Expresson 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

American Journal of Pathology

Volumn 159, Issue 1, 2001, Pages 223-235

  Straume, Oddbjørn ^a   Akslen, Lars Andreas ^a  

^a HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL CELL GROWTH FACTOR; GROWTH FACTOR RECEPTOR; ISOPROTEIN; LYMPHOKINE; MESSENGER RNA; ONCOPROTEIN; PROTEIN TYROSINE KINASE; THROMBOSPONDIN 1; VASCULOTROPIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1;

ARTICLE; BLOOD VESSEL; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; MELANOMA; METABOLISM; METHODOLOGY; MICROCIRCULATION; PATHOLOGY; SKIN TUMOR; STAINING; SURVIVAL; VASCULARIZATION;

BLOOD VESSELS; ENDOTHELIAL GROWTH FACTORS; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHOKINES; MELANOMA; MICROCIRCULATION; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, GROWTH FACTOR; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RNA, MESSENGER; SKIN NEOPLASMS; STAINING AND LABELING; SURVIVAL ANALYSIS; THROMBOSPONDIN 1; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0035404270     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)61688-4     Document Type: Article

References (99)

1. Folkman J: What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst 1990, 82:4-6
2. Weidner N, Semple JP, Welch WR, Folkman J: Tumor angiogenesis and metastasis- correlation in invasive breast carcinoma. N Engl J Med 1991, 324:1-8
3. Salvesen HB, Iversen OE, Akslen LA: Prognostic significance of angiogenesis and Ki-67, p53, and p21 expression: a population-based endometrial carcinoma study. J Clin Oncol 1999, 17:1382-1390
4. Weidner N, Carroll PR, Flax J, Blumenfeld W, Folkman J: Tumor angiogenesis correlates with metastasis in invasive prostate carcinoma. Am J Pathol 1993, 143:401-409
5. Carnochan P, Briggs JC, Westbury G, Davies AJ: The vascularity of cutaneous melanoma: a quantitative histological study of lesions 0.85-1.25 mm in thickness. Br J Cancer 1991, 64:102-107
6. Ribatti D, Vacca A, Palma W, Lospalluti M, Dammacco F: Angiogenesis during tumor progression in human malignant melanoma. EXS 1992, 61:415-420
7. Barnhill RL, Fandrey K, Levy MA, Mihm MC Jr, Hyman B: Angiogenesis and tumor progression of melanoma: quantification of vascularity in melanocytic nevi and cutaneous malignant melanoma. Lab Invest 1992, 67:331-337
8. Graham CH, Rivers J, Kerbel RS, Stankiewicz KS, White WL: Extent of vascularization as a prognostic indicator in thin (< 0.76 mm) malignant melanomas. Am J Pathol 1994, 145:510-514
9. Busam KJ, Berwick M, Blessing K, Fandrey K, Kang S, Karaoli T, Fine J, Cochran AJ, White WL, Rivers J: Tumor vascularity is not a prognostic factor for malignant melanoma of the skin. Am J Pathol 1995, 147:1049-1056
10. Rongioletti F, Miracco C, Gambini C, Pastorino A, Tosi P, Rebora A: Tumor vascularity as a prognostic indicator in intermediate-thickness (0.76-4 mm) cutaneous melanoma: a quantitative assay. Am J Dermatopathol 1996, 18:474-477
11. Marcoval J, Moreno A, Graells J, Vidal A, Escriba JM, Garcia Ramirez M, Fabra A: Angiogenesis and malignant melanoma: angiogenesis is related to the development of vertical (tumorigenic) growth phase. J Cutan Pathol 1997, 24:212-218
12. Neitzel LT, Neitzel CD, Magee KL, Malafa MP: Angiogenesis correlates with metastasis in melanoma. Ann Surg Oncol 1999, 6:70-74
13. Straume O, Salvesen HB, Akslen LA: Angiogenesis is prognostically important in vertical growth phase melanomas. Int J Oncol 1999, 15:595-599
