Angiogenesis, vasculogenic mimicry and vascular invasion in cutaneous malignant melanoma-implications for therapeutic strategies and targeted therapies

Expert Review of Anticancer Therapy

Volumn 14, Issue 5, 2014, Pages 621-639

  Chung, Hye Jin ^a   Mahalingam, Meera ^b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; anti angiogenesis; lymphovascular invasion; melanoma; vascular invasion; vasculogenic mimicry

Indexed keywords

BEVACIZUMAB; CARBOPLATIN; CYCLIC AMP; ENDOSTATIN; ETARACIZUMAB; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; GALECTIN 3; INTEGRIN; INTERLEUKIN 8; MATRIX METALLOPROTEINASE; PACLITAXEL; PLATELET DERIVED GROWTH FACTOR; PRINOMASTAT; PROTEIN KINASE INHIBITOR; SORAFENIB; TEMSIROLIMUS; THROMBOSPONDIN; VASCULOTROPIN;

ADVANCED CANCER; ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; CANCER CELL; CANCER GROWTH; CANCER STAGING; CANCER SURVIVAL; CARCINOGENESIS; CUTANEOUS MELANOMA; DRUG RESPONSE; DRUG TARGETING; HUMAN; MELANOMA; MICROCIRCULATION; MOLECULARLY TARGETED THERAPY; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; TUMOR INVASION; TUMOR VASCULARIZATION; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; VASCULARIZATION;

HUMANS; MELANOMA; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84898950560     PISSN: 14737140     EISSN: 17448328     Source Type: Journal    
DOI: 10.1586/14737140.2014.883281     Document Type: Review

References (261)

1. Wolf JE Jr., Hubler WR Jr. Tumor angiogenic factor and human skin tumors. Arch Dermatol 1975;111(3):321-7
2. Warren BA, Shubik P. The growth of the blood supply to melanoma transplants in the hamster cheek pouch. Lab Invest 1966; 15(2):464-78
3. Schumacker PT, Samsel RW. Analysis of oxygen delivery and uptake relationships in the Krogh tissue model. J Appl Physiol 1989;67(3):1234-44
4. Ehrmann RL, Knoth M. Choriocarcinoma. Transfilter stimulation of vasoproliferation in the hamster cheek pouch. Studied by light and electron microscopy. J Natl Cancer Inst 1968;41(6):1329-41
5. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971;285(21): 1182-6
6. Maniotis AJ, Folberg R, Hess A, et al. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999; 155(3):739-52
7. Mohammed RA, Martin SG, Gill MS, et al. Improved methods of detection of lymphovascular invasion demonstrate that it is the predominant method of vascular invasion in breast cancer and has important clinical consequences. Am J Surg Pathol 2007;31(12):1825-33
8. Mohammed RA, Ellis IO, Lee AH, Martin SG. Vascular invasion in breast cancer; an overview of recent prognostic developments and molecular pathophysiological mechanisms. Histopathology 2009;55(1):1-9
9. Bu Z, Zheng Z, Li Z, et al. Lymphatic vascular invasion is an independent correlated factor for lymph node metastasis and the prognosis of resectable T2 gastric cancer patients. Tumour Biol 2013;34(2):1005-12
10. Gresta LT, Rodrigues-Junior IA, de Castro LP, et al. Assessment of vascular invasion in gastric cancer: a comparative study. World J Gastroenterol 2013;19(24): 3761-9
11. Betge J, Pollheimer MJ, Lindtner RA, et al. Intramural and extramural vascular invasion in colorectal cancer: prognostic significance and quality of pathology reporting. Cancer 2012;118(3):628-38
12. Courtney ED, West NJ, Kaur C, et al. Extramural vascular invasion is an adverse prognostic indicator of survival in patients with colorectal cancer. Colorectal Dis 2009; 11(2):150-6
13. Khanna M, Fortier-Riberdy G, Dinehart SM, Smoller B. Histopathologic evaluation of cutaneous squamous cell carcinoma: results of a survey among dermatopathologists. J Am Acad Dermatol 2003;48(5):721-6
14. Sondergaard K, Schou G. Therapeutic and clinico-pathological factors in the survival of 1,469 patients with primary cutaneous malignant melanoma in clinical stage I. A multivariate regression analysis. Virchows Arch A Pathol Anat Histopathol 1985; 408(2-3):249-58
15. Gamel JW, George SL, Stanley WE, Seigler HF. Skin melanoma. Cured fraction and survival time as functions of thickness, site, histologic type, age, and sex. Cancer 1993;72(4):1219-23
16. Bachaud JM, Shubinski R, Boussin G, et al. Stage I cutaneous malignant melanoma: risk factors of loco-regional recurrence after wide local excision and clinical perspectives. Eur J Surg Oncol 1992;18(5):442-8
17. MacKie RM, Aitchison T, Sirel JM, et al. Prognostic models for subgroups of melanoma patients from the Scottish Melanoma Group database 1979-86, and their subsequent validation. Br J Cancer 1995;71(1):173-6
18. Kashani-Sabet M, Sagebiel RW, Ferreira CM, et al. Vascular involvement in the prognosis of primary cutaneous melanoma. Arch Dermatol 2001;137(9): 1169-73
19. Storr SJ, Safuan S, Mitra A, et al. Objective assessment of blood and lymphatic vessel invasion and association with macrophage infiltration in cutaneous melanoma. Mod Pathol 2012;25(4):493-504
20. Balch CM, Gershenwald JE, Soong SJ, et al. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 2009;27(36):6199-206
21. Folkman J. Angiogenesis. Annu Rev Med 2006;57:1-18
22. Streit M, Detmar M. Angiogenesis, lymphangiogenesis, and melanoma metastasis. Oncogene 2003;22(20):3172-9
23. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 1999;13(1):9-22
24. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev 2004;25(4):581-611
25. Redondo P, Bandres E, Solano T, et al. Vascular endothelial growth factor (VEGF) and melanoma. N-acetylcysteine downregulates VEGF production in vitro. Cytokine 2000;12(4):374-8
26. Potgens AJ, Lubsen NH, van Altena MC, et al. Vascular permeability factor expression influences tumor angiogenesis in human melanoma lines xenografted to nude mice. Am J Pathol 1995;146(1):197-209
27. Yu JL, Rak JW, Klement G, Kerbel RS. Vascular endothelial growth factor isoform expression as a determinant of blood vessel patterning in human melanoma xenografts. Cancer Res 2002;62(6):1838-46
28. Pritchard-Jones RO, Dunn DB, Qiu Y, et al. Expression of VEGF(xxx)b, the inhibitory isoforms of VEGF, in malignant melanoma. Br J Cancer 2007;97(2):223-30
