Regulation of tumor angiogenesis by thrombospondin-1

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1765, Issue 2, 2006, Pages 178-188

  Ren, Bin ^a   Yee, Karen O ^a   Lawler, Jack ^a   Khosravi Far, Roya ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Angiogenesis; Gene; Metastasis; TGF beta; Thrombospondin 1; Tumor progression

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; CD36 ANTIGEN; CD47 ANTIGEN; CD9 ANTIGEN; GELATINASE B; N ACETYLSARCOSYLGLYCYLVALYL DEXTRO ALLOISOLEUCYLTHREONYLNORVALYLISOLEUCYLARGINYLPROLINE ETHYLAMIDE; POLYETHYLENEIMINE; PROTEIN P53; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA1; VASCULOTROPIN C;

ADVANCED CANCER; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANGIOGENESIS; CANCER INVASION; CANCER SURVIVAL; CARCINOMA IN SITU; CELL MIGRATION; DOWN REGULATION; FAMILIAL CANCER; GENE EXPRESSION; GLIOMA; HUMAN; LUNG METASTASIS; LUNG NON SMALL CELL CANCER; MELANOMA; MICROVASCULATURE; MOLECULAR CLONING; NEOVASCULARIZATION (PATHOLOGY); NEPHROBLASTOMA; NONHUMAN; ONCOGENE; ONCOGENE MYC; OVARY CARCINOMA; OVERALL SURVIVAL; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATECTOMY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; PROTEIN SYNTHESIS REGULATION; REVIEW; SQUAMOUS CELL CARCINOMA; STRUCTURAL HOMOLOGY; SURVIVAL RATE; SURVIVAL TIME; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; UTERINE CERVIX CANCER; WILD TYPE;

ANGIOGENESIS INHIBITORS; ANIMALS; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; THROMBOSPONDIN 1;

EID: 33646136232     PISSN: 0304419X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbcan.2005.11.002     Document Type: Review

References (145)

1. Yano K., Brown L.F., Lawler J., Miyakawa T., and Detmar M. Thrombospondin-1 plays a critical role in the induction of hair follicle involution and vascular regression during the catagen phase. J. Invest. Dermatol. 120 (2003) 14-19
2. Folkman J., and Klagsbrun M. Angiogenic factors. Science 235 (1987) 442-447
3. Folkman J. Angiogenesis. 15th ed. (2001), McGraw Hill, New York
4. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1 (1995) 27-31
5. Folkman J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 285 (1971) 1182-1186
6. Aishima S., Taguchi K., Sugimachi K., Asayama Y., Nishi H., Shimada M., and Tsuneyoshi M. The role of thymidine phosphorylase and thrombospondin-1 in angiogenesis and progression of intrahepatic cholangiocarcinoma. Int. J. Surg. Pathol. 10 (2002) 47-56
7. Armstrong L.C., and Bornstein P. Thrombospondins 1 and 2 function as inhibitors of angiogenesis. Matrix Biol. 22 (2003) 63-71
8. Good D.J., Polverini P.J., Rastinejad F., Le Beau M.M., Lemons R.S., Frazier W.A., and Bouck N.P. A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 6624-6628
9. Tolsma S.S., Volpert O.V., Good D.J., Frazier W.A., Polverini P.J., and Bouck N. Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity. J. Cell Biol. 122 (1993) 497-511
10. Weinstat-Saslow D.L., Zabrenetzky V.S., VanHoutte K., Frazier W.A., Roberts D.D., and Steeg P.S. Transfection of thrombospondin 1 complementary DNA into a human breast carcinoma cell line reduces primary tumor growth, metastatic potential, and angiogenesis. Cancer Res. 54 (1994) 6504-6511
11. Nor J.E., Mitra R.S., Sutorik M.M., Mooney D.J., Castle V.P., and Polverini P.J. Thrombospondin-1 induces endothelial cell apoptosis and inhibits angiogenesis by activating the caspase death pathway. J. Vasc. Res. 37 (2000) 209-218
12. Lawler J. The functions of thrombospondin-1 and-2. Curr. Opin. Cell Biol. 12 (2000) 634-640
13. Volpert O.V. Modulation of endothelial cell survival by an inhibitor of angiogenesis thrombospondin-1: a dynamic balance. Cancer Metastasis Rev. 19 (2000) 87-92
14. Bornstein P. Thrombospondins as matricellular modulators of cell function. J. Clin. Invest. 107 (2001) 929-934
15. Hsu S.C., Volpert O.V., Steck P.A., Mikkelsen T., Polverini P.J., Rao S., Chou P., and Bouck N.P. Inhibition of angiogenesis in human glioblastomas by chromosome 10 induction of thrombospondin-1. Cancer Res. 56 (1996) 5684-5691