14. Ferrara N: Molecular and biological properties of vascular endothelial growth factor J Mol Med 1999, 77:527-543
15. Guidi AJ, Schnitt SJ, Fischer L, Tognazzi K, Harris JR, Dvorak HF, Brown LF: Vascular permeability factor (vascular endothelial growth factor) expression and angiogenesis in patients with ductal carcinoma in situ of the breast. Cancer 1997, 80:1945-1953
16. Kang SM, Maeda K, Onoda N, Chung YS, Nakata B, Nishiguchi Y, Sowa M: Combined analysis of p53 and vascular endothelial growth factor expression in colorectal carcinoma for determination of tumor vascularity and liver metastasis. Int J Cancer 1997, 74:502-507
17. Fontanini G, Boldrini L, Calcinai A, Chine S, Lucchi M, Mussi A, Angeletti CA, Basolo F, 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 1999, 5:155-161
18. Takahashi Y, Bucana CD, Cleary KR, Ellis LM: p53, vessel count, and vascular endothelial growth factor expression in human colon cancer. Int J Cancer 1998, 79:34-38
19. Claffey KP, Brown LF, del Aguila LF, Tognazzi K, Yeo KT, Manseau EJ, Dvorak HF: Expression of vascular permeability factor/vascular endothelial growth factor by melanoma cells increases tumor growth, angiogenesis, and experimental metastasis. Cancer Res 1996, 56: 172-181
20. Detmar M, Velasco P, Richard L, Claffey KP, Streit M, Riccardi L, Skobe M, Brown LF: Expression of vascular endothelial growth factor induces an invasive phenotype in human squamous cell carcinomas. Am J Pathol 2000, 156:159-167
21. Erhard H, Rietveld FJ, van Altena MC, Brocker EB, Ruiter DJ, de Waal RM: Transition of horizontal to vertical growth phase melanoma is accompanied by induction of vascular endothelial growth factor expression and angiogenesis. Melanoma Res 1997, 7(Suppl 2):19-26
22. Salven P, Heikkila P, Joensuu H: Enhanced expression of vascular endothelial growth factor in metastatic melanoma. Br J Cancer 1997, 930-934
23. Houck KA, Ferrara N, Winer J, Cachianes G, Li B, Leung DW: The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol Endocrinol 1991, 5:1806-1814
24. Fontanini G, Boldrini L, Chine S, Pisaturo F, Basolo F, Calcinai A, Lucchi M, Mussi A, Angeletti CA, Bevilacqua G: Expression of vascular endothelial growth factor mRNA in non-small-cell lung carcinomas. Br J Cancer 1999, 79:363-369
25. Tokunaga T, Oshika Y, Abe Y, Ozeki Y, Sadahiro S, Kijima H, Tsuchida T, Yamazaki H, Ueyama Y, Tamaoki N, Nakamura M: Vascular endothelial growth factor (VEGF) mRNA isoform expression pattern is correlated with liver metastasis and poor prognosis in colon cancer. Br J Cancer 1998, 77:998-1002
26. Tomisawa M, Tokunaga T, Oshika Y, Tsuchida T, Fukushima Y, Sato H, Kijima H, Yamazaki H, Ueyama Y, Tamaoki N, Nakamura M: Expression pattern of vascular endothelial growth factor isoform is closely correlated with tumour stage and vascularisation in renal cell carcinoma. Eur J Cancer 1999, 35:133-137
27. Lee YH, Tokunaga T, Oshika Y, Suto R, Yanagisawa K, Tomisawa M, Fukuda H, Nakano H, Abe S, Tateishi A, Kijima H, Yamazaki H, Tamaoki N, Ueyama Y, Nakamura M: Cell-retained isoforms of vascular endothelial growth factor (VEGF) are correlated with poor prognosis in osteosarcoma. Eur J Cancer 1999, 35:1089-1093
28. de Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT: The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 1992, 255:989-991
29. Terman BI, Dougher-Vermazen M, Carrion ME, Dimitrov D, Armellino DC, Gospodarowicz D, Bohlen P: Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor. Biochem Biophys Res Commun 1992, 187:1579-1586