29. Ribatti D. The discovery of the placental growth factor and its role in angiogenesis: a historical review. Angiogenesis 2008;11(3): 215-21
30. Odorisio T, Cianfarani F, Failla CM, Zambruno G. The placenta growth factor in skin angiogenesis. J Dermatol Sci 2006; 41(1):11-19
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(3):702-8
32. Ribatti D, Nico B, Floris C, et al. Microvascular density, vascular endothelial growth factor immunoreactivity in tumor cells, vessel diameter and intussusceptive microvascular growth in primary melanoma. Oncol Rep 2005;14(1):81-4
33. Erhard H, Rietveld FJ, van Altena MC, et al. 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):S19-26
34. Gorski DH, Leal AD, Goydos JS. Differential expression of vascular endothelial growth factor-A isoforms at different stages of melanoma progression. J Am Coll Surg 2003;197(3):408-18
35. Rajabi P, Neshat A, Mokhtari M, et al. The role of VEGF in melanoma progression. J Res Med Sci 2012;17(6):534-9
36. Salven P, Heikkila P, Joensuu H. Enhanced expression of vascular endothelial growth factor in metastatic melanoma. Br J Cancer 1997;76(7):930-4
37. Mehnert JM, McCarthy MM, Jilaveanu L, et al. Quantitative expression of VEGF, VEGF-R1, VEGF-R2, and VEGF-R3 in melanoma tissue microarrays. Hum Pathol 2010;41(3):375-84
38. Tas F, Duranyildiz D, Oguz H, et al. Circulating levels of vascular endothelial growth factor (VEGF), matrix metalloproteinase-3 (MMP-3), and BCL-2 in malignant melanoma. Med Oncol 2008;25(4):431-6
39. Redondo P, Sanchez-Carpintero I, Bauza A, et al. Immunologic escape and angiogenesis in human malignant melanoma. J Am Acad Dermatol 2003;49(2):255-63
40. Ugurel S, Rappl G, Tilgen W, Reinhold U. Increased serum concentration of angiogenic factors in malignant melanoma patients correlates with tumor progression and survival. J Clin Oncol 2001;19(2):577-83
41. Pelletier F, Bermont L, Puzenat E, et al. Circulating vascular endothelial growth factor in cutaneous malignant melanoma. Br J Dermatol 2005;152(4):685-9
42. Barak V, Pe'er J, Kalickman I, Frenkel S. VEGF as a biomarker for metastatic uveal melanoma in humans. Curr Eye Res 2011; 36(4):386-90
43. Bayer-Garner IB, Hough AJ Jr., Smoller BR. Vascular endothelial growth factor expression in malignant melanoma: prognostic versus diagnostic usefulness. Mod Pathol 1999;12(8):770-4
44. Depasquale I, Thompson WD. Prognosis in human melanoma: PAR-1 expression is superior to other coagulation components and VEGF. Histopathology 2008;52(4): 500-9
45. Presta M, Dell'Era P, Mitola S, et al. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev 2005;16(2): 159-78
46. Acevedo VD, Ittmann M, Spencer DM. Paths of FGFR-driven tumorigenesis. Cell Cycle 2009;8(4):580-8
47. Rogelj S, Klagsbrun M, Atzmon R, et al. Basic fibroblast growth factor is an extracellular matrix component required for supporting the proliferation of vascular endothelial cells and the differentiation of PC12 cells. J Cell Biol 1989;109(2):823-31
48. Folkman J, Klagsbrun M, Sasse J, et al. A heparin-binding angiogenic protein-basic fibroblast growth factor-is stored within basement membrane. Am J Pathol 1988; 130(2):393-400
49. DiMario J, Buffinger N, Yamada S, Strohman RC. Fibroblast growth factor in the extracellular matrix of dystrophic (mdx) mouse muscle. Science 1989;244(4905): 688-90
50. Halaban R, Ghosh S, Baird A. bFGF is the putative natural growth factor for human melanocytes. In Vitro Cell Dev Biol 1987; 23(1):47-52
51. Reed JA, McNutt NS, Albino AP. Differential expression of basic fibroblast growth factor (bFGF) in melanocytic lesions demonstrated by in situ hybridization. Implications for tumor progression. Am J Pathol 1994;144(2):329-36
52. Ueda M, Funasaka Y, Ichihashi M, Mishima Y. Stable and strong expression of basic fibroblast growth factor in naevus cell naevus contrasts with aberrant expression in melanoma. Br J Dermatol 1994;130(3): 320-4
53. Albino AP, Davis BM, Nanus DM. Induction of growth factor RNA expression in human malignant melanoma: markers of transformation. Cancer Res 1991;51(18): 4815-20
54. Streit S, Mestel DS, Schmidt M, et al. FGFR4 Arg388 allele correlates with tumour thickness and FGFR4 protein expression with survival of melanoma patients. Br J Cancer 2006;94(12):1879-86
55. Demirkesen C, Buyukpinarbasili N, Ramazanoglu R, et al. The correlation of angiogenesis with metastasis in primary cutaneous melanoma: a comparative analysis of microvessel density, expression of vascular endothelial growth factor and basic fibroblastic growth factor. Pathology 2006; 38(2):132-7
56. Coleman AB, Lugo TG. Normal human melanocytes that express a bFGF transgene still require exogenous bFGF for growth in vitro. J Invest Dermatol 1998;110(5):793-9
57. Wang Y, Becker D. Antisense targeting of basic fibroblast growth factor and fibroblast growth factor receptor-1 in human melanomas blocks intratumoral angiogenesis and tumor growth. Nat Med 1997;3(8): 887-93
58. Yu Y, Gao S, Li Q, et al. The FGF2-binding peptide P7 inhibits melanoma growth in vitro and in vivo. J Cancer Res Clin Oncol 2012;138(8): 1321-8
59. Becker D, Meier CB, Herlyn M. Proliferation of human malignant melanomas is inhibited by antisense oligodeoxynucleotides targeted against basic fibroblast growth factor. EMBO J 1989; 8(12):3685-91
60. Valesky M, Spang AJ, Fisher GW, et al. Noninvasive dynamic fluorescence imaging of human melanomas reveals that targeted inhibition of bFGF or FGFR-1 in melanoma cells blocks tumor growth by apoptosis. Mol Med 2002;8(2):103-12
61. Li D, Wang H, Xiang JJ, et al. Monoclonal antibodies targeting basic fibroblast growth factor inhibit the growth of B16 melanoma in vivo and in vitro. Oncol Rep 2010;24(2): 457-63
62. Metzner T, Bedeir A, Held G, et al. Fibroblast growth factor receptors as therapeutic targets in human melanoma: synergism with BRAF inhibition. J Invest Dermatol 2011;131(10):2087-95
63. Fischer H, Taylor N, Allerstorfer S, et al. Fibroblast growth factor receptor-mediated signals contribute to the malignant phenotype of non-small cell lung cancer cells: therapeutic implications and synergism with epidermal growth factor receptor inhibition. Mol Cancer Ther 2008;7(10): 3408-19