16. Jimenez B., Volpert O.V., Crawford S.E., Febbraio M., Silverstein R.L., and Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat. Med. 6 (2000) 41-48
17. Akhurst R.J., and Derynck R. TGF-beta signaling in cancer-A double-edged sword. Trends Cell Biol. 11 (2001) S44-S51
18. Lawler J., and Detmar M. Tumor progression: the effects of thrombospondin-1 and -2. Int. J. Biochem. Cell Biol. 36 (2004) 1038-1045
19. Albo D., Shinohara T., and Tuszynski G.P. Up-regulation of matrix metalloproteinase 9 by thrombospondin 1 in gastric cancer. J. Surg. Res. 108 (2002) 51-60
20. Giaccia A.J., and Kastan M.B. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev. 12 (1998) 2973-2983
21. Bouck N. P53 and angiogenesis. Biochim. Biophys. Acta 1287 (1996) 63-66
22. Chen Q.R., and Mixson A.J. Systemic gene therapy with p53 inhibits breast cancer: recent advances and therapeutic implications. Front Biosci. 3 (1998) D997-D1004
23. Dameron K.M., Volpert O.V., Tainsky M.A., and Bouck N. Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science 265 (1994) 1582-1584
24. Laderoute K.R., Alarcon R.M., Brody M.D., Calaoagan J.M., Chen E.Y., Knapp A.M., Yun Z., Denko N.C., and Giaccia A.J. Opposing effects of hypoxia on expression of the angiogenic inhibitor thrombospondin 1 and the angiogenic inducer vascular endothelial growth factor. Clin. Cancer Res. 6 (2000) 2941-2950
25. Stellmach V., Volpert O.V., Crawford S.E., Lawler J., Hynes R.O., and Bouck N. Tumour suppressor genes and angiogenesis: the role of TP53 in fibroblasts. Eur. J. Cancer 32A (1996) 2394-2400
26. Volpert O.V., Dameron K.M., and Bouck N. Sequential development of an angiogenic phenotype by human fibroblasts progressing to tumorigenicity. Oncogene 14 (1997) 1495-1502
27. Gautam A., Densmore C.L., Melton S., Golunski E., and Waldrep J.C. Aerosol delivery of PEI-p53 complexes inhibits B16-F10 lung metastases through regulation of angiogenesis. Cancer Gene Ther. 9 (2002) 28-36
28. Kwak C., Jin R.J., Lee C., Park M.S., and Lee S.E. Thrombospondin-1, vascular endothelial growth factor expression and their relationship with p53 status in prostate cancer and benign prostatic hyperplasia. BJU Int. 89 (2002) 303-309
29. Alvarez A.A., Axelrod J.R., Whitaker R.S., Isner P.D., Bentley R.C., Dodge R.K., and Rodriguez G.C. Thrombospondin-1 expression in epithelial ovarian carcinoma: association with p53 status, tumor angiogenesis, and survival in platinum-treated patients. Gynecol. Oncol. 82 (2001) 273-278
30. Harada H., Nakagawa K., Saito M., Kohno S., Nagato S., Furukawa K., Kumon Y., Hamada K., and Ohnishi T. Introduction of wild-type p53 enhances thrombospondin-1 expression in human glioma cells. Cancer Lett. 191 (2003) 109-119
31. Grant S.W., Kyshtoobayeva A.S., Kurosaki T., Jakowatz J., and Fruehauf J.P. Mutant p53 correlates with reduced expression of thrombospondin-1, increased angiogenesis, and metastatic progression in melanoma. Cancer Detect. Prev. 22 (1998) 185-194
32. Lawler J., Miao W.M., Duquette M., Bouck N., Bronson R.T., and Hynes R.O. Thrombospondin-1 gene expression affects survival and tumor spectrum of p53-deficient mice. Am. J. Pathol. 159 (2001) 1949-1956
33. Vikhanskaya F., Bani M.R., Borsotti P., Ghilardi C., Ceruti R., Ghisleni G., Marabese M., Giavazzi R., Broggini M., and Taraboletti G. p73 Overexpression increases VEGF and reduces thrombospondin-1 production: implications for tumor angiogenesis. Oncogene 20 (2001) 7293-7300
34. Tokunaga T., Nakamura M., Oshika Y., Tsuchida T., Kazuno M., Fukushima Y., Kawai K., Abe Y., Kijima H., Yamazaki H., Tamaoki N., and Ueyama Y. Alterations in tumour suppressor gene p53 correlate with inhibition of thrombospondin-1 gene expression in colon cancer cells. Virchows Arch. 433 (1998) 415-418
