., Krutzsch H.C., Roberts D.D., Murphy-Ullrich J.E., Regulation of transforming growth factor-beta activation by discrete sequences of thrombospondin 1, J. Biol. Chem., 270: 7304-7310, 1995
17. Ribeiro S.M.F., Poczatek M., Schultz-Cherry S., Villain M., Murphy-Ullrich J.E.M., The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-β, J. Biol. Chem., 274: 13586-13593, 1999
18. Lawler J., Sunday M., Thibert V., Duquette M., George E.L., Rayburn H., Hynes R.O., Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia, J. Clin. Invest., 101: 982-992, 1998
19. Crawford S.E., Stellmach V., Murphy-Ullrich J.E., Ribeiro S.M.F., Lawler J., Hynes R.O., Boivin G.P., Bouck N., Thrombospondin-1 is a major activator of TGF-β1 in vivo, Cell, 93: 1159-1170, 1998
20. Abdelouahed M., Ludlow A., Brunner G, Lawler J., Activation of platelet transforming growth factor-beta 1 in the absence of thrombospondin-1, J. Biol. Chem., 275: 17933-17936, 2000
21. Grainger D.J., Frow E.K., Thrombospondin 1 does not activate transforming growth factor beta1 in a chemically defined system or in smooth-muscle-cell cultures, Biochem. J., 350: 291-8, 2000
22. Bailly S., Brand C., Chambaz E.M., Feige J.J., Analysis of small latent transforming growth factor-beta complex formation and dissociation by surface plasmon resonance. Absence of direct interaction with thrombospondins, J. Biol. Chem., 272: 16329-34, 1997
23. Hofsteenge J., Huwiler K.G, Macek B., Hess D., Lawler J., Mosher D.F., Peter-Katalinic J., C-mannosylation and O-fucosylation of the thrombospondin type 1 module, J. Biol. Chem., 276: 6485-98, 2001
24. Misenheimer T.M., Mosher D.F., Calcium ion binding to thrombospondin-1, J. Biol. Chem., 270: 1729-1733, 1995
25. Lawler J., Simons E., Cooperative binding of calcium to thrombospondin, J. Biol. Chem., 258: 12098-12101, 1983
26. Lawler J., Derick L.H., Connolly J.E., Chen J.-H., Chao F.C., The structure of human platelet thrombospondin, J. Biol. Chem., 260: 3762-3772, 1985
27. Lawler J., Hynes R.O., 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, 1986
28. Sun X., Skorstengaard K., Mosher D.F., Disulfides modulate RGD-inhibitable cell adhesive activity of thrombospondin, J. Cell Biol., 118: 693-701, 1992
29. Gao A.-G., Lindberg F.P., Finn M.B., Blystone S.D., Brown E.J., Frazier W.A., Integrin-associated protein is a receptor for the C-terminal domain of thrombospondin, J. Biol. Chem., 271: 21-24, 1996
30. 3 function through integrin-associated protein, J. Biol. Chem., 135: 533-544, 1996
31. Green J.M., Zhelesnyak A., Chung J., Lindberg F.P., Sarfati M., Frazier W.A., Brown E.J., Role of cholesterol in formation and function of a signaling complex involving alphavbeta3, integrin-associated protein (CD47), and heterotrimeric G proteins, J. Cell. Biol., 146: 673-82, 1999
32. BenEzra D., Griffin B.W., Maftzir G., Aharonov O., Thrombospondin and in vivo angiogenesis induced by basic fibroblast growth factor or lipopolysaccharide, Invest. Ophthalmol. Vis. Sci., 34: 3601-8, 1993
33. Nicosia R.F., Tuszynski G.P., Matrix-bound thrombospondin promotes angiogenesis in vitro, J. Cell Biol., 124: 183-93, 1994
34. Iruela-Arispe M.L., Lombardo M., Krutzsch H.C., Lawler J., Roberts D.D., Inhibition of angiogenesis by thrombospondin-1 is mediated by 2 independent regions within the type 1 repeats, Circulation, 100: 1423-31, 1999
35. Guo N.-H., Drutzch H.C., Inman J.K., Roberts D.D., Thrombospondin 1 and type 1 repeat peptides of thrombospondin 1 specifically induce apoptosis of endothelial cells, Cancer Res., 57: 1735-1742, 1997