64. Kono SA, Marshall ME, Ware KE, Heasley LE. The fibroblast growth factor receptor signaling pathway as a mediator of intrinsic resistance to EGFR-specific tyrosine kinase inhibitors in non-small cell lung cancer. Drug Resist Updat 2009;12(4-5): 95-102
65. Barnhill RL, Xiao M, Graves D, Antoniades HN. Expression of platelet-derived growth factor (PDGF)-A, PDGF-B and the PDGF-alpha receptor, but not the PDGF-beta receptor, in human malignant melanoma in vivo. Br J Dermatol 1996;135(6):898-904
66. McGary EC, Onn A, Mills L, et al. Imatinib mesylate inhibits platelet-derived growth factor receptor phosphorylation of melanoma cells but does not affect tumorigenicity in vivo. J Invest Dermatol 2004;122(2):400-5
67. Furuhashi M, Sjoblom T, Abramsson A, et al. Platelet-derived growth factor production by B16 melanoma cells leads to increased pericyte abundance in tumors and an associated increase in tumor growth rate. Cancer Res 2004;64(8):2725-33
68. Robinson SP, Ludwig C, Paulsson J, Ostman A. The effects of tumor-derived platelet-derived growth factor on vascular morphology and function in vivo revealed by susceptibility MRI. Int J Cancer 2008; 122(7):1548-56
69. Hasumi Y, Klosowska-Wardega A, Furuhashi M, et al. Identification of a subset of pericytes that respond to combination therapy targeting PDGF and VEGF signaling. Int J Cancer 2007; 121(12):2606-14
70. Willenberg A, Saalbach A, Simon JC, Anderegg U. Melanoma cells control HA synthesis in peritumoral fibroblasts via PDGF-AA and PDGF-CC: impact on melanoma cell proliferation. J Invest Dermatol 2012;132(2):385-93
71. Hansen TM, Singh H, Tahir TA, Brindle NP. Effects of angiopoietins-1 and-2 on the receptor tyrosine kinase Tie2 are differentially regulated at the endothelial cell surface. Cell Signal 2010;22(3):527-32
72. Seftor EA, Meltzer PS, Kirschmann DA, et al. The epigenetic reprogramming of poorly aggressive melanoma cells by a metastatic microenvironment. J Cell Mol Med 2006;10(1):174-96
73. Hendrix MJ, Seftor EA, Hess AR, Seftor RE. Vasculogenic mimicry and tumour-cell plasticity: lessons from melanoma. Nat Rev Cancer 2003;3(6): 411-21
74. Cai J, Kehoe O, Smith GM, et al. The angiopoietin/Tie-2 system regulates pericyte survival and recruitment in diabetic retinopathy. Invest Ophthalmol Vis Sci 2008;49(5):2163-71
75. Helfrich I, Edler L, Sucker A, et al. Angiopoietin-2 levels are associated with disease progression in metastatic malignant melanoma. Clin Cancer Res 2009;15(4): 1384-92
76. Gardizi M, Kurschat C, Riese A, et al. A decreased ratio between serum levels of the antagonistic angiopoietins 1 and 2 indicates tumour progression of malignant melanoma. Arch Dermatol Res 2012; 304(5):397-400
77. Derin D, Soydinc HO, Guney N, et al. Serum IL-8 and IL-12 levels in breast cancer. Med Oncol 2007;24(2):163-8
78. Akiba J, Yano H, Ogasawara S, et al. Expression and function of interleukin-8 in human hepatocellular carcinoma. Int J Oncol 2001;18(2):257-64
79. Xu L, Fidler IJ. Interleukin 8: an autocrine growth factor for human ovarian cancer. Oncol Res 2000;12(2):97-106
80. Matsuo Y, Ochi N, Sawai H, et al. CXCL8/IL-8 and CXCL12/SDF-1alpha co-operatively promote invasiveness and angiogenesis in pancreatic cancer. Int J Cancer 2009;124(4):853-61
81. Mattei S, Colombo MP, Melani C, et al. Expression of cytokine/growth factors and their receptors in human melanoma and melanocytes. Int J Cancer 1994;56(6):853-7
82. Bennicelli JL, Guerry D 4th. Production of multiple cytokines by cultured human melanomas. Exp Dermatol 1993;2(4): 186-90
83. Liu G, Zhang F, Lee J, Dong Z. Selective induction of interleukin-8 expression in metastatic melanoma cells by transforming growth factor-beta Cytokine 2005;31(3): 241-9
84. Wang JM, Taraboletti G, Matsushima K, et al. Induction of haptotactic migration of melanoma cells by neutrophil activating protein/interleukin-8. Biochem Biophys Res Commun 1990;169(1):165-70
85. Bar-Eli M. Role of interleukin-8 in tumor growth and metastasis of human melanoma. Pathobiology 1999;67(1):12-18
86. Singh S, Nannuru KC, Sadanandam A, et al. CXCR1 and CXCR2 enhances human melanoma tumourigenesis, growth and invasion. Br J Cancer 2009;100(10): 1638-46
87. Gabellini C, Trisciuoglio D, Desideri M, et al. Functional activity of CXCL8 receptors, CXCR1 and CXCR2, on human malignant melanoma progression. Eur J Cancer 2009;45(14):2618-27
88. Varney ML, Johansson SL, Singh RK. Distinct expression of CXCL8 and its receptors CXCR1 and CXCR2 and their association with vessel density and aggressiveness in malignant melanoma. Am J Clin Pathol 2006;125(2):209-16
89. Huang S, Mills L, Mian B, et al. Fully humanized neutralizing antibodies to interleukin-8 (ABX-IL8) inhibit angiogenesis, tumor growth, and metastasis of human melanoma. Am J Pathol 2002; 161(1):125-34
90. Scheibenbogen C, Mohler T, Haefele J, et al. Serum interleukin-8 (IL-8) is elevated in patients with metastatic melanoma and correlates with tumour load. Melanoma Res 1995;5(3):179-81
91. Crawford S, Belajic D, Wei J, et al. A novel B-RAF inhibitor blocks interleukin-8 (IL-8) synthesis in human melanoma xenografts, revealing IL-8 as a potential pharmacodynamic biomarker. Mol Cancer Ther 2008;7(3):492-9
92. Brennecke S, Deichmann M, Naeher H, Kurzen H. Decline in angiogenic factors, such as interleukin-8, indicates response to chemotherapy of metastatic melanoma. Melanoma Res 2005;15(6):515-22
93. Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci 2010;123(Pt 24):4195-200
94. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002;2(3): 161-74
95. Hofmann UB, Westphal JR, Van Muijen GN, Ruiter DJ. Matrix metalloproteinases in human melanoma. J Invest Dermatol 2000;115(3):337-44
96. Riker AI, Enkemann SA, Fodstad O, et al. The gene expression profiles of primary and metastatic melanoma yields a transition point of tumor progression and metastasis. BMC Med Genomics 2008;1:13
97. Hofmann UB, Westphal JR, Zendman AJ, et al. Expression and activation of matrix metalloproteinase-2 (MMP-2) and its co-localization with membrane-type 1 matrix metalloproteinase (MT1-MMP) correlate with melanoma progression. J Pathol 2000;191(3):245-56