35. Grossfeld G.D., Carroll P.R., Lindeman N., Meng M., Groshen S., Feng A.C., Hawes D., and Cote R.J. Thrombospondin-1 expression in patients with pathologic stage T3 prostate cancer undergoing radical prostatectomy: association with p53 alterations, tumor angiogenesis, and tumor progression. Urology 59 (2002) 97-102
36. Kawahara N., Ono M., Taguchi K., Okamoto M., Shimada M., Takenaka K., Hayashi K., Mosher D.F., Sugimachi K., Tsuneyoshi M., and Kuwano M. Enhanced expression of thrombospondin-1 and hypovascularity in human cholangiocarcinoma. Hepatology 28 (1998) 1512-1517
37. Reiher F.K., Ivanovich M., Huang H., Smith N.D., Bouck N.P., and Campbell S.C. The role of hypoxia and p53 in the regulation of angiogenesis in bladder cancer. J. Urol. 165 (2001) 2075-2081
38. Fontanini G., Boldrini L., Calcinai A., Chine S., Lucchi M., Mussi A., Angeletti C.A., Basolo F., and Bevilacqua G. Thrombospondins I and II messenger RNA expression in lung carcinoma: relationship with p53 alterations, angiogenic growth factors, and vascular density. Clin. Cancer Res. 5 (1999) 155-161
39. Mettouchi A., Cabon F., Montreau N., Vernier P., Mercier G., Blangy D., Tricoire H., Vigier P., and Binetruy B. SPARC and thrombospondin genes are repressed by the c-jun oncogene in rat embryo fibroblasts. EMBO J. 13 (1994) 5668-5678
40. Dejong V., Degeorges A., Filleur S., Ait-Si-Ali S., Mettouchi A., Bornstein P., Binetruy B., and Cabon F. The Wilms' tumor gene product represses the transcription of thrombospondin 1 in response to overexpression of c-Jun. Oncogene 18 (1999) 3143-3151
41. Slack J.L., and Bornstein P. Transformation by v-src causes transient induction followed by repression of mouse thrombospondin-1. Cell Growth Differ. 5 (1994) 1373-1380
42. Tikhonenko A.T., Black D.J., and Linial M.L. Viral Myc oncoproteins in infected fibroblasts down-modulate thrombospondin-1, a possible tumor suppressor gene. J. Biol. Chem. 271 (1996) 30741-30747
43. Janz A., Sevignani C., Kenyon K., Ngo C.V., and Thomas-Tikhonenko A. Activation of the myc oncoprotein leads to increased turnover of thrombospondin-1 mRNA. Nucleic Acids Res. 28 (2000) 2268-2275
44. Watnick R.S., Cheng Y.N., Rangarajan A., Ince T.A., and Weinberg R.A. Ras modulates Myc activity to repress thrombospondin-1 expression and increase tumor angiogenesis. Cancer Cell 3 (2003) 219-231
45. Rak J., Mitsuhashi Y., Sheehan C., Tamir A., Viloria-Petit A., Filmus J., Mansour S.J., Ahn N.G., and Kerbel R.S. Oncogenes and tumor angiogenesis: differential modes of vascular endothelial growth factor up-regulation in ras-transformed epithelial cells and fibroblasts. Cancer Res. 60 (2000) 490-498
46. Volpert O.V., Pili R., Sikder H.A., Nelius T., Zaichuk T., Morris C., Shiflett C.B., Devlin M.K., Conant K., and Alani R.M. Id1 regulates angiogenesis through transcriptional repression of thrombospondin-1. Cancer Cell 2 (2002) 473-483
47. Markowitz S.D., and Roberts A.B. Tumor suppressor activity of the TGF-beta pathway in human cancers. Cytokine Growth Factor Rev. 7 (1996) 93-102
48. Schultz-Cherry S., Ribeiro S., Gentry L., and Murphy-Ullrich J.E. Thrombospondin binds and activates the small and large forms of latent transforming growth factor-beta in a chemically defined system. J. Biol. Chem. 269 (1994) 26775-26782
49. Schultz-Cherry S., Lawler J., and Murphy-Ullrich J.E. The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-beta. J. Biol. Chem. 269 (1994) 26783-26788
50. Schultz-Cherry S., Chen H., Mosher D.F., Misenheimer T.M., Krutzsch H.C., Roberts D.D., and Murphy-Ullrich J.E. Regulation of transforming growth factor-beta activation by discrete sequences of thrombospondin 1. J. Biol. Chem. 270 (1995) 7304-7310
51. Murphy-Ullrich J.E., and Poczatek M. Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology. Cytokine Growth Factor Rev. 11 (2000) 59-69
52. Iruela-Arispe M.L., Lombardo M., Krutzsch H.C., Lawler J., and Roberts D.D. Inhibition of angiogenesis by thrombospondin-1 is mediated by 2 independent regions within the type 1 repeats. Circulation 100 (1999) 1423-1431
