Survivin enhances motility of melanoma cells by supporting Akt activation and α5 integrin upregulation

Cancer Research

Volumn 70, Issue 20, 2010, Pages 7927-7937

  McKenzie, Jodi A ^b,c   Liu, Tong ^c   Goodson, Agnessa G ^a   Grossman, Douglas ^a,b,c  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA5 INTEGRIN; FIBRONECTIN; FIBRONECTIN RECEPTOR; MATRIGEL; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; RECEPTOR ANTIBODY; SURVIVIN;

APOPTOSIS; ARTICLE; CANCER INVASION; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN TISSUE; MELANOMA; MELANOMA CELL; METASTASIS; PRIORITY JOURNAL; RNA INTERFERENCE; ULTRAVIOLET RADIATION; UPREGULATION;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; ENZYME ACTIVATION; FORESKIN; HUMANS; INTEGRIN ALPHA5BETA1; MALE; MELANOCYTES; MELANOMA; MICROTUBULE-ASSOCIATED PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM INVASIVENESS; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; UP-REGULATION;

EID: 78049267203     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-0194     Document Type: Article

References (55)

1. Vicente-Manzanares M, Choi CK, Horwitz AR. Integrins in cell migration-the actin connection. J Cell Sci 2009;122:199-206.
2. Condeelis J, Singer RH, Segall JE. The great escape: when cancer cells hijack the genes for chemotaxis and motility. Annu Rev Cell Dev Biol 2005;21:695-718. (Pubitemid 41740651)
3. Miller AJ, Mihm MC, Jr. Melanoma. N Engl J Med 2006;355:51-65.
4. Cohen C, Zavala-Pompa A, Sequeira JH, et al. Mitogen-actived protein kinase activation is an early event in melanoma progression. Clin Cancer Res 2002;8:3728-33. (Pubitemid 35424762)
5. Davies H, Bignell GR, Cox C, et al. Mutations of the BRAF gene in human cancer. Nature 2002;417:949-54. (Pubitemid 34716871)
6. Govindarajan B, Bai X, Cohen C, et al. Malignant transformation of melanocytes to melanoma by constitutive activation of mitogen-activated protein kinase kinase (MAPKK) signaling. J Biol Chem 2003;278:9790-5. (Pubitemid 36800479)
7. Robertson GP. Functional and therapeutic significance of Akt deregulation in malignant melanoma. Cancer Metastasis Rev 2005;24:273-85.
8. Neudauer CL, McCarthy JB. Insulin-like growth factor I-stimulated melanoma cell migration requires phosphoinositide 3-kinase but not extracellular-regulated kinase activation. Exp Cell Res 2003;286:128-37.
9. Shin DH, Kim OH, Jun HS, Kang MK. Inhibitory effect of capsaicin on B16-10 melanoma cell migration via the phosphatidylinositol 3-kinase/Akt/Rac1 signal pathway. Exp Mol Med 2008;40:486-94.
10. Horst B, Gruvberger-Saal SK, Hopkins BD, et al. Gab2-mediated signaling promotes melanoma metastasis. Am J Pathol 2009;174:1524-33.
11. Govindarajan B, Sligh JE, Vincent BJ, et al. Overexpression of Akt converts radial growth melanoma to vertical growth melanoma. J Clin Invest 2007;117:719-29. (Pubitemid 46348530)
12. Altieri DC. Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer 2008;8:61-70.
13. Vong QP, Cao K, Li HY, Iglesias PA, Zheng Y. Chromosome alignment and segregation regulated by ubiquitination of survivin. Science 2005;310:1499-504. (Pubitemid 41746347)
14. Liu T, Biddle D, Hanks AN, et al. Activation of dual apoptotic pathways in human melanocytes and protection by survivin. J Invest Dermatol 2006;126:2247-56. (Pubitemid 44413172)
15. Liu T, Brouha B, Grossman D. Rapid induction of mitochondrial events and caspase-independent apoptosis in Survivin-targeted melanoma cells. Oncogene 2004;23:39-48. (Pubitemid 38142238)