98. Schnaeker EM, Ossig R, Ludwig T, et al. Microtubule-dependent matrix metalloproteinase-2/matrix metalloproteinase-9 exocytosis: prerequisite in human melanoma cell invasion. Cancer Res 2004;64(24):8924-31
99. Tatti O, Arjama M, Ranki A, et al. Membrane-type-3 matrix metalloproteinase (MT3-MMP) functions as a matrix composition-dependent effector of melanoma cell invasion. PLoS One 2011; 6(12):e28325
100. Ohnishi Y, Tajima S, Ishibashi A. Coordinate expression of membrane type-matrix metalloproteinases-2 and 3 (MT2-MMP and MT3-MMP) and matrix metalloproteinase-2 (MMP-2) in primary and metastatic melanoma cells. Eur J Dermatol 2001;11(5):420-3
101. Kuphal S, Bauer R, Bosserhoff AK. Integrin signaling in malignant melanoma. Cancer Metastasis Rev 2005;24(2):195-222
102. Stupack DG, Cheresh DA. Integrins and angiogenesis. Curr Top Dev Biol 2004;64: 207-38
103. Seftor RE. Role of the beta3 integrin subunit in human primary melanoma progression: multifunctional activities associated with alpha(v)beta3 integrin expression. Am J Pathol 1998;153(5): 1347-51
104. Felding-Habermann B, Mueller BM, Romerdahl CA, Cheresh DA. Involvement of integrin alpha V gene expression in human melanoma tumorigenicity. J Clin Invest 1992;89(6):2018-22
105. Geissinger E, Weisser C, Fischer P, et al. Autocrine stimulation by osteopontin contributes to antiapoptotic signalling of melanocytes in dermal collagen. Cancer Res 2002;62(16):4820-8
106. Reiniger IW, Wolf A, Welge-Lussen U, et al. Osteopontin as a serologic marker for metastatic uveal melanoma: results of a pilot study. Am J Ophthalmol 2007;143(4): 705-7
107. Filia A, Elliott F, Wind T, et al. Plasma osteopontin concentrations in patients with cutaneous melanoma. Oncol Rep 2013; 30(4):1575-80
108. Bosserhoff AK. Novel biomarkers in malignant melanoma. Clin Chim Acta 2006;367(1-2):28-35
109. Seftor RE, Seftor EA, Stetler-Stevenson WG, Hendrix MJ. The 72 kDa type IV collagenase is modulated via differential expression of alpha v beta 3 and alpha 5 beta 1 integrins during human melanoma cell invasion. Cancer Res 1993;53(14): 3411-15
110. Kim S, Bell K, Mousa SA, Varner JA. Regulation of angiogenesis in vivo by ligation of integrin alpha5beta1 with the central cell-binding domain of fibronectin. Am J Pathol 2000;156(4):1345-62
111. Boudreau NJ, Varner JA. The homeobox transcription factor Hox D3 promotes integrin alpha5beta1 expression and function during angiogenesis. J Biol Chem 2004;279(6):4862-8
112. Sil H, Sen T, Chatterjee A. Fibronectinintegrin (alpha5beta1) modulates migration and invasion of murine melanoma cell line B16F10 by involving MMP-9. Oncol Res 2011;19(7):335-48
113. Pisano M, DE Paola I, Nieddu V, et al. In vitro activity of the alphavbeta3 integrin antagonist RGDechi-hCit on malignant melanoma cells. Anticancer Res 2013;33(3): 871-9
114. Weis SM, Cheresh DA. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat Med 2011;17(11):1359-70
115. Serini G, Valdembri D, Bussolino F. Integrins and angiogenesis: a sticky business. Exp Cell Res 2006;312(5):651-8
116. Chung J, Mercurio AM. Contributions of the alpha6 integrins to breast carcinoma survival and progression. Mol Cells 2004; 17(2):203-9
117. Mercurio AM, Rabinovitz I, Shaw LM. The alpha 6 beta 4 integrin and epithelial cell migration. Curr Opin Cell Biol 2001;13(5): 541-5
118. Dajee M, Lazarov M, Zhang JY, et al. NF-kappaB blockade and oncogenic Ras trigger invasive human epidermal neoplasia. Nature 2003;421(6923):639-43
119. Nikolopoulos SN, Blaikie P, Yoshioka T, et al. Integrin beta4 signaling promotes tumor angiogenesis. Cancer Cell 2004;6(5): 471-83
120. Germain M, De Arcangelis A, Robinson SD, et al. Genetic ablation of the alpha 6-integrin subunit in Tie1Cre mice enhances tumour angiogenesis. J Pathol 2010;220(3):370-81
121. Nyberg P, Xie L, Kalluri R. Endogenous inhibitors of angiogenesis. Cancer Res 2005; 65(10):3967-79
122. Reijneveld JC, Taphoorn MJ, Kerckhaert OA, et al. Angiostatin prolongs the survival of mice with leptomeningeal metastases. Eur J Clin Invest 2003;33(1): 76-81
123. Yang H, Xu Z, Iuvone PM, Grossniklaus HE. Angiostatin decreases cell migration and vascular endothelium growth factor (VEGF) to pigment epithelium derived factor (PEDF) RNA ratio in vitro and in a murine ocular melanoma model. Mol Vis 2006;12:511-17
124. Yang H, Akor C, Dithmar S, Grossniklaus HE. Low dose adjuvant angiostatin decreases hepatic micrometastasis in murine ocular melanoma model. Mol Vis 2004;10:987-95
125. Kim KS, Kim DS, Chung KH, Park YS. Inhibition of angiogenesis and tumor progression by hydrodynamic cotransfection of angiostatin K1-3, endostatin, and saxatilin genes. Cancer Gene Ther 2006; 13(6):563-71
126. Rodolfo M, Cato EM, Soldati S, et al. Growth of human melanoma xenografts is suppressed by systemic angiostatin gene therapy. Cancer Gene Ther 2001;8(7):491-6
127. Chan RC, Gutierrez B, Ichim TE, Lin F. Enhancement of DNA cancer vaccine efficacy by combination with anti-angiogenesis in regression of established subcutaneous B16 melanoma. Oncol Rep 2009;22(5):1197-203
128. Yang H, Grossniklaus HE. Combined immunologic and anti-angiogenic therapy reduces hepatic micrometastases in a murine ocular melanoma model. Curr Eye Res 2006;31(6):557-62
129. Wahl ML, Kenan DJ, Gonzalez-Gronow M, Pizzo SV. Angiostatin's molecular mechanism: aspects of specificity and regulation elucidated. J Cell Biochem 2005; 96(2):242-61
130. de Groot-Besseling RR, Ruers TJ, van Kraats AA, et al. Anti-tumor activity of a combination of plasminogen activator and captopril in a human melanoma xenograft model. Int J Cancer 2004;112(2):329-34
131. de Groot-Besseling RR, Ruers TJ, Lamers-Elemans IL, et al. Angiostatin generating capacity and anti-tumour effects of D-penicillamine and plasminogen activators. BMC Cancer 2006;6:149
132. Soff GA, Wang H, Cundiff DL, et al. In vivo generation of angiostatin isoforms by administration of a plasminogen activator and a free sulfhydryl donor: a phase I study of an angiostatic cocktail of tissue plasminogen activator and mesna. Clin Cancer Res 2005;11(17):6218-25