53. Yee K.O., Streit M., Hawighorst T., Detmar M., and Lawler J. Expression of the type-1 repeats of thrombospondin-1 inhibits tumor growth through activation of transforming growth factor-beta. Am. J. Pathol. 165 (2004) 541-552
54. Miao W.M., Seng W.L., Duquette M., Lawler P., Laus C., and Lawler J. Thrombospondin-1 type 1 repeat recombinant proteins inhibit tumor growth through transforming growth factor-beta-dependent and -independent mechanisms. Cancer Res. 61 (2001) 7830-7839
55. Lawler J. Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J. Cell Mol. Med. 6 (2002) 1-12
56. Crawford S.E., Stellmach V., Murphy-Ullrich J.E., Ribeiro S.M., Lawler J., Hynes R.O., Boivin G.P., and Bouck N. Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell 93 (1998) 1159-1170
57. Young G.D., and Murphy-Ullrich J.E. Molecular interactions that confer latency to transforming growth factor-beta. J. Biol. Chem. 279 (2004) 38032-38039
58. Young G.D., and Murphy-Ullrich J.E. 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 (2004) 47633-47642
59. Hinck A.P., Archer S.J., Qian S.W., Roberts A.B., Sporn M.B., Weatherbee J.A., Tsang M.L., Lucas R., Zhang B.L., Wenker J., and Torchia D.A. Transforming growth factor beta 1: three-dimensional structure in solution and comparison with the X-ray structure of transforming growth factor beta 2. Biochemistry 35 (1996) 8517-8534
60. Narayan S., Thangasamy T., and Balusu R. Transforming growth factor-beta receptor signaling in cancer. Front Biosci. 10 (2005) 1135-1145
61. Letterio J.J. TGF-beta signaling in T cells: roles in lymphoid and epithelial neoplasia. Oncogene 24 (2005) 5701-5712
62. Roberts A.B., and Wakefield L.M. The two faces of transforming growth factor beta in carcinogenesis. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 8621-8623
63. Radisky D.C., and Bissell M.J. Cancer. Respect thy neighbor!. Science 303 (2004) 775-777
64. Sasaki A., Naganuma H., Satoh E., Kawataki T., Amagasaki K., and Nukui H. Participation of thrombospondin-1 in the activation of latent transforming growth factor-beta in malignant glioma cells. Neurol. Med. Chir. (Tokyo) 41 (2001) 253-258 (Discussion 258-9)
65. Miyanaga K., Kato Y., Nakamura T., Matsumura M., Amaya H., Horiuchi T., Chiba Y., and Tanaka K. Expression and role of thrombospondin-1 in colorectal cancer. Anticancer Res. 22 (2002) 3941-3948
66. Kawataki T., Naganuma H., Sasaki A., Yoshikawa H., Tasaka K., and Nukui H. Correlation of thrombospondin-1 and transforming growth factor-beta expression with malignancy of glioma. Neuropathology 20 (2000) 161-169
67. Fontana A., Filleur S., Guglielmi J., Frappart L., Bruno-Bossio G., Boissier S., Cabon F., and Clezardin P. Human breast tumors override the antiangiogenic effect of stromal thrombospondin-1 in vivo. Int. J. Cancer 116 (2005) 686-691
68. Filleur S., Volpert O.V., Degeorges A., Voland C., Reiher F., Clezardin P., Bouck N., and Cabon F. In vivo mechanisms by which tumors producing thrombospondin 1 bypass its inhibitory effects. Genes Dev. 15 (2001) 1373-1382
69. Schiemann W.P., Pfeifer W.M., Levi E., Kadin M.E., and Lodish H.F. A deletion in the gene for transforming growth factor beta type I receptor abolishes growth regulation by transforming growth factor beta in a cutaneous T-cell lymphoma. Blood 94 (1999) 2854-2861
70. Chen T., Triplett J., Dehner B., Hurst B., Colligan B., Pemberton J., Graff J.R., and Carter J.H. Transforming growth factor-beta receptor type I gene is frequently mutated in ovarian carcinomas. Cancer Res. 61 (2001) 4679-4682
71. Baxter S.W., Choong D.Y., Eccles D.M., and Campbell I.G. Transforming growth factor beta receptor 1 polyalanine polymorphism and exon 5 mutation analysis in breast and ovarian cancer. Cancer Epidemiol. Biomarkers Prev. 11 (2002) 211-214
72. Chen T., Yan W., Wells R.G., Rimm D.L., McNiff J., Leffell D., and Reiss M. Novel inactivating mutations of transforming growth factor-beta type I receptor gene in head-and-neck cancer metastases. Int. J. Cancer 93 (2001) 653-661
