Cilengitide downmodulates invasiveness and vasculogenic mimicry of neuropilin 1 expressing melanoma cells through the inhibition of αvβ5 integrin

International Journal of Cancer

Volumn 136, Issue 6, 2015, Pages E545-E558

  Ruffini, Federica ^a   Graziani, Grazia ^b   Levati, Lauretta ^a   Tentori, Lucio ^b   D'Atri, Stefania ^a   Lacal, Pedro M ^a  

^a LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Cilengitide; Integrins; Melanoma; Neuropilin 1; Vasculogenic mimicry

Indexed keywords

ALPHAVBETA5 INTEGRIN; CILENGITIDE; COLLAGEN; GELATINASE B; NEUROPILIN 1; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2; VITRONECTIN; VITRONECTIN RECEPTOR;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL ADHESION; CELL INVASION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IN VITRO STUDY; MELANOMA CELL; PROTEIN EXPRESSION; PROTEIN SECRETION; VASCULOGENIC MIMICRY;

EID: 84944964277     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29252     Document Type: Article

References (50)

1. Ria R, Reale A, Castrovilli A, et al. Angiogenesis and progression in human melanoma. Dermatol Res Pract 2010;2010:185687. doi:10.1155/2010/185687.
2. Hofmann UB, Houben R, Bröcker E-B, et al. Role of matrix metalloproteinases in melanoma cell invasion. Biochimie 2005;87:307-14.
3. Kuphal S, Bauer R, Bosserhoff AK. Integrin signaling in malignant melanoma. Cancer Metastasis Rev 2005;24:195-222.
4. Seftor RE, Hess AR, Seftor EA, et al. Tumor cell vasculogenic mimicry: from controversy to therapeutic promise. Am J Pathol 2012;181:1115-25.
5. Guo W, Giancotti FG. Integrin signalling during tumour progression. Nature Rev 2004;5:816-26.
6. Harburger DS, Calderwood DA. Integrin signalling at a glance. J Cell Sci 2009;122:159-63.
7. Pinon P, Wehrle-Haller B. Integrins: versatile receptors controlling melanocyte adhesion, migration and proliferation. Pigment Cell Mel Res 2010;24:282-94.
8. Bosserhoff AK. Novel biomarkers in malignant melanoma. Clin Chim Acta 2006;367:28-35.
9. Mas-Moruno C, Rechenmacher F, Kessler H. Cilengitide: the first anti-angiogenic small molecule drug candidate design, synthesis and clinical evaluation. Anticancer Agents Med Chem 2010;10:753-68.
10. Reardon DA, Cheresh DA. A prototypic integrin inhibitor for the treatment of glioblastoma and other malignancies. Genes Cancer 2011;2:1159-65.
11. Reardon DA, Neyns B, Weller M, et al. Cilengitide: an RGD pentapeptide αvβ3 and αvβ5 integrin inhibitor in development for glioblastoma and other malignancies. Future Oncol 2011;7:339-54.
12. 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;22:294-301.
13. Tentori L, Dorio AS, Muzi A, et al. The integrin antagonist cilengitide increases the antitumor activity of temozolomide against malignant melanoma. Oncol Rep 2008;19:1039-43.
14. Lacal PM, Ruffini F, Pagani E, et al. An autocrine loop directed by the vascular endothelial growth factor promotes invasiveness of human melanoma cells. Int J Oncol 2005;27:1625-32.
15. Ruffini F, Tentori L, Dorio AS, et al. Platelet derived growth factor C and calpain-3 are modulators of human melanoma cell invasiveness. Oncol Rep 2013;30: 2887-96.
16. Ruffini F, D'Atri S, Lacal PM. Neuropilin-1 expression promotes invasiveness of melanoma cells through vascular endothelial growth factor receptor-2 dependent and independent mechanisms. Int J Oncol 2013;43:297-306.
17. Ellis LM. The role of neuropilins in cancer. Mol Cancer Ther 2006;5:1099-107.
18. Pellet-Many C, Frankel P, Jia H, et al. Neuropilins: structure, function and role in disease. Biochem J 2008;411:211-26.
19. Hansel DE, Wilentz RE, Yeo CJ, et al. Expression of neuropilin-1 in high-grade dysplasia, invasive cancer and metastases of the human gastrointestinal tract. Am J Surg Pathol 2004;28:347-56.
20. Latil A, Bieche I, Pesche S, et al. VEGF overexpression in clinically localized prostate tumors and neuropilin-1 overexpression in metastatic forms. Int J Cancer 2000;89:167-71.
21. Ruffini F, Failla CM, Orecchia A, et al. Expression of the soluble vascular endothelial growth factor receptor-1 in cutaneous melanoma: role in tumour progression. Br J Dermatol 2011;164:1061-70.
22. Lacal PM, Morea V, Ruffini F, et al. Inhibition of endothelial cell migration and angiogenesis by a vascular endothelial growth factor receptor-1 derived peptide. Eur. J. Cancer 2008;44:1914-21.
23. Lacal PM, Failla CM, Pagani E, et al. Human melanoma cells secrete and respond to placenta growth factor and vascular endothelial growth factor. J Invest Dermatol 2000;115:1000-7.