16. Yan H, Thomas J, Liu T, et al. Induction of melanoma cell apoptosis and inhibition of tumor growth using a cell-permeable Survivin antagonist. Oncogene 2006;25:6968-74. (Pubitemid 44684837)
17. Raj D, Liu T, Samadashwily G, Li F, Grossman D. Survivin repression by p53, Rb and E2F2 in normal human melanocytes. Carcinogenesis 2008;29:194-201.
18. Gradilone A, Gazzaniga P, Ribuffo D, et al. Survivin, bcl-2, bax, and bcl-X gene expression in sentinel lymph nodes from melanoma patients. J Clin Oncol 2003;21:306-12. (Pubitemid 46606160)
19. Takeuchi H, Morton DL, Elashoff D, Hoon DS. Survivin expression by metastatic melanoma predicts poor disease outcome in patients receiving adjuvant polyvalent vaccine. Int J Cancer 2005;117:1032-8. (Pubitemid 41688581)
20. Thomas J, Liu T, Cotter MA, et al. Melanocyte expression of survivin promotes development and metastasis of UV-induced melanoma in HGF-transgenic mice. Cancer Res 2007;67:5172-8. (Pubitemid 46997254)
21. Salz W, Eisenberg D, Plescia J, et al. A survivin gene signature predicts aggressive tumor behavior. Cancer Res 2005;65:3531-4. (Pubitemid 40616325)
22. Allen SM, Florell SR, Hanks AN, et al. Survivin expression in mouse skin prevents papilloma regression and promotes chemical-induced tumor progression. Cancer Res 2003;63:567-72.
23. Stupack DG, Cheresh DA. Get a ligand, get a life: integrins, signaling and cell survival. J Cell Sci 2002;115:3729-38.
24. Bowen AR, Hanks AN, Allen SM, Alexander A, Diedrich MJ, Grossman D. Apoptosis regulators and responses in human melanocytic and keratinocytic cells. J Invest Dermatol 2003;120:48-55. (Pubitemid 36120970)
25. Grossman D, McNiff JM, Li F, Altieri DC. Expression and targeting of the apoptosis inhibitor, survivin, in human melanoma. J Invest Dermatol 1999;113:1076-81. (Pubitemid 30013356)
26. Grossman D, Kim PJ, Schechner JS, Altieri DC. Inhibition of melanoma tumor growth in vivo by survivin targeting. Proc Natl Acad Sci U S A 2001;98:635-40. (Pubitemid 32105095)
27. Mesri M, Wall NR, Li J, Kim RW, Altieri DC. Cancer gene therapy using a survivin mutant adenovirus. J Clin Invest 2001;108:981-90. (Pubitemid 32946072)
28. Liu WS, Yan HJ, Qin RY, et al. siRNA directed against survivin enhances pancreatic cancer cell gemcitabine chemosensitivity. Dig Dis Sci 2009;54:89-96.
29. Zhen HN, Li LW, Zhang W, et al. Short hairpin RNA targeting survivin inhibits growth and angiogenesis of glioma U251 cells. Int J Oncol 2007;31:1111-7.
30. Pennati M, Colella G, Folini M, Citti L, Daidone MG, Zaffaroni N. Ribozyme-mediated attenuation of survivin expression sensitizes human melanoma cells to cisplatin-induced apoptosis. J Clin Invest 2002;109:285-6. (Pubitemid 34083749)
31. Tse JC,Kalluri R.Mechanismsofmetastasis: epithelial-to-mesenchymal transition and contribution of tumor microenvironment. J Cell Biochem 2007;101:816-29.
32. Meier F, Busch S, Lasithiotakis K, et al. Combined targeting of MAPK and AKT signalling pathways is a promising strategy for melanoma treatment. Br J Dermatol 2007;156:1204-13. (Pubitemid 47029801)
33. Ambrosini G, Adida C, Sirugo G, Altieri DC. Induction of apoptosis and inhibition of cell proliferation by survivin gene targeting. J Biol Chem 1998;273:11177-82. (Pubitemid 28204967)
34. Felding-Habermann B. Integrin adhesion receptors in tumor metastasis. Clin Exp Metastasis 2003;20:203-13. (Pubitemid 36513225)