73. Danielpour D. Functions and regulation of transforming growth factor-beta (TGF-beta) in the prostate. Eur. J. Cancer 41 (2005) 846-857
74. Bhowmick N.A., Chytil A., Plieth D., Gorska A.E., Dumont N., Shappell S., Washington M.K., Neilson E.G., and Moses H.L. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303 (2004) 848-851
75. Kang Y., He W., Tulley S., Gupta G.P., Serganova I., Chen C.R., Manova-Todorova K., Blasberg R., Gerald W.L., and Massague J. Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway. Proc. Natl .Acad. Sci. U. S. A. 102 (2005) 13909-13914
76. Tian F., Byfield S.D., Parks W.T., Stuelten C.H., Nemani D., Zhang Y.E., and Roberts A.B. Smad-binding defective mutant of transforming growth factor beta type I receptor enhances tumorigenesis but suppresses metastasis of breast cancer cell lines. Cancer Res. 64 (2004) 4523-4530
77. Dimmeler S., and Zeiher A.M. Endothelial cell apoptosis in angiogenesis and vessel regression. Circ. Res. 87 (2000) 434-439
78. Benjamin L.E., and Keshet E. Conditional switching of vascular endothelial growth factor (VEGF) expression in tumors: induction of endothelial cell shedding and regression of hemangioblastoma-like vessels by VEGF withdrawal. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 8761-8766
79. Hanahan D., and Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86 (1996) 353-364
80. Hiroko B., and Masakazu T. Tumor Angiogenesis, Macrophages, and Cytokines. Angiogenesis: from the Molecular to Integrative Pharmacology (2000), Academic/Plenum Publishers, New York
81. Schuch G., Kisker O., Atala A., and Soker S. Pancreatic tumor growth is regulated by the balance between positive and negative modulators of angiogenesis. Angiogenesis 5 (2002) 181-190
82. Mousa S.A., and Mousa A.S. Angiogenesis inhibitors: current and future directions. Curr. Pharm. Des. 10 (2004) 1-9
83. Holmgren L., O'Reilly M.S., and Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat. Med. 1 (1995) 149-153
84. Salvesen H.B., and Akslen L.A. Significance of tumour-associated macrophages, vascular endothelial growth factor and thrombospondin-1 expression for tumour angiogenesis and prognosis in endometrial carcinomas. Int. J. Cancer 84 (1999) 538-543
85. Dawson D.W., Pearce S.F., Zhong R., Silverstein R.L., Frazier W.A., and Bouck N.P. CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell Biol. 138 (1997) 707-717
86. Tsuchida T., Kijima H., Tokunaga T., Oshika Y., Hatanaka H., Fukushima Y., Abe Y., Kawai K., Yoshida Y., Miura S., Yamazaki H., Tamaoki N., Ueyama Y., and Nakamura M. Expression of the thrombospondin 1 receptor CD36 is correlated with decreased stromal vascularisation in colon cancer. Int. J. Oncol. 14 (1999) 47-51
87. Dawson D.W., and Bouck N.P. In: Teicher B.A. (Ed). Antiangiogenic Agents in Cancer Therapy (1999), Humana Press Inc, Totowa, NJ 185-203
88. Huang H., Campbell S.C., Bedford D.F., Nelius T., Veliceasa D., Shroff E.H., Henkin J., Schneider A., Bouck N., and Volpert O.V. Peroxisome proliferator-activated receptor gamma ligands improve the antitumor efficacy of thrombospondin peptide ABT510. Mol. Cancer Res. 2 (2004) 541-550
89. Lawler J., and 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 (1986) 1635-1648
90. Tucker R.P. The thrombospondin type 1 repeat superfamily. Int. J. Biochem. Cell Biol. 36 (2004) 969-974
91. Westphal J.R. Technology evaluation: ABT-510, Abbott. Curr. Opin. Mol. Ther. 6 (2004) 451-457
92. Tan K., Duquette M., Liu J.H., Dong Y., Zhang R., Joachimiak A., Lawler J., and Wang J.H. Crystal structure of the TSP-1 type 1 repeats: a novel layered fold and its biological implication. J. Cell Biol. 159 (2002) 373-382
93. Guo N., Templeton N.S., Al-Barazi H., Cashel J.A., Sipes J.M., Krutzsch H.C., and Roberts D.D. Thrombospondin-1 promotes alpha3beta1 integrin-mediated adhesion and neurite-like outgrowth and inhibits proliferation of small cell lung carcinoma cells. Cancer Res. 60 (2000) 457-466