36. Guo N.-H., Krutzsch H.C., Negre E., Vogel T., Blake D.A., Roberts D.D., Heparin- and sulfatide-binding peptides from the type 1 repeats of human thrombospondin promote melanoma cell adhesion, Proc. Natl. Acad. Sci. USA, 89: 3040-3044, 1992
37. Vogel T., Guo N.H., Krutzsch H.C., Blake D.A., Hartman J., Mendelovitz S., Panet A., Roberts D.D., Modulation of endothelial cell proliferation, adhesion, and motility by recombinant heparin-binding domain and synthetic peptides from the type I repeats of thrombospondin, J. Cell Biochem., 53: 74-84, 1993
38. Panetti T.S., Kudryk B.J., Mosher D.F., Interaction of recombinant procollagen and properdin modules of thrombospondin-1 with heparin and fibrinogen/fibrin, J. Biol. Chem., 274: 430-437, 1999
39. Yu H., Tyrrell D., Cashel J., Guo N., Vogel T., Sipes J.M., Lam L., Fillit H.M., Hartman J., Mendelovitz S., Panel A., Roberts D.D., Specificities of Heparin-binding Sites from the Amino-Terminus and Type 1 Repeats of Thrombospondin-1, Arch. Biochem. Biophys., 374: 13-23, 2000
40. Dawson D.W., Pearce S.F.A., Zhong R., Silverstein R.L., Frazier W.A., Bouck N.P., CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell Biol., 138: 707-717, 1997
41. Jimenez B., Volpert O.V., Crawford S.E., Febbraio M., Silverstein R.L., Bouck N., Signals leading to opoptosis-dependent inhibition of neovascularization by thrombospondin-1, Nature Medicine, 6: 41-48, 2000
42. Dorahy D.J., Lincz L.F., Meldrum C.J., Burns GE, Biochemical isolation of a membrane microdomain from resting platelets highly enriched in the plasma membrane glycoprotein CD36, Biochem., 319: 67-72, 1996
43. Thorne R.F., Marshall J.F., Shafren D.R., Gibson P.G., Hart I.R., Burns G.F., The integrins alpha(3)beta(1) and alpha(6)beta(1) physically and functionally associate with CD36 in human melanoma cells. Requirement for the extracellular domain of CD36, J. Biol. Chem., 275: 35264-75, 2000
44. Miao W., Seng W.L., Duquette M., Laus C., Detmar M., Lawler J., Thrombospondin-1 type 1 repeat recombinant proteins inhibit tumor growth, Blood, 97: 1689-1696, 2001
45. Jimenez B., Volpert O.V., Reiher F., Chang L., Munoz A., Karin M., Bouck N., c-Jun N-terminal kinase activation is required for the inhibition of neovascularization by thrombospondin-1, Oncogene, 20: 3443-8, 2001
46. Nor J.E., Mitra R.S., Sutorik M.M., Mooney D.J., Castle V.P., Polverini P.J., Thrombospondin-1 induces endothelial cell apoptosis and inhibits angiogenesis by activating the caspase death pathway, J. Vasc. Res., 37: 209-18, 2000
47. Rodriguez-Manzaneque J.C., Lane T.F., Ortega M.A., Hynes R.O., Lawler J., Iruela-Arispe M.L., Thrombospondin-1 suppresses tumor growth by a novel mechanism that includes blockade of matrix metalloproteinase-9 activation, Proc. Natl. Acad. Sci. USA, 98: 12485-12490, 2001
48. Taraboletti G., Morbidelli L., Donnini S., Parenti A., Granger H.J., Giavazzi R., Ziche M., The heparin binding 25 kDa fragment of thrombospondin-1 promotes angiogenesis and modulates gelatinase and TIMP-2 production in endothelial cells, FASEB J., 14: 1674-6, 2000
49. de Fraipont F., Nicholson A.C., Feige J.J., Van Meir E.G., Thrombospondins and tumor angiogenesis, Trends Mol. Med., 7: 401-7., 2001
50. Grant S.W., Kyshtoobayeva A.S., Kurosaki T., Jakowatz J., Fruehauf J.P., Mutant p53 correlates with reduced expression of thrombospondin-1, increased angiogenesis, and metastatic progression in melanoma, Cancer Detect. Prev., 22: 185-94, 1998
51. Grossfeld G.D., Ginsberg D.A., Stein J.P., Bochner B.H., Esrig D., Grosher S., Dunn M., Nichols P.W., Taylor C.R., Skinner D.G., Cote R.J., Thrombospondin-1 expression in bladder cancer: Association with p53 alterations, tumor angiogenesis and tumor progression, J. Natl. Cancer Institute, 89: 219-227, 1997