30. Boocock CA, Charnock-Jones DS, Sharkey AM, McLaren J, Barker PJ, Wright KA, Twentyman PR, Smith SK: Expression of vascular endothelial growth factor and its receptors flt and KDR in ovarian carcinoma. J Natl Cancer Inst 1995, 87:506-516
31. Gitay-Goren H, Halaban R, Neufeld G: Human melanoma cells but not normal melanocytes express vascular endothelial growth factor receptors. Biochem Biophys Res Commun 1993, 190:702-708
32. Stitt AW, Simpson DA, Boocock C, Gardiner TA, Murphy GM, Archer DB: Expression of vascular endothelial growth factor (VEGF) and its receptors is regulated in eyes with intra-ocular tumors. J Pathol 1998, 186:306-312
33. Graeven U, Fiedler W, Karpinski S, Ergun S, Kilic N, Rodeck U, Schmiegel W, Hossfeld DK: Melanoma-associated expression of vascular endothelial growth factor and its receptors FLT-1 and KDR. J Cancer Res Clin Oncol 1999, 125:621-629
34. Bunone G, Vigneri P, Mariani L, Buto S, Collini P, Pilotti S, Pierotti MA, Bongarzone I: Expression of angiogenesis stimulators and inhibitors in human thyroid tumors and correlation with clinical pathological features. Am J Pathol 1999, 155:1967-1976
35. de Jong JS, van Diest PJ, van der Valk P, Baak JP: Expression of growth factors, growth inhibiting factors, and their receptors in invasive breast cancer. I: An inventory in search of autocrine and paracrine loops. J Pathol 1998, 184:44-52
36. Liu B, Earl HM, Baban D, Shoaibi M, Fabra A, Kerr DJ, Seymour LW: Melanoma cell lines express VEGF receptor KDR and respond to exogenously added VEGF. Biochem Biophys Res Commun 1995, 217:721-727
37. Herold-Mende C, Steiner HH, Andl T, Riede D, Buttler A, Reisser C, Fusenig NE, Mueller MM: Expression and functional significance of vascular endothelial growth factor receptors in human tumor cells. Lab Invest 1999, 79:1573-1582
38. Roberts DD: Regulation of tumor growth and metastasis by thrombospondin-1. FASEB J 1996, 10:1183-1191
39. Tuszynski GP, Gasic TB, Rothman VL, Knudsen KA, Gasic GJ: Thrombospondin, a potentiator of tumor cell metastasis. Cancer Res 1987, 47:4130-4133
40. Wong SY, Purdie AT, Han P: Thrombospondin and other possible related matrix proteins in malignant and benign breast disease: an immunohistochemical study. Am J Pathol 1992, 140:1473-1482
41. Wang TN, Qian X, Granick MS, Solomon MP, Rothman VL, Berger DH, Tuszynski GP: Thrombospondin-1 (TSP-1) promotes the invasive properties of human breast cancer: J Surg Res 1996, 63:39-43
42. Weinstat-Saslow DL, Zabrenetzky VS, VanHoutte K, Frazier WA, Roberts DD, Steeg PS: Transfection of thrombospondin 1 complementary DNA into a human breast carcinoma cell line reduces primary tumor growth, metastatic potential and angiogenesis. Cancer Res 1994, 54:6504-6511
43. Zabrenetzky V, Harris CC, Steeg PS, Roberts DD: Expression of the extracellular matrix molecule thrombospondin inversely correlates with malignant progression in melanoma, lung and breast carcinoma cell lines. Int J Cancer 1994, 59:191-195
44. Dameron KM, Volpert OV, Tainsky MA, Bouck N: Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science 1994, 265:1582-1584
45. Grossfeld GD, Ginsberg DA, Stein JP, Bochner BH, Esrig D, Groshen S, Dunn M, Nichols PW, Taylor CR, Skinner DG, Cote RJ: Thrombospondin-1 expression in bladder cancer: association with p53 alterations, tumor angiogenesis, and tumor progression. J Natl Cancer Inst 1997, 89:219-227
46. Volpert OV, Dameron KM, Bouck N: Sequential development of an angiogenic phenotype by human fibroblasts progressing to tumorigenicity. Oncogene 1997, 14:1495-1502
47. Grant SW, Kyshtoobayeva AS, Kurosaki T, Jakowatz J, Fruehauf JP: Mutant p53 correlates with reduced expression of thrombospondin-1, increased angiogenesis, and metastatic progression in melanoma. Cancer Detect Prev 1998, 22:185-194
48. Tokunaga T, Nakamura M, Oshika Y, Abe Y, Ozeki Y, Fukushima Y, Hatanaka H, Sadahiro S, Kijima H, Tsuchida T, Yamazaki H, Tamaoki N, Ueyama Y: Thrombospondin 2 expression is correlated with inhibition of angiogenesis and metastasis of colon cancer. Br J Cancer 1999, 79:354-359
49. Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N: Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 2000, 6:41-48
50. Chandrasekaran L, He CZ, Al-Barazi H, Krutzsch HC, Iruela-Arispe ML, Roberts DD: Cell contact-dependent activation of α3β1 integrin modulates endothelial cell responses to thrombospondin-1. Mol Biol Cell 2000, 11:2885-2900
51. Taraboletti G, Morbidelli L, Donnini S, Parenti A, Granger HJ, 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 2000, 14:1674-1676
52. Mukhopadhyay D, Tsiokas L, Sukhatme VP: Wild-type p53 and v-Src exert opposing influences on human vascular endothelial growth factor gene expression. Cancer Res 1995, 55:6161-6165
53. Fontanini G, Vignati S, Lucchi M, Mussi A, Calcinai A, Boldrini L, Chine S, Silvestri V, Angeletti CA, Basolo F, Bevilacqua G: Neoangiogenesis and p53 protein in lung cancer: their prognostic role and their relation with vascular endothelial growth factor (VEGF) expression. Br J Cancer 1997, 75:1295-1301
54. Kamb A, Shattuck Eidens D, Eeles R, Liu Q, Gruis NA, Ding W, Hussey C, Tran T, Miki Y, Weaver Feldhaus J, McClure M, Aitken JF, Anderson DE, Bergman W, Frants R, Goldgar DE, Green A, MacLennan R, Martin NG, Meyer LJ, Youl P, Zone JJ, Skolnick MH, Cannon-Albright LA: Analysis of the p16 gene (CDKN2) as a candidate for the chromosome 9p melanoma susceptibility locus. Nat Genet 1994, 8:23-26
55. Kumar R, Lundh Rozell B, Louhelainen J, Hemminki K: Mutations in the CDKN2A (p16INK4a) gene in microdissected sporadic primary melanomas. Int J Cancer 1998, 75:193-198
56. Straume O, Sviland L, Akslen LA: Loss of nuclear p16 protein expression correlates with increased tumor cell proliferation (Ki-67) and poor prognosis in patients with vertical growth phase melanoma. Clin Cancer Res 2000, 6:1845-1853
57. Harada H, Nakagawa K, Iwata S, Saito M, Kumon Y, Sakaki S, Sato K, Hamada K: Restoration of wild-type p16 down-regulates vascular endothelial growth factor expression and inhibits angiogenesis in human gliomas. Cancer Res 1999, 59:3783-3789
58. Watanabe Y, Lee SW, Detmar M, Ajioka I, Dvorak HF: Vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) delays and induces escape from senescence in human dermal microvascular endothelial cells. Oncogene 1997, 14:2025-2032
59. Elder DE, Murphy GF: Melanocytic tumors of the skin. Atlas of Tumor Pathology, Edited by J Rosai and LH Sobin Washington DC, AFIP, 1991, pp 119-131
60. Yoneda J, Kuniyasu H, Crispens MA, Price JE, Bucana CD, Fidler IJ: Expression of angiogenesis-related genes and progression of human ovarian carcinomas in nude mice. J Natl Cancer Inst 1998, 90:447-454
61. Yamamoto S, Yasu W, Kitadai Y, Yokozaki H, Haruma K, Kajiyama G, Tahara E: Expression of vascular endothelial growth factor in human gastric carcinomas. Pathol Int 1998, 48:499-506
62. Chomczynski P, Sacchi N: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987, 162:156-159