35. Natali PG, Nicotra MR, Di Filippo F, Bigotti A. Expression of fibronectin, fibronectin isoforms and integrin receptors in melanocytic lesions. Br J Cancer 1995;71:1243-7.
36. Qian F, Zhang ZC, Wu XF, Li YP, Xu Q. Interaction between integrin α(5) and fibronectin is required for metastasis of B16F10 melanoma cells. Biochem Biophys Res Commun 2005;333:1269-75.
37. Seftor RE, Seftor EA, Gehlsen KR, et al. Role of the α v β 3 integrin in human melanoma cell invasion. Proc Natl Acad Sci U S A 1992;89:1557-61.
38. Bai J, Zhang J, Wu J, et al. JWA regulates melanoma metastasis by integrin α(V)β(3) signaling. Oncogene 2009;29:1227-37.
39. Danen EH, Ten Berge PJ, Van Muijen GN, Van 't Hof-Grootenboer AE, Brocker EB, Ruiter DJ. Emergence of α 5 β 1 fibronectin- and α v β 3 vitronectin-receptor expression in melanocytic tumour progression. Histopathology 1994;24:249-56.
40. Brooks PC, Stromblad S, Sanders LC, et al. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin α v β 3. Cell 1996;85:683-93.
41. Hofmann UB, Westphal JR, Waas ET, Becker JC, Ruiter DJ, van Muijen GN. Coexpression of integrin α(v)β3 and matrix metalloproteinase-2 (MMP-2) coincides with MMP-2 activation: correlation with melanoma progression. J Invest Dermatol 2000;115:625-32.
42. Hood JD, Cheresh DA. Role of integrins in cell invasion and migration. Nat Rev Cancer 2002;2:91-100. (Pubitemid 37328796)
43. Sieg DJ, Hauck CR, Schlaepfer DD. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J Cell Sci 1999;112:2677-91.
44. Klekotka PA, Santoro SA, Wang H, Zutter MM. Specific residues within the α 2 integrin subunit cytoplasmic domain regulate migration and cell cycle progression via distinct MAPK pathways. J Biol Chem 2001;276:32353-61.
45. Zheng DQ, Woodard AS, Tallini G, Languino LR. Substrate specificity of α(v)β(3) integrin-mediated cell migration and phosphatidylinositol 3-kinase/AKT pathway activation. J Biol Chem 2000;275:24565-74.
46. Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 2009;9:537-49.
47. Zhang B, Gu F, She C, et al. Reduction of Akt2 inhibits migration and invasion of glioma cells. Int J Cancer 2009;125:585-95.
48. Guha M, Plescia J, Leav I, Li J, Languino LR, Altieri DC. Endogenous tumor suppression mediated by PTEN involves survivin gene silencing. Cancer Res 2009;69:4954-8.
49. Li J, Ballif BA, Powelka AM, Dai J, Gygi SP, Hsu VW. Phosphorylation of ACAP1 by Akt regulates the stimulation-dependent recycling of integrin β1 to control cell migration. Dev Cell 2005;9:663-73. (Pubitemid 41555148)
50. Somanath PR, Kandel ES, Hay N, Byzova TV. Akt1 signaling regulates integrin activation, matrix recognition, and fibronectin assembly. J Biol Chem 2007;282:22964-76. (Pubitemid 47267339)
51. Corbi AL, Jensen UB, Watt FM. The α2 and α5 integrin genes: identification of transcription factors that regulate promoter activity in epidermal keratinocytes. FEBS Lett 2000;474:201-7.
52. Gingras ME, Masson-Gadais B, Zaniolo K, et al. Differential binding of the transcription factors Sp1, AP-1, and NFI to the promoter of the human α5 integrin gene dictates its transcriptional activity. Invest Ophthalmol Vis Sci 2009;50:57-67.
53. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70.
54. Fujita M, High WA, Asgari S, Lewis KD, Gonzalez R. Development of vitiligo during melanoma treatment with a novel survivin inhibitor: a case report and review of the literature. Int J Dermatol 2009;48:426-30.
55. Mehrotra S, Languino LR, Raskett CM, MercurioAM, Dohi T, Altieri DC. IAP regulation of metastasis. Cancer Cell 17:53-64.