133. Lawler J, Miao WM, Duquette M, et al. Thrombospondin-1 gene expression affects survival and tumor spectrum of p53-deficient mice. Am J Pathol 2001; 159(5):1949-56
134. Lee YJ, Koch M, Karl D, et al. Variable inhibition of thrombospondin 1 against liver and lung metastases through differential activation of metalloproteinase ADAMTS1. Cancer Res 2010;70(3):948-56
135. Ribatti D. Endogenous inhibitors of angiogenesis: a historical review. Leuk Res 2009;33(5):638-44
136. Rofstad EK, Graff BA. Thrombospondin-1-mediated metastasis suppression by the primary tumor in human melanoma xenografts. J Invest Dermatol 2001;117(5):1042-9
137. Wang S, Neekhra A, Albert DM, et al. Suppression of thrombospondin-1 expression during uveal melanoma progression and its potential therapeutic utility. Arch Ophthalmol 2012;130(3): 336-41
138. Rofstad EK, Galappathi K, Mathiesen B. Thrombospondin-1 treatment prevents growth of dormant lung micrometastases after surgical resection and curative radiation therapy of the primary tumor in human melanoma xenografts. Int J Radiat Oncol Biol Phys 2004;58(2):493-9
139. Morandi V. The N-terminal domain of thrombospondin-1: a key for the dual effect of TSP-1 in angiogenesis and cancer progression ScientificWorldJournal 2009;9: 133-6
140. Poon RT, Chung KK, Cheung ST, et al. Clinical significance of thrombospondin 1 expression in hepatocellular carcinoma. Clin Cancer Res 2004;10(12 Pt 1):4150-7
141. Byrne GJ, Hayden KE, McDowell G, et al. Angiogenic characteristics of circulating and tumoural thrombospondin-1 in breast cancer. Int J Oncol 2007;31(5):1127-32
142. Straume O, Akslen LA. Increased expression of VEGF-receptors (FLT-1, KDR, NRP-1) and thrombospondin-1 is associated with glomeruloid microvascular proliferation, an aggressive angiogenic phenotype, in malignant melanoma. Angiogenesis 2003; 6(4):295-301
143. Markovic SN, Suman VJ, Rao RA, et al. A phase II study of ABT-510 (thrombospondin-1 analog) for the treatment of metastatic melanoma. Am J Clin Oncol 2007;30(3):303-9
144. O'Reilly MS, Boehm T, Shing Y, et al. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 1997; 88(2):277-85
145. Dhanabal M, Ramchandran R, Waterman MJ, et al. Endostatin induces endothelial cell apoptosis. J Biol Chem 1999;274(17):11721-6
146. Dixelius J, Cross M, Matsumoto T, et al. Endostatin regulates endothelial cell adhesion and cytoskeletal organization. Cancer Res 2002;62(7):1944-7
147. Kim YM, Jang JW, Lee OH, et al. Endostatin inhibits endothelial and tumor cellular invasion by blocking the activation and catalytic activity of matrix metalloproteinase. Cancer Res 2000;60(19): 5410-13
148. Kim YM, Hwang S, Kim YM, et al. Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J Biol Chem 2002;277(31):27872-9
149. van der Schaft DW, Seftor RE, Seftor EA, et al. Effects of angiogenesis inhibitors on vascular network formation by human endothelial and melanoma cells. J Natl Cancer Inst 2004;96(19):1473-7
150. Feldman AL, Tamarkin L, Paciotti GF, et al. Serum endostatin levels are elevated and correlate with serum vascular endothelial growth factor levels in patients with stage IV clear cell renal cancer. Clin Cancer Res 2000;6(12):4628-34
151. Suzuki M, Iizasa T, Ko E, et al. Serum endostatin correlates with progression and prognosis of non-small cell lung cancer. Lung Cancer 2002;35(1):29-34
152. Kurschat P, Eming S, Nashan D, et al. Early increase in serum levels of the angiogenesis-inhibitor endostatin and of basic fibroblast growth factor in melanoma patients during disease progression. Br J Dermatol 2007;156(4):653-8
153. Berger AC, Alexander HR, Tang G, et al. Endothelial monocyte activating polypeptide II induces endothelial cell apoptosis and may inhibit tumor angiogenesis. Microvasc Res 2000;60(1):70-80
154. Airoldi I, Di Carlo E, Cocco C, et al. Endogenous IL-12 triggers an antiangiogenic program in melanoma cells. Proc Natl Acad Sci USA 2007;104(10): 3996-4001
155. Folberg R, Maniotis AJ. Vasculogenic mimicry. APMIS 2004;112(7-8):508-25
156. Shirakawa K, Kobayashi H, Heike Y, et al. Hemodynamics in vasculogenic mimicry and angiogenesis of inflammatory breast cancer xenograft. Cancer Res 2002;62(2): 560-6
157. Sharma N, Seftor RE, Seftor EA, et al. Prostatic tumor cell plasticity involves cooperative interactions of distinct phenotypic subpopulations: role in vasculogenic mimicry. Prostate 2002;50(3): 189-201
158. Sood AK, Fletcher MS, Coffin JE, et al. Functional role of matrix metalloproteinases in ovarian tumor cell plasticity. Am J Obstet Gynecol 2004;190(4):899-909
159. Chen Y, Jing Z, Luo C, et al. Vasculogenic mimicry-potential target for glioblastoma therapy: an in vitro and in vivo study. Med Oncol 2012;29(1):324-31
160. Wang SY, Ke YQ, Lu GH, et al. Vasculogenic mimicry is a prognostic factor for postoperative survival in patients with glioblastoma. J Neurooncol 2013;112(3): 339-45
161. Liu Z, Li Y, Zhao W, et al. Demonstration of vasculogenic mimicry in astrocytomas and effects of Endostar on U251 cells. Pathol Res Pract 2011;207(10):645-51
162. Passalidou E, Trivella M, Singh N, et al. Vascular phenotype in angiogenic and non-angiogenic lung non-small cell carcinomas. Br J Cancer 2002;86(2):244-9
163. Vartanian AA, Stepanova EV, Gutorov SL, et al. Prognostic significance of periodic acid-Schiff-positive patterns in clear cell renal cell carcinoma. Can J Urol 2009; 16(4):4726-32
164. Sun B, Zhang S, Zhao X, et al. Vasculogenic mimicry is associated with poor survival in patients with mesothelial sarcomas and alveolar rhabdomyosarcomas. Int J Oncol 2004;25(6):1609-14
165. McDonald DM, Munn L, Jain RK. Vasculogenic mimicry: how convincing, how novel, and how significant Am J Pathol 2000;156(2):383-8
166. Seftor RE, Hess AR, Seftor EA, et al. Tumor cell vasculogenic mimicry: from controversy to therapeutic promise. Am J Pathol 2012;181(4):1115-25
167. Paulis YW, Soetekouw PM, Verheul HM, et al. Signalling pathways in vasculogenic mimicry. Biochim Biophys Acta 2010; 1806(1):18-28
168. Kirschmann DA, Seftor EA, Hardy KM, et al. Molecular pathways: vasculogenic mimicry in tumor cells: diagnostic and therapeutic implications. Clin Cancer Res 2012;18(10):2726-32
169. Folberg R, Rummelt V, Parys-Van Ginderdeuren R, et al. The prognostic value of tumor blood vessel morphology in primary uveal melanoma. Ophthalmology 1993;100(9):1389-98
170. Clarijs R, Otte-Holler I, Ruiter DJ, de Waal RM. Presence of a fluid-conducting meshwork in xenografted cutaneous and primary human uveal melanoma. Invest Ophthalmol Vis Sci 2002;43(4):912-18
171. Kobayashi H, Shirakawa K, Kawamoto S, et al. Rapid accumulation and internalization of radiolabeled herceptin in an inflammatory breast cancer xenograft with vasculogenic mimicry predicted by the contrast-enhanced dynamic MRI with the macromolecular contrast agent G6-(1B4MGd)( 256). Cancer Res 2002;62(3):860-6
172. Maniotis AJ, Chen X, Garcia C, et al. Control of melanoma morphogenesis, endothelial survival, and perfusion by extracellular matrix. Lab Invest 2002;82(8): 1031-43
173. Bittner M, Meltzer P, Chen Y, et al. Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature 2000;406(6795):536-40
174. Demou ZN, Hendrix MJ. Microgenomics profile the endogenous angiogenic phenotype in subpopulations of aggressive melanoma. J Cell Biochem 2008;105(2): 562-73
175. Mihic-Probst D, Ikenberg K, Tinguely M, et al. Tumor cell plasticity and angiogenesis in human melanomas. PLoS One 2012; 7(3):e33571
176. Comito G, Calvani M, Giannoni E, et al. HIF-1alpha stabilization by mitochondrial ROS promotes Met-dependent invasive growth and vasculogenic mimicry in melanoma cells. Free Radic Biol Med 2011; 51(4):893-904
177. Seftor RE, Seftor EA, Koshikawa N, et al. Cooperative interactions of laminin 5 gamma2 chain, matrix metalloproteinase-2, and membrane type-1-matrix/metalloproteinase are required for mimicry of embryonic vasculogenesis by aggressive melanoma. Cancer Res 2001;61(17):6322-7
178. Seftor RE, Seftor EA, Kirschmann DA, Hendrix MJ. Targeting the tumor microenvironment with chemically modified tetracyclines: inhibition of laminin 5 gamma2 chain promigratory fragments and vasculogenic mimicry. Mol Cancer Ther 2002;1(13):1173-9
179. Casal C, Torres-Collado AX, Plaza-Calonge Mdel C, et al. ADAMTS1 contributes to the acquisition of an endothelial-like phenotype in plastic tumor cells. Cancer Res 2010;70(11):4676-86
180. Hendrix MJ, Seftor EA, Meltzer PS, et al. Expression and functional significance of VE-cadherin in aggressive human melanoma cells: role in
181. Hess AR, Seftor EA, Gruman LM, et al. VE-cadherin regulates EphA2 in aggressive melanoma cells through a novel signaling pathway: implications for vasculogenic mimicry. Cancer Biol Ther 2006;5(2): 228-33
182. Hess AR, Hendrix MJ. Focal adhesion kinase signaling and the aggressive melanoma phenotype. Cell Cycle 2006;5(5): 478-80
183. Hess AR, Seftor EA, Seftor RE, Hendrix MJ. Phosphoinositide 3-kinase regulates membrane Type 1-matrix metalloproteinase (MMP) and MMP-2 activity during melanoma cell vasculogenic mimicry. Cancer Res 2003;63(16):4757-62
184. Vartanian A, Stepanova E, Grigorieva I, et al. VEGFR1 and PKCalpha signaling control melanoma vasculogenic mimicry in a VEGFR2 kinase-independent manner. Melanoma Res 2011;21(2):91-8
185. Cai J, Ahmad S, Jiang WG, et al. Activation of vascular endothelial growth factor receptor-1 sustains angiogenesis and Bcl-2 expression via the phosphatidylinositol 3-kinase pathway in endothelial cells. Diabetes 2003;52(12):2959-68
186. Taylor AP, Leon E, Goldenberg DM. Placental growth factor (PlGF) enhances breast cancer cell motility by mobilising ERK1/2 phosphorylation and cytoskeletal rearrangement. Br J Cancer 2010;103(1): 82-9
187. Lesslie DP, Summy JM, Parikh NU, et al. Vascular endothelial growth factor receptor-1 mediates migration of human colorectal carcinoma cells by activation of Src family kinases. Br J Cancer 2006; 94(11):1710-17
188. Spinella F, Caprara V, Di Castro V, et al. Endothelin-1 induces the transactivation of vascular endothelial growth factor receptor-3 and modulates cell migration and vasculogenic mimicry in melanoma cells. J Mol Med (Berl) 2013;91(3):395-405
189. Dumaz N, Marais R. Integrating signals between cAMP and the RAS/RAF/MEK/ERK signalling pathways. Based on the anniversary prize of the Gesellschaft fur Biochemie und Molekularbiologie Lecture delivered on 5 July 2003 at the Special FEBS Meeting in Brussels. FEBS J 2005; 272(14):3491-504
190. Roscioni SS, Elzinga CR, Schmidt M. Epac: effectors and biological functions. Naunyn Schmiedebergs Arch Pharmacol 2008; 377(4-6):345-57
191. Lissitzky JC, Parriaux D, Ristorcelli E, et al. Cyclic AMP signaling as a mediator of vasculogenic mimicry in aggressive human melanoma cells in vitro. Cancer Res 2009; 69(3):802-9
192. Strizzi L, Hardy KM, Seftor EA, et al. Development and cancer: at the crossroads of Nodal and Notch signaling. Cancer Res 2009;69(18):7131-4
193. McAllister JC, Zhan Q, Weishaupt C, et al. The embryonic morphogen, Nodal, is associated with channel-like structures in human malignant melanoma xenografts. J Cutan Pathol 2010;37(Suppl 1):19-25
194. Topczewska JM, Postovit LM, Margaryan NV, et al. Embryonic and tumorigenic pathways converge via Nodal signaling: role in melanoma aggressiveness. Nat Med 2006;12(8):925-32
195. Strizzi L, Postovit LM, Margaryan NV, et al. Nodal as a biomarker for melanoma progression and a new therapeutic target for clinical intervention. Expert Rev Dermatol 2009;4(1):67-78
196. Krebs LT, Iwai N, Nonaka S, et al. Notch signaling regulates left-right asymmetry determination by inducing Nodal expression. Genes Dev 2003;17(10):1207-12
197. Hardy KM, Kirschmann DA, Seftor EA, et al. Regulation of the embryonic morphogen Nodal by Notch4 facilitates manifestation of the aggressive melanoma phenotype. Cancer Res 2010;70(24): 10340-50
198. Vartanian A, Gatsina G, Grigorieva I, et al. The involvement of Notch signaling in melanoma vasculogenic mimicry. Clin Exp Med 2013;13(3):201-9