24. Tentori L, Lacal PM, Muzi A, et al. Poly(ADP-ribose) polymerase (PARP) inhibition or PARP-1 gene deletion reduces angiogenesis. Eur J Cancer 2007;43:2124-33.
25. Jin H, Varner J. Integrins: roles in cancer development and as treatment targets. Br J Cancer 2004;90:561-5.
26. Kirmse R, Otto H, Ludwig T. Interdependency of cell adhesion, force generation and extracellular proteolysis in matrix remodeling. J Cell Sci 2011;124:1857-66.
27. Vartanian A, Stepanova E, Grigorieva I, et al. Melanoma vasculogenic mimicry capillary-like structure formation depends on integrin and calcium signaling. Microcirculation 2011;18:390-9.
28. Oliveira-Ferrer L, Hauschild J, Fiedler W, et al. Cilengitide induces cellular detachment and apoptosis in endothelial and glioma cells mediated by inhibition of FAK/src/AKT pathway. J Exp Clin Cancer Res 2008;27:86. doi: 10.1186/1756-9966-27-86.
29. Cheng NC, van Zandwijk N, Reid G. Cilengitide inhibits attachment and invasion of malignant pleural mesothelioma cells through antagonism of integrins αvβ3 and αvβ5. PLoS One 2014;9:e90374.
30. Desch A, Strozyk EA, Bauer AT, et al. Highly invasive melanoma cells activate the vascular endothelium via an MMP-2/integrin αvβ5-induced secretion of VEGF-A. Am J Pathol 2012;181:693-705.
31. Lu H, Hu L, Yu L, et al. KLF8 and FAK cooperatively enrich the active MMP14 on the cell surface required for the metastatic progression of breast cancer. Oncogene 2014;33:2909-17.
32. Murga M, Fernandez-Capetillo O, Tosato G. Neuropilin-1 regulates attachment in human endothelial cells independently of vascular endothelial growth factor receptor-2. Blood 2005;105:1992-9.
33. Snuderl M1, Batista A, Kirkpatrick ND, et al. Targeting placental growth factor/neuropilin 1 pathway inhibits growth and spread of medulloblastoma. Cell 2013;152:1065-76.
34. Preissner KT, Seiffert D. Role of vitronectin and its receptors in haemostasis and vascular remodeling. Thromb Res 1998;89:1-21.
35. Smith HW, Marshall CJ. Regulation of cell signaling by uPAR. Nat Rev Mol Cell Biol 2010;11:23-36.
36. Wei Y, Eble JA, Wang Z, et al. Urokinase receptors promote beta1 integrin function through interactions with integrin alpha3beta1. Mol Biol Cell 2001;12:2975-86.
37. Borges E, Jan Y, Ruoslahti E. Platelet-derived growth factor receptor beta and vascular endothelial growth factor receptor 2 bind to the beta 3 integrin through its extracellular domain. J Biol Chem 2000;275:39867-73.
38. Somanath PR, Malinin NL, Byzova TV. Cooperation between integrin alphavbeta3 and VEGFR2 in angiogenesis. Angiogenesis 2009;12:177-85.
39. Robinson SD, Reynolds LE, Kostourou V, et al. αvβ3 integrin limits the contribution of neuropilin-1 to vascular endothelial growth factor-induced angiogenesis. J Biol Chem 2009;284:33966-81.
40. Misra RM, Bajaj MS, Kale VP. Vasculogenic mimicry of HT1080 tumour cells in vivo: critical role of HIF-1a-neuropilin-1 axis. PLoS One 2012;7:e50153. doi: 10.1371/journal.pone.0050153.
41. Vogetseder A, Thies S, Ingold B, et al. αv-Integrin isoform expression in primary human tumors and brain metastases. Int J Cancer 2013;133:2362-71.
42. Lewis JM, Cheresh DA, Schwartz MA. Protein kinase C regulates αvβ5-dependent cytoskeletal associations and focal adhesion kinase phosphorylation. J Cell Biol 1996;134:1323-32.
43. Ricono JM, Huang M, Barnes LA, et al. Specific cross-talk between epidermal growth factor receptor and integrin alphavbeta5 promotes carcinoma cell invasion and metastasis. Cancer Res 2009;69:1383-91.
44. Paulis YW, Soetekouw PM, Verheul HM, et al. Signalling pathways in vasculogenic mimicry. Biochim Biophys Acta 2010;1806:18-28.
45. Vartanian A, Stepanova E, Grigorieva I, et al. VEGFR1 and PKCα signaling control melanoma vasculogenic mimicry in a VEGFR2 kinase-independent manner. Melanoma Res 2011;21:91-8.
46. Sennino B, McDonald DM. Controlling escape from angiogenesis inhibitors. Nat Rev Cancer 2012;12:699-709.
47. Tentori L, Lacal PM, Graziani G. Challenging resistance mechanisms to therapies for metastatic melanoma. Trends Pharmacol Sci 2013;34:656-66.
48. Emmett MS, Dewing D, Pritchard-Jones RO. Angiogenesis and melanoma - from basic science to clinical trials. Am J Cancer Res 2011;1:852-68.
49. Rybak SM, Sanovich E, Hollingshead MG, et al. "Vasocrine" formation of tumor cell-lined vascular spaces: implications for rational design of antiangiogenic therapies. Cancer Res 2003;63:2812-9.
50. 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;96:1473-7.