94. Freyberg M.A., Kaiser D., Graf R., Vischer P., and Friedl P. Integrin-associated protein and thrombospondin-1 as endothelial mechanosensitive death mediators. Biochem. Biophys. Res. Commun. 271 (2000) 584-588
95. Kanda S., Shono T., Tomasini-Johansson B., Klint P., and Saito Y. Role of thrombospondin-1-derived peptide, 4NIK, in FGF-2-induced angiogenesis. Exp. Cell Res. 252 (1999) 262-272
96. Guo N.-H., Drutzch H.C., Inman J.K., and Roberts D.D. Thrombospondin 1 and type 1 repeat peptides of thrombospondin 1 specifically induce apoptosis of endothelial cells. Cancer Res. 57 (1997) 1735-1742
97. Short S., Derrien A., Narsimhan R., Lawler J., Ingber D., and Zetter B. Thrombospondin type 1 repeats inhibit endothelial cell migration via b1 integrins by a CD36-independent mechanism. J. Cell Biol. 168 (2005) 643-653
98. Calzada M.J., Zhou L., Sipes J.M., Zhang J., Krutzsch H.C., Iruela-Arispe M.L., Annis D.S., Mosher D.F., and Roberts D.D. Alpha4beta1 integrin mediates selective endothelial cell responses to thrombospondins 1 and 2 in vitro and modulates angiogenesis in vivo. Circ. Res. 94 (2004) 462-470
99. Miao W.M., Vasile E., Lane W.S., and Lawler J. CD36 associates with CD9 and integrins on human blood platelets. Blood 97 (2001) 1689-1696
100. Primo L., Ferrandi C., Roca C., Marchio S., di Blasio L., Alessio M., and Bussolino F. Identification of CD36 molecular features required for its in vitro angiostatic activity. FASEB J. (2005) (Electronic publication ahead of print)
101. Mateo V., Lagneaux L., Bron D., Biron G., Armant M., Delespesse G., and Sarfati M. CD47 ligation induces caspase-independent cell death in chronic lymphocytic leukemia. Nat. Med. 5 (1999) 1277-1284
102. Rodriguez-Manzaneque J.C., Lane T.F., Ortega M.A., Hynes R.O., Lawler J., and Iruela-Arispe M.L. Thrombospondin-1 supresses tumor growth by a novel mechanism that includes blockade of matrix matalloproteinase-9 activation. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 12485-12490
103. Gupta K., Gupta P., Wild R., Ramakrishnan S., and Hebbel R.P. Binding and displacement of vascular endothelial growth factor (VEGF) by thrombospondin: effect on human microvascular endothelial cell proliferation and angiogenesis. Angiogenesis 3 (1999) 147-158
104. Gutierrez L.S., Suckow M., Lawler J., Ploplis V.A., and Castellino F.J. Thrombospondin 1-a regulator of adenoma growth and carcinoma progression in the APC(Min/+) mouse model. Carcinogenesis 24 (2003) 199-207
105. Oue N., Matsumura S., Nakayama H., Kitadai Y., Taniyama K., Matsusaki K., and Yasui W. Reduced expression of the TSP1 gene and its association with promoter hypermethylation in gastric carcinoma. Oncology 64 (2003) 423-429
106. Bleuel K., Popp S., Fusenig N.E., Stanbridge E.J., and Boukamp P. Tumor suppression in human skin carcinoma cells by chromosome 15 transfer or thrombospondin-1 overexpression through halted tumor vascularization. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 2065-2070
107. Streit M., Velasco P., Brown L.F., Skobe M., Richard L., Riccardi L., Lawler J., and Detmar M. Overexpression of thrombospondin-1 decreases angiogenesis and inhibits the growth of human cutaneous squamous cell carcinomas. Am. J. Pathol. 155 (1999) 441-452
108. Rofstad E.K., and Graff B.A. Thrombospondin-1-mediated metastasis suppression by the primary tumor in human melanoma xenografts. J. Invest. Dermatol. 117 (2001) 1042-1049
109. Taraboletti G., Benelli R., Borsotti P., Rusnati M., Presta M., Giavazzi R., Ruco L., and Albini A. Thrombospondin-1 inhibits Kaposi's sarcoma (KS) cell and HIV-1 Tat-induced angiogenesis and is poorly expressed in KS lesions. J. Pathol. 188 (1999) 76-81
110. Jin R.J., Kwak C., Lee S.G., Lee C.H., Soo C.G., Park M.S., Lee E., and Lee S.E. The application of an anti-angiogenic gene (thrombospondin-1) in the treatment of human prostate cancer xenografts. Cancer Gene Ther. 7 (2000) 1537-1542