199. Prieto VG, Mourad-Zeidan AA, Melnikova V, et al. Galectin-3 expression is associated with tumor progression and pattern of sun exposure in melanoma. Clin Cancer Res 2006;12(22):6709-15
200. Mourad-Zeidan AA, Melnikova VO, Wang H, et al. Expression profiling of Galectin-3-depleted melanoma cells reveals its major role in melanoma cell plasticity and vasculogenic mimicry. Am J Pathol 2008;173(6):1839-52
201. Fallowfield ME, Cook MG. Vascular invasion in malignant melanomas. An independent prognostic variable Am J Surg Pathol 1989;13(3):217-20
202. McGovern VJ, Mihm MC Jr., Bailly C, et al. The classification of malignant melanoma and its histologic reporting. Cancer 1973;32(6):1446-57
203. Lugassy C, Barnhill RL. Angiotropic melanoma and extravascular migratory metastasis: a review. Adv Anat Pathol 2007; 14(3):195-201
204. Laser J, Cangiarella J, Singh B, et al. Invasive lobular carcinoma of the breast: role of endothelial lymphatic marker D2-40. Ann Clin Lab Sci 2008;38(2):99-104
205. Inoue M, Takakuwa T, Minami M, et al. Clinicopathologic factors influencing postoperative prognosis in patients with small-sized adenocarcinoma of the lung. J Thorac Cardiovasc Surg 2008;135(4): 830-6
206. Mori D, Yamasaki F, Shibaki M, Tokunaga O. Lateral peritumoral lymphatic vessel invasion can predict lymph node metastasis in esophageal squamous cell carcinoma. Mod Pathol 2007;20(6):694-700
207. Yonemura Y, Endou Y, Tabachi K, et al. Evaluation of lymphatic invasion in primary gastric cancer by a new monoclonal antibody, D2-40. Hum Pathol 2006;37(9): 1193-9
208. Walgenbach-Bruenagel G, Tolba RH, Varnai AD, et al. Detection of lymphatic invasion in early stage primary colorectal cancer with the monoclonal antibody D2-40. Eur Surg Res 2006;38(5):438-44
209. Horiguchi A, Ito K, Sumitomo M, et al. Intratumoral lymphatics and lymphatic invasion are associated with tumor aggressiveness and poor prognosis in renal cell carcinoma. Urology 2008;71(5):928-32
210. Toll A, Gimeno-Beltran J, Ferrandiz-Pulido C, et al. D2-40 immunohistochemical overexpression in cutaneous squamous cell carcinomas: a marker of metastatic risk. J Am Acad Dermatol 2012;67(6):1310-18
211. Sahni D, Robson A, Orchard G, et al. The use of LYVE-1 antibody for detecting lymphatic involvement in patients with malignant melanoma of known sentinel node status. J Clin Pathol 2005;58(7): 715-21
212. Niakosari F, Kahn HJ, McCready D, et al. Lymphatic invasion identified by monoclonal antibody D2-40, younger age, and ulceration: predictors of sentinel lymph node involvement in primary cutaneous melanoma. Arch Dermatol 2008;144(4): 462-7
213. Niakosari F, Kahn HJ, Marks A, From L. Detection of lymphatic invasion in primary melanoma with monoclonal antibody D2-40: a new selective immunohistochemical marker of lymphatic endothelium. Arch Dermatol 2005;141(4):440-4
214. Doeden K, Ma Z, Narasimhan B, et al. Lymphatic invasion in cutaneous melanoma is associated with sentinel lymph node metastasis. J Cutan Pathol 2009;36(7): 772-80
215. Petersson F, Diwan AH, Ivan D, et al. Immunohistochemical detection of lymphovascular invasion with D2-40 in melanoma correlates with sentinel lymph node status, metastasis and survival. J Cutan Pathol 2009;36(11):1157-63
216. Petitt M, Allison A, Shimoni T, et al. Lymphatic invasion detected by D2-40/S-100 dual immunohistochemistry does not predict sentinel lymph node status in melanoma. J Am Acad Dermatol 2009; 61(5):819-28
217. Xu X, Gimotty PA, Guerry D, et al. Lymphatic invasion revealed by multispectral imaging is common in primary melanomas and associates with prognosis. Hum Pathol 2008;39(6):901-9
218. Rose AE, Christos PJ, Lackaye D, et al. Clinical relevance of detection of lymphovascular invasion in primary melanoma using endothelial markers D2-40 and CD34. Am J Surg Pathol 2011; 35(10):1441-9
219. Li Y, Wang MN, Li H, et al. Active immunization against the vascular endothelial growth factor receptor flk1 inhibits tumor angiogenesis and metastasis. J Exp Med 2002;195(12): 1575-84
220. Oku T, Tjuvajev JG, Miyagawa T, et al. Tumor growth modulation by sense and antisense vascular endothelial growth factor gene expression: effects on angiogenesis, vascular permeability, blood volume, blood flow, fluorodeoxyglucose uptake, and proliferation of human melanoma intracerebral xenografts. Cancer Res 1998; 58(18):4185-92
221. Perez DG, Suman VJ, Fitch TR, et al. Phase 2 trial of carboplatin, weekly paclitaxel, and biweekly bevacizumab in patients with unresectable stage IV melanoma: a North Central Cancer Treatment Group study, N047A. Cancer 2009;115(1):119-27
222. Biswas S, Wrigley J, East C, et al. A randomised trial evaluating bevacizumab as adjuvant therapy following resection of AJCC stage IIB, IIC and III cutaneous melanoma: an update. Ecancermedicalscience 2008;2:108
223. Terheyden P, Hofmann MA, Weininger M, et al. Anti-vascular endothelial growth factor antibody bevacizumab in conjunction with chemotherapy in metastasising melanoma. J Cancer Res Clin Oncol 2007;133(11): 897-901
224. Varker KA, Biber JE, Kefauver C, et al. A randomized phase 2 trial of bevacizumab with or without daily low-dose interferon alfa-2b in metastatic malignant melanoma. Ann Surg Oncol 2007;14(8):2367-76
225. Vihinen PP, Hernberg M, Vuoristo MS, et al. A phase II trial of bevacizumab with dacarbazine and daily low-dose interferonalpha2a as first line treatment in metastatic melanoma. Melanoma Res 2010;20(4): 318-25
226. Kim KB, Sosman JA, Fruehauf JP, et al. BEAM: a randomized phase II study evaluating the activity of bevacizumab in combination with carboplatin plus paclitaxel in patients with previously untreated advanced melanoma. J Clin Oncol 2012; 30(1):34-41
227. Slingluff CL Jr., Petroni GR, Molhoek KR, et al. Clinical activity and safety of combination therapy with temsirolimus and bevacizumab for advanced melanoma: a Phase II Trial (CTEP 7190/Mel47). Clin Cancer Res 2013;19(13):3611-20
228. Kottschade LA, Suman VJ, Perez DG, et al. A randomized phase 2 study of temozolomide and bevacizumab or nab-paclitaxel, carboplatin, and bevacizumab in patients with unresectable stage IV melanoma: a North Central Cancer Treatment Group study, N0775. Cancer 2013;119(3):586-92