52. Tokunaga T., Nakamura M., Oshika Y., Tsuchida T., Kazuno M., Fukushima Y., Kawai K., Abe Y., Kijima H., Yamazaki H., Tamaoki N., Ueyama Y., Alterations in tumour suppressor gene p53 correlate with inhibition of thrombospondin-1 gene expression in colon cancer cells, Virchows Arch., 433: 415-418, 1998
53. Tenan M., Fulci G., Albertoni M., Diserens A.C., Hamou M.F., El Atifi-Borel M., Feige J.J., Pepper M.S., Van Meir E.G., Thrombospondin-1 is downregulated by anoxia and suppresses tumorigenicity of human glioblastoma cells, J. Exp. Med., 191: 1789-98, 2000
54. Hsu S.C., Volpert O.V., Steck P.A., Mikkelsen T., Polverini P.J., Rao S., Chou P., Bouck N.P., Inhibition of angiogenesis in human glioblastomas by chromosome 10 induction of thrombospondin-1, Cancer Res., 56: 5684-5691, 1996
55. Janz A., Sevignani C., Kenyon K., Ngo C.V., Thomas-Tikhonenko A., Activation of the myc oncoprotein leads to increased turnover of thrombospondin-1 mRNA, Nucleic Acids Res., 28: 2268-75, 2000
56. Majack R.A., Cook S.C., Bornstein P., Control of smooth muscle cell growth by components of the extracellular matrix: Autocrine role for thrombospondin, Proc. Natl. Acad. Sci. USA, 83: 9050-9054, 1986
57. Dejong V., Degeorges A., Filleur S., Ait-Si-Ali S., Mettouchi A., Bornstein P., Binetruy B., Cabon F., The Wilms' tumor gene product represses the transcription of thrombospondin 1 in response to overexpression of c-Jun, Oncogene, 18: 3143-51, 1999
58. Lawler J., Miao W.M., Duquette M., Bouck N., Bronson R.T., Hynes R.O., Thrombospondin-1 gene expression affects survival and tumor spectrum of p53-deficient mice, Am. J. Pathol., 159: 1949-56, 2001
59. Yao L., Zhao Y.L., Itoh S., Wada S., Yue L., Furuta I., Thrombospondin-1 expression in oral squamous cell carcinomas: correlations with tumor vascularity, clinicopathological features and survival, Oral Oncol., 36: 539-44, 2000
60. Bleuel K., Popp S., Fusenig N.B., Stanbridge E.J., Boukamp P., Tumor suppression in human skin carcinoma cells by chromosome 15 transfer or thrombospondin-1 overexpression through halted tumor vasculature, Proc. Natl. Acad. Sci. (USA), 96: 2065-2070, 1999
61. Clezardin P., Frappart L., Clerget M., Pechoux C., Delmar P.D., Expression of thrombospondin (TSP-1) and its receptors (CD36 and CD31) in normal, hyperplastic and neoplastic human breast, Cancer Res., 53: 1421-1430, 1993
62. Streit M., Riccardi L., Velasco P., Brown L.F., Hawighorst T., Bornstein P., Detmar M., Thrombospondin-2: a potent endogenous inhibitor of tumor growth and angiogenesis, Proc. Natl. Acad. Sci. U. S. A., 96: 14888-93, 1999
63. Bertin N., Clezardin P., Kubiak R., Frappart L., Thrombospondin-1 and -2 messenger RNA expression in normal, benign and neoplastic human breast tissues: Correlation with prognostic factors, tumor angiogenesis and fibroblastic desmoplasia, Cancer Res., 57: 396-399, 1997
64. Gasparini G., Toi M., Biganzoli E., Dittadi R., Fanelli M., Morabito A., Boracchi P., Gion M., Thrombospondin-1 and -2 in node-negative breast cancer: correlation with angiogenic factors, p53, cathepsin D, hormone receptors and prognosis, Oncology, 60: 72-80, 2001
65. Kerbel R.S., A cancer therapy resistant to resistance, Nature, 390: 335-6, 1997
66. Filleur S., Volpert O.V., Degeorges A., Voland C., Reiher F., Clezardin P., Bouck N., Cabon F., In vivo mechanisms by which tumors producing thrombospondin 1 bypass its inhibitory effects, Genes Dev, 15: 1373-82, 2001