111. Doll J.A., Reiher F.K., Crawford S.E., Pins M.R., Campbell S.C., and Bouck N.P. Thrombospondin-1, vascular endothelial growth factor and fibroblast growth factor-2 are key functional regulators of angiogenesis in the prostate. Prostate 49 (2001) 293-305
112. Hawighorst T., Oura H., Streit M., Janes L., Nguyen L., Brown L.F., Oliver G., Jackson D.G., and Detmar M. Thrombospondin-1 selectively inhibits early-stage carcinogenesis and angiogenesis but not tumor lymphangiogenesis and lymphatic metastasis in transgenic mice. Oncogene 21 (2002) 7945-7956
113. Tenan M., Fulci G., Albertoni M., Diserens A.C., Hamou M.F., El Atifi-Borel M., Feige J.J., Pepper M.S., and Van Meir E.G. Thrombospondin-1 is downregulated by anoxia and suppresses tumorigenicity of human glioblastoma cells. J. Exp. Med. 191 (2000) 1789-1798
114. Yamaguchi M., Sugio K., Ondo K., Yano T., and Sugimachi K. Reduced expression of thrombospondin-1 correlates with a poor prognosis in patients with non-small cell lung cancer. Lung Cancer 36 (2002) 143-150
115. Tanaka K., Sonoo H., Kurebayashi J., Nomura T., Ohkubo S., Yamamoto Y., and Yamamoto S. Inhibition of infiltration and angiogenesis by thrombospondin-1 in papillary thyroid carcinoma. Clin. Cancer Res. 8 (2002) 1125-1131
116. Yao L., Zhao Y.L., Itoh S., Wada S., Yue L., and Furuta I. Thrombospondin-1 expression in oral squamous cell carcinomas: correlations with tumor vascularity, clinicopathological features and survival. Oral. Oncol. 36 (2000) 539-544
117. Maeda K., Nishiguchi Y., Yashiro M., Yamada S., Onoda N., Sawada T., Kang S.M., and Hirakawa K. Expression of vascular endothelial growth factor and thrombospondin-1 in colorectal carcinoma. Int. J. Mol. Med. 5 (2000) 373-378
118. Maeda K., Nishiguchi Y., Kang S.M., Yashiro M., Onoda N., Sawada T., Ishikawa T., and Hirakawa K. Expression of thrombospondin-1 inversely correlated with tumor vascularity and hematogenous metastasis in colon cancer. Oncol. Rep. 8 (2001) 763-766
119. Rice A.J., Steward M.A., and Quinn C.M. Thrombospondin 1 protein expression relates to good prognostic indices in ductal carcinoma in situ of the breast. J. Clin. Pathol. 55 (2002) 921-925
120. Brown L.F., Guidi A.J., Schnitt S.J., Van De Water L., Iruela-Arispe M.L., Yeo T.K., Tognazzi K., and Dvorak H.F. Vascular stroma formation in carcinoma in situ, invasive carcinoma, and metastatic carcinoma of the breast. Clin. Cancer Res. 5 (1999) 1041-1056
121. Kodama J., Hashimoto I., Seki N., Hongo A., Yoshinouchi M., Okuda H., and Kudo T. Thrombospondin-1 and -2 messenger RNA expression in invasive cervical cancer: correlation with angiogenesis and prognosis. Clin. Cancer Res. 7 (2001) 2826-2831
122. Goddard J.C., Sutton C.D., Jones J.L., O'Byrne K.J., and Kockelbergh R.C. Reduced thrombospondin-1 at presentation predicts disease progression in superficial bladder cancer. Eur. Urol. 42 (2002) 464-468
123. Zhang J., Ito R., Oue N., Zhu X., Kitadai Y., Yoshida K., Nakayama H., and Yasui W. Expression of thrombospondin-1 is correlated with microvessel density in gastric carcinoma. Virchows Arch. 442 (2003) 563-568
124. Qian X., Rothman V.L., Nicosia R.F., and Tuszynski G.P. Expression of thrombospondin-1 in human pancreatic adenocarcinomas: role in matrix metalloproteinase-9 production. Pathol. Oncol. Res. 7 (2001) 251-259
125. Wang T.N., Albo D., and Tuszynski G.P. Fibroblasts promote breast cancer cell invasion by upregulating tumor matrix metalloproteinase-9 production. Surgery 132 (2002) 220-225
126. Albo D., Berger D.H., Rothman V.L., and Tuszynski G.P. Role of urokinase plasminogen activator receptor in thrombospondin 1-mediated tumor cell invasion. J. Surg. Res. 82 (1999) 331-338
127. Amagasaki K., Sasaki A., Kato G., Maeda S., Nukui H., and Naganuma H. Antisense-mediated reduction in thrombospondin-1 expression reduces cell motility in malignant glioma cells. Int. J. Cancer 94 (2001) 508-512