63. Burrows FJ, Derbyshire EJ, Tazzari PL, Amlot P, Gazdar AF, King SW, Letarte M, Vitetta ES, Thorpe PE: Up-regulation of endoglin on vascular endothelial cells in human solid tumors: implications for diagnosis and therapy. Clin Cancer Res 1995, 1:1623-1634
64. Bodey B, Bodey B Jr. Siegel SE, Kaiser HE: Up-regulation of endoglin (CD105) expression during childhood brain tumor-related angiogenesis. Anti-angiogenic therapy. Anticancer Res 1998, 18:1485-1500
65. Miller DW, Graulich W, Karges B, Stahl S, Ernst M, Ramaswamy A, Sedlacek HH, Muller R, Adamkiewicz J: Elevated expression of endoglin, a component of the TGF-β-receptor complex, correlates with proliferation of tumor endothelial cells. Int J Cancer 1999, 81:568-572
66. Matsuno F, Haruta Y, Kondo M, Tsai H, Barcos M, Seon BK: Induction of lasting complete regression of preformed distinct solid tumors by targeting the tumor vasculature using two new anti-endoglin monoclonal antibodies. Clin Cancer Res 1999, 5:371-382
67. Grossfeld GD, Shi SR, Ginsberg DA, Rich KA, Skinner DG, Taylor CR, Cote RJ: Immunohistochemical detection of thrombospondin-1 in formalin-fixed, paraffin-embedded tissue. J Histochem Cytochem 1996, 44:761-766
68. Norusis M: SPSS Advanced Statistics, Version 6.1. SPSS. Inc., Chicago, IL, 1994
69. Cox DR: Regression models and life-tables. J R Stat Soc 1972, 34:187-222
70. Weidner N: Tumoural vascularity as a prognostic factor in cancer: the evidence continues to grow. J Pathol 1998, 184:119-122
71. Norrby K: Angiogenesis: new aspects relating to its initiation and control. Acta Pathol Microbiol Immunol Scand 1997, 105:417-437
72. Freeman MR, Schneck FX, Gagnon ML, Corless C, Soker S, Niknejad K, Peoples GE Klagsbrun M: Peripheral blood T lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role for T cells in angiogenesis. Cancer Res 1995, 55:4140-4145
73. Watanabe M, McCormick KL, Volker K, Ortaldo JR, Wigginton JM, Brunda MJ, Wiltrout RH, Fogler WE: Regulation of local host-mediated anti-tumor mechanisms by cytokines: direct and indirect effects on leukocyte recruitment and angiogenesis. Am J Pathol 1997, 150: 1869-1880
74. Kumar S, Ghellal A, Li C, Byrne G, Haboubi N, Wang JM, Bundred N: Breast carcinoma: vascular density determined using CD1C5 antibody correlates with tumor prognosis. Cancer Res 1999, 59:856-861
75. Maniotis AJ, Folberg R, Hess A, Seftor EA, Gardner LM Pe'er J, Trent JM, Meltzer PS, Hendrix MJ: Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999, 155:739-752
76. Folberg R, Hendrix MJ, Maniotis AJ: Vasculogenic mimicry and tumor angiogenesis. Am J Pathol 2000, 156:361-381
77. McDonald DM, Munn L, Jain RK: Vasculogenic mimicry: how convincing, how novel, and how significant? Am J Pathol 2000, 156:383-388
78. Nor JE, Christensen J, Mooney DJ, Polverini PJ: Vascular endothelial growth factor (VEGF)-mediated angiogenesis is associated with enhanced endolhellal cell survival and induction of Bcl-2 expression. Am J Pathol 1999, 154:375-384
79. Potgens AJ, van Altena MC, Lubsen NH, Ruiter DJ, de Waal RM: Analysis of the tumor vasculature and metastatic behavior of xenografts of human melanoma cell lines transfected with vascular permeability factor Am J Pathol 1996, 148:1203-1217
80. Stone J, Itin A, Alon T, Pe'er J, Gnessin H, Chan-Ling T, Keshet E: Development of retinal vasculature s mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 1995, 15:4738-4747
81. Damelsen T, Rofstad EK: The constitutive level of vascular endothelial growth factor (VEGF) is more important than hypoxia-induced VEGF up-regulation in the angiogenesis of human melanoma xenografts. Br J Cancer 2000, 82:1528-1534
82. Westphal JR, Hullenaar RV, Peek R, Willems RW, Crickard K, Crickard U, Askaa J, Clemmensen I, Ruiter DJ, De Waal RMW: Angicgenic balance in human melanoma: expression of VEGF, bFGF, IL-8, PDGF and angiostatin in relation to vascular density of xenografts in vivo. Int J Cancer 2000, 86:768-776
83. Easty DJ, Hill SP, Hsu MY, Fallowfield ME, Florenes VA Herlyn M, Bennett DC: Up-regulation of ephrin-A1 during melanoma progression. Int J Cancer 1999, 84:494-501
84. Rofstad EK, Halsor EF: Vascular endothelial growth factor interleukin 8, platelet-derived endothelial cell growth factor, and basic fibroblast growth factor promote angiogenesis and metastasis in human melanoma xenografts. Cancer Res 2000 60:4932-4938
85. Mineta H, Miura K, Ogino T, Takebayashi S, Misawa K, Ueda Y, Suzuki I, Dictor M, Borg A, Wennerberg J: Prognostic value of vascular endothelial growth factor (VEGF) in head and neck squamous cell carcinomas. Br J Cancer 2000, 83:775-781
86. Clauss M, Weich H, Breier G, Knies U, Rockl W, Waltenberger J, Risau W: The vascular endothelial growth factor receptor Flt-1 mediates biological activities. Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J Biol Chem 1996, 271:17629-17634
87. Wang H, Keiser JA: Vascular endothelial growth factor up-regulates the expression of matrix metalloproteinases in vascular smooth muscle cells: role of flt-1. Circ Res 1998, 83:832-840
88. Xie B, Tam NN Tsao SW, Wong YC: Co-expression of vascular endothelial growth factor (VEGF) and its receptors (flk-1 and flt-1) in hormone-induced mammary cancer in the Noble rat. Br J Cancer 1999, 81:1335-1343
89. Dunk C, Ahmed A: Vascular endothelial growth factor receptor-2-mediated mitogenesis is negatively regulated by vascular endothelial growth factor receptor-1 in tumor epithelial cells. Am J Pathol 2001, 158:265-273
90. Veikkola T, Karkkainen M, Claesson-Welsh L, Alitalo K: Regulation of angiogenesis via vascular endothelial growth factor receptors. Cancer Res 2000, 60:203-212
91. DiPietro LA: Thrombospondin as a regulator of angiogenesis. EXS 1997, 79:295-314
92. Roberts DD, Sherwood JA, Ginsburg V: Platelet thrombospondin mediates attachment and spreading of human melanoma cells. J Cell Biol 1987, 104:131-139
93. Tuszynski GP, Nicosia RF: The role of thrombospondin-1 in tumor progression and angiogenesis. Bioessays 1996, 18:71-76
94. Tuszynski GP, Wang TN, Berger D: Adhesive proteins and the hematogenous spread of cancer. Acta Haematol 1997, 97:29-39
95. Roth JJ, Albo D, Rothman VL, Longaker MT, Granick MS, Long CD, Solomon MP, Tuszynski GP: Thrombospondin-1 and its CSVTCG-specific receptor in wound healing and cancer. Ann Plast Surg 1998, 40:494-501
96. Albelda SM, Mette SA, Elder DE, Stewart R, Damjanovich L, Herlyn M, Buck CA: Integrin distribution in malignant melanoma: association of the β 3 subunit with tumor progression. Cancer Res 1990, 50:6757-6764
97. Felding-Habermann B, Mueller BM, Romerdahl CA, Cheresh DA: Involvement of integrin α V gene expression in human melanoma tumorigenicity. J Clin Invest 1992, 89:2018-2022
98. Hieken TJ, Farolan M, Ronan SG, Shilkaitis A, Wild L, Das Gupta TK β3 integrin expression in melanoma predicts subsequent metastasis. J Surg Res 1996, 63:169-173
99. Van Belle PA, Elenitsas R, Satyamoorthy K, Wolfe JT, Guerry Dt, Schuchter L, Van Belle TJ, Albelda S, Tahin P, Herlyn M, Elder DE: Progression-related expression of β3 integrin in melanomas and nevi. Hum Pathol 1999, 30:562-567