229. Spratlin JL, Cohen RB, Eadens M, et al. Phase I pharmacologic and biologic study of ramucirumab (IMC-1121B), a fully human immunoglobulin G1 monoclonal antibody targeting the vascular endothelial growth factor receptor-2. J Clin Oncol 2010;28(5): 780-7
230. Tarhini AA, Frankel P, Margolin KA, et al. Aflibercept (VEGF Trap) in inoperable stage III or stage iv melanoma of cutaneous or uveal origin. Clin Cancer Res 2011; 17(20):6574-81
231. Eisen T, Ahmad T, Flaherty KT, et al. Sorafenib in advanced melanoma: a Phase II randomised discontinuation trial analysis. Br J Cancer 2006;95(5):581-6
232. Hauschild A, Agarwala SS, Trefzer U, et al. Results of a phase III, randomized, placebo-controlled study of sorafenib in combination with carboplatin and paclitaxel as second-line treatment in patients with unresectable stage III or stage IV melanoma. J Clin Oncol 2009;27(17):2823-30
233. Amaravadi RK, Schuchter LM, McDermott DF, et al. Phase II Trial of Temozolomide and Sorafenib in Advanced Melanoma Patients with or without Brain Metastases. Clin Cancer Res 2009;15(24): 7711-18
234. Flaherty KT, Lee SJ, Zhao F, et al. Phase III trial of carboplatin and paclitaxel with or without sorafenib in metastatic melanoma. J Clin Oncol 2013;31(3):373-9
235. Fruehauf J, Lutzky J, McDermott D, et al. Multicenter, phase II study of axitinib, a selective second-generation inhibitor of vascular endothelial growth factor receptors 1, 2, and 3, in patients with metastatic melanoma. Clin Cancer Res 2011;17(23): 7462-9
236. Kim KB, Chesney J, Robinson D, et al. Phase I/II and pharmacodynamic study of dovitinib (TKI258), an inhibitor of fibroblast growth factor receptors and VEGF receptors, in patients with advanced melanoma. Clin Cancer Res 2011;17(23): 7451-61
237. Hersey P, Sosman J, O'Day S, et al. A randomized phase 2 study of etaracizumab, a monoclonal antibody against integrin alpha(v)beta(3), + or-dacarbazine in patients with stage IV metastatic melanoma. Cancer 2010;116(6): 1526-34
238. Schadendorf D, Algarra SM, Bastholt L, et al. Immunotherapy of distant metastatic disease. Ann Oncol 2009;20(Suppl 6): vi41-50
239. Zaki KA, Basu B, Corrie P. The role of angiogenesis inhibitors in the management of melanoma. Curr Top Med Chem 2012; 12(1):32-49
240. O'Day S, Pavlick A, Loquai C, et al. A randomised, phase II study of intetumumab, an anti-alphav-integrin mAb, alone and with dacarbazine in stage IV melanoma. Br J Cancer 2011;105(3): 346-52
241. Kim KB, Prieto V, Joseph RW, et al. A randomized phase II study of cilengitide (EMD 121974) in patients with metastatic melanoma. Melanoma Res 2012;22(4): 294-301
242. Kuwada SK. Drug evaluation: volociximab, an angiogenesis-inhibiting chimeric monoclonal antibody. Curr Opin Mol Ther 2007;9(1):92-8
243. Ozerdem U, Mach-Hofacre B, Varki N, et al. The effect of prinomastat (AG3340), a synthetic inhibitor of matrix metalloproteinases, on uveal melanoma rabbit model. Curr Eye Res 2002;24(2): 86-91
244. Chirivi RG, Garofalo A, Crimmin MJ, et al. Inhibition of the metastatic spread and growth of B16-BL6 murine melanoma by a synthetic matrix metalloproteinase inhibitor. Int J Cancer 1994;58(3):460-4
245. Quirt I, Bodurth A, Lohmann R, et al. Phase II study of marimastat (BB-2516) in malignant melanoma: a clinical and tumor biopsy study of the National Cancer Institute of Canada Clinical Trials Group. Invest New Drugs 2002;20(4):431-7
246. Pavlaki M, Zucker S. Matrix metalloproteinase inhibitors (MMPIs): the beginning of phase I or the termination of phase III clinical trials. Cancer Metastasis Rev 2003;22(2-3):177-203
247. Paez-Ribes M, Allen E, Hudock J, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009;15(3):220-31
248. Ebos JM, Lee CR, Cruz-Munoz W, et al. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009;15(3):232-9
249. Cong R, Sun Q, Yang L, et al. Effect of Genistein on vasculogenic mimicry formation by human uveal melanoma cells. J Exp Clin Cancer Res 2009;28:124
250. Chen LX, He YJ, Zhao SZ, et al. Inhibition of tumor growth and vasculogenic mimicry by curcumin through down-regulation of the EphA2/PI3K/MMP pathway in a murine choroidal melanoma model. Cancer Biol Ther 2011;11(2):229-35
251. Zhang S, Li M, Gu Y, et al. Thalidomide influences growth and vasculogenic mimicry channel formation in melanoma. J Exp Clin Cancer Res 2008;27:60
252. Su M, Feng YJ, Yao LQ, et al. Plasticity of ovarian cancer cell SKOV3ip and vasculogenic mimicry in vivo. Int J Gynecol Cancer 2008;18(3):476-86
253. Banerji S, Ni J, Wang SX, et al. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 1999;144(4):789-801
254. Schacht V, Dadras SS, Johnson LA, et al. Up-regulation of the lymphatic marker podoplanin, a mucin-type transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumors. Am J Pathol 2005;166(3):913-21
255. Wilting J, Papoutsi M, Christ B, et al. The transcription factor Prox1 is a marker for lymphatic endothelial cells in normal and diseased human tissues. FASEB J 2002; 16(10):1271-3
256. Folpe AL, Chand EM, Goldblum JR, Weiss SW. Expression of Fli-1, a nuclear transcription factor, distinguishes vascular neoplasms from potential mimics. Am J Surg Pathol 2001;25(8):1061-6
257. Hewett PW, Nishi K, Daft EL, Clifford Murray J. Selective expression of erg isoforms in human endothelial cells. Int J Biochem Cell Biol 2001;33(4):347-55
258. Torlakovic EE, Slipicevic A, Florenes VA, et al. Fli-1 expression in malignant melanoma. Histol Histopathol 2008;23(11): 1309-14
259. Podgrabinska S, Braun P, Velasco P, et al. Molecular characterization of lymphatic endothelial cells. Proc Natl Acad Sci USA 2002;99(25):16069-74
260. Yamamoto K, de Waard V, Fearns C, Loskutoff DJ. Tissue distribution and regulation of murine von Willebrand factor gene expression in vivo. Blood 1998;92(8): 2791-801
261. Pusztaszeri MP, Seelentag W, Bosman FT. Immunohistochemical expression of endothelial markers CD31, CD34, von Willebrand factor, and Fli-1 in normal human tissues. J Histochem Cytochem 2006;54(4):385-95