128. Straume O., and Akslen L.A. Expression of vascular endothelial growth factor, its receptors (FLT-1, KDR) and TSP-1 related to microvessel density and patient outcome in vertical growth phase melanomas. Am. J. Pathol. 159 (2001) 223-235
129. Poon R.T., Chung K.K., Cheung S.T., Lau C.P., Tong S.W., Leung K.L., Yu W.C., Tuszynski G.P., and Fan S.T. Clinical significance of thrombospondin 1 expression in hepatocellular carcinoma. Clin. Cancer Res. 10 (2004) 4150-4157
130. BenEzra D. Angiogenesis-Critical Assessment of In Vitro Assays and In Vivo Models. Angiogenesis: Models, Modulators, and Clinical Applications (1998), Plenum Press, New York
131. Nicosia R.F., and Tuszynski G.P. Matrix-bound thrombospondin promotes angiogenesis in vitro. J. Cell Biol. 124 (1994) 183-193
132. Vogel T., Guo N.H., Krutzsch H.C., Blake D.A., Hartman J., Mendelovitz S., Panet A., and 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 (1993) 74-84
133. Taraboletti G., Morbidelli L., Donnini S., Parenti A., Granger H.J., Giavazzi R., and 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 (2000) 1674-1676
134. Donnini S., Morbidelli L., Taraboletti G., and Ziche M. ERK1-2 and p38 MAPK regulate MMP/TIMP balance and function in response to thrombospondin-1 fragments in the microvascular endothelium. Life Sci. 74 (2004) 2975-2985
135. Ferrari do Outeiro-Bernstein M.A., Nunes S.S., Andrade A.C., Alves T.R., Legrand C., and Morandi V. A recombinant NH(2)-terminal heparin-binding domain of the adhesive glycoprotein, thrombospondin-1, promotes endothelial tube formation and cell survival: a possible role for syndecan-4 proteoglycan. Matrix Biol. 21 (2002) 311-324
136. Chandrasekaran L., He C.-Z., Al-Barazi H., Krutzsch H.C., Iruela-Arispe M.L., and Roberts D.D. Mol. Biol. Cell 11 (2000) 2885-2900
137. Lawler J., Sunday M., Thibert V., Duquette M., George E.L., Rayburn H., and Hynes R.O. Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia. J. Clin. Invest. 101 (1998) 982-992
138. Damas C., Vink T., Nieuwenhuis H.K., and Sixma J.J. The 33-kDa platelet alpha-granule membrane protein (GMP-33) is an N-terminal proteolytic fragment of thrombospondin. Thromb. Haemost. 86 (2001) 887-893
139. Gordon M., Mendelson D., Guirguis M., Knight R., Humerickhouse R., Stopeck A., and Wang Q. ABT-510, an anti-angiogenic, thrombospondin-1 (TSP-1) mimetic peptide, exhibits favorable safety profile and early signals of activity in a randomized phase IB trial. Proc. Am. Soc. Clin. Oncol. 22 (2003) 195 (Abstract no. 780)
140. Reiher F.K., Volpert O.V., Jimenez B., Crawford S.E., Dinney C.P., Henkin J., Haviv F., Bouck N.P., and Campbell S.C. Inhibition of tumor growth by systemic treatment with thrombospondin-1 peptide mimetics. Int. J. Cancer 98 (2002) 682-689
141. Cline E.I., Bicciato S., DiBello C., and Lingen M.W. Prediction of in vivo synergistic activity of antiangiogenic compounds by gene expression profiling. Cancer Res. 62 (2002) 7143-7148
142. Shaked Y., Bertolini F., Man S., Rogers M.S., Cervi D., Foutz T., Rawn K., Voskas D., Dumont D.J., Ben-David Y., Lawler J., Henkin J., Huber J., Hicklin D.J., D'Amato R.J., and Kerbel R.S. Genetic heterogeneity of the vasculogenic phenotype parallels angiogenesis; Implications for cellular surrogate marker analysis of antiangiogenesis. Cancer Cell 7 (2005) 101-111
143. Bussolati B., Deambrosis I., Russo S., Deregibus M.C., and Camussi G. Altered angiogenesis and survival in human tumor-derived endothelial cells. FASEB J. 17 (2003) 1159-1161
144. St Croix B., Rago C., Velculescu V., Traverso G., Romans K.E., Montgomery E., Lal A., Riggins G.J., Lengauer C., Vogelstein B., and Kinzler K.W. Genes expressed in human tumor endothelium. Science 289 (2000) 1197-1202
145. Orr A.W., Elzie C.A., Kucik D.F., and Murphy-Ullrich J.E. Thrombospondin signaling through the calreticulin/LDL receptor-related protein co-complex stimulates random and directed cell. J. Cell Sci. 116 (2003) 2912-2917