Raf kinase inhibitor RKIP inhibits MDA-9/syntenin-mediated metastasis in melanoma

Cancer Research

Volumn 72, Issue 23, 2012, Pages 6217-6226

  Das, Swadesh K ^a,b   Bhutia, Sujit K ^a   Sokhi, Upneet K ^a   Azab, Belal ^a   Su, Zhao Zhong ^a   Boukerche, Habib ^c   Anwar, Talha ^d   Moen, Erika L ^d   Chatterjee, Devasis ^d   Pellecchia, Maurizio ^e   Sarkar, Devanand ^a,b   Fisher, Paul B ^a,b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c University Lyon 1   (France)

^d RHODE ISLAND HOSPITAL   (United States)

^e BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MELANOMA DIFFERENTIATION ASSOCIATED GENE 9 PROTEIN; MESSENGER RNA; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PROTEIN TYROSINE KINASE; SYNTENIN; UNCLASSIFIED DRUG;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER TISSUE; CARCINOGENESIS; CELL INVASION; CHICK EMBRYO; CHORIOALLANTOIS; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUNG METASTASIS; MELANOMA; MELANOMA CELL; MOLECULAR INTERACTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TISSUE MICROARRAY; TRANSCRIPTION REGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CHICK EMBRYO; DOWN-REGULATION; FOCAL ADHESION KINASE 1; HUMANS; IMMUNOHISTOCHEMISTRY; MELANOMA; NEOPLASM INVASIVENESS; NF-KAPPA B; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; RAF KINASES; RNA, MESSENGER; SIGNAL TRANSDUCTION; SYNTENINS;

EID: 84870380884     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-0402     Document Type: Article

References (50)

1. American Cancer Society. Cancer facts and figures 2011. Atlanta: American Cancer Society; 2011.p. 1-70.Available from: http://www.cancer.org.
2. Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, et al. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 2009;27:6199-206.
3. Welch DR, Rinker-Schaeffer CW. What defines a useful marker of metastasis in human cancer? J Natl Cancer Inst 1999;9:1351-3. (Pubitemid 29399993)
4. Sarkar D, Fisher PB. Metastasis-promoting genes. In: Welch DR, Lyden DC, Psaila C, editors. Cancer metastasis: biologic basis and therapeutics. New York: Cambridge University Press; 2011. p. 55-63.
5. Yeung K, Janosch P, McFerran B, Rose DW, Mischak H, Sedivy JM, et al. Mechanism of suppression of the Raf/MEK/extracellular signal-regulated kinase pathway by the raf kinase inhibitor protein. Mol Cell Biol 2000;20:3079-85. (Pubitemid 30215020)
6. Lin JJ, Jiang H, Fisher PB. Characterization of a novel melanoma differentiation-associated gene, mda-9, that is downregulated during terminal differentiation. Mol Cell Differ 1996;4:317-33. (Pubitemid 27111424)
7. Lin JJ, Jiang H, Fisher PB. Melanoma differentiation associated gene-9, mda-9, is a human gamma interferon responsive gene. Gene 1998;207:105-10. (Pubitemid 28085338)
8. Boukerche H, Su ZZ, Emdad L, Baril P, Balme B, Thomas L, et al. MDA-9/Syntenin: a positive regulator of melanoma metastasis. Cancer Res 2005;65:10901-11. (Pubitemid 41713358)
9. Helmke BM, Polychronidis M, Benner A, Thome M, Arribas J, Deichmann M. Melanoma metastasis is associated with enhanced expression of the syntenin gene. Oncol Rep 2004;12:221-8.
10. Sarkar D, Boukerche H, Su ZZ, Fisher PB. MDA-9/syntenin: more than just a simple adapter protein when it comes to cancer metastasis. Cancer Res 2008;68:3087-93.
11. Sarkar D, Boukerche H, Su ZZ, Fisher PB. MDA-9/syntenin: recent insights into a novel cell signaling and metastasis-associated gene. Pharmacol Ther 2004;104:101-15. (Pubitemid 39429466)
12. Boukerche H, Su ZZ, Emdad L, Sarkar D, Fisher PB. MDA-9/syntenin regulates the metastatic phenotype in human melanoma cells by activating nuclear factor-kappaB. Cancer Res 2007;67:1812-22. (Pubitemid 46383408)
13. Boukerche H, Su ZZ, Prevot C, Sarkar D, Fisher PB. MDA-9/Syntenin promotes metastasis in human melanoma cells by activating c-Src. Proc Natl Acad Sci U S A 2008;105:15914-9.
14. Boukerche H, Aissaoui H, Prevost C, Hirbec H, Das SK, Su ZZ, et al. Src kinase activation is mandatory for MDA-9/syntenin-mediated activation of nuclear factor-kappaB. Oncogene 2010;29:3054-66.
15. Koo TH, Lee JJ, Kim EM, Kim KW, Do Kim H, Lee JH. Syntenin is overexpressed and promotes cell migration in metastatic human breast and gastric cancer cell lines. Oncogene 2002;21:4080-8.
16. Weiss A, Baumgartner M, Radziwill G, Dennler J, Moelling K. c-Src is a PDZ interaction partner and substrate of the E3 ubiquitin ligase Ligand-of-Numb protein X1. FEBS Lett 2007;581:5131-6. (Pubitemid 47576099)
17. Baumgartner M, Weiss A, Fritzius T, Heinrich J, Moelling K. The PDZ protein MPP2 interacts with c-Src in epithelial cells. Exp Cell Res 2009;315:2888-98.
18. Baumgartner M, Radziwill G, Lorger M, Weiss A, Moelling K. c-Srcmediated epithelial cell migration and invasion regulated by PDZ binding site. Mol Cell Biol 2008;28:642-55.
19. Radziwill G, Weiss A, Heinrich J, Baumgartner M, Boisguerin P, Owada K, et al. Regulation of c-Src by binding to the PDZ domain of AF-6. EMBO J 2007;26:2633-44. (Pubitemid 46884275)
20. Yeung KC, Rose DW, Dhillon AS, Yaros D, Gustafsson M, Chatterjee D, et al. Raf kinase inhibitor protein interacts with NF-kappaB-inducing kinase and TAK1 and inhibits NF-kappaB activation. Mol Cell Biol 2001;21:7207-17. (Pubitemid 32953475)
21. Steeg PS, Bevilacqua G, Kopper L, Thorgeirsson UP, Talmadge JE, Liotta LA, et al. Evidence for a novel gene associated with low tumor metastatic potential. J Natl Cancer Inst 1988;80:200-4.
22. Dong JT, Lamb PW, Rinker-Schaeffer CW, Vukanovic J, Ichikawa T, Isaacs JT, et al. KAI1, a metastasis suppressor gene for prostate cancer on human chromosome 11p11.2. Science 1995;268:884-6.
23. Yang X, Welch DR, Phillips KK, Weissman BE, Wei LL. KAI1, a putative marker for metastatic potential in human breast cancer. Cancer Lett 1997;119:149-55. (Pubitemid 27478097)
24. Yeung K, Seitz T, Li S, Janosch P, McFerran B, Kaiser C, et al. Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature 1999;401:173-7. (Pubitemid 29436321)
25. Kroslak T, Koch T, Kahl E, Hollt V. Human phosphatidylethanolamine- binding protein facilitates heterotrimeric G protein-dependent signaling. J Biol Chem 2001;276:39772-8.
26. Klysik J, Theroux SJ, Sedivy JM, Moffit JS, Boekelheide K. Signaling crossroads: the function of Raf kinase inhibitory protein in cancer, the central nervous system and reproduction. Cell Signal 2008;20:1-9. (Pubitemid 350138364)
27. Fu Z, Smith PC, Zhang L, Rubin MA, Dunn RL, Yao Z, et al. Effects of raf kinase inhibitor protein expression on suppression of prostate cancer metastasis. J Natl Cancer Inst 2003;95:878-89. (Pubitemid 36833879)
28. Fu Z, Kitagawa Y, Shen R, Shah R, Mehra R, Rhodes D, et al. Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer. Prostate 2006;66:248-56. (Pubitemid 43191224)
29. Li HZ, Gao Y, Zhao XL, Liu YX, Sun BC, Yang J, et al. Effects of raf kinase inhibitor protein expression on metastasis and progression of human breast cancer. Mol Cancer Res 2009;7:832-40.
30. Li HZ, Wang Y, Gao Y, Shao J, Zhao XL, Deng WM, et al. Effects of raf kinase inhibitor protein expression on metastasis and progression of human epithelial ovarian cancer. Mol Cancer Res 2008;6:917-28.
31. Park S, Yeung ML, Beach S, Shields JM, Yeung KC. RKIP down-regulates B-Raf kinase activity in melanoma cancer cells. Oncogene. 2005;24:3535-40. (Pubitemid 40756254)
32. Schuierer MM, Bataille F, Hagan S, Kolch W, Bosserhoff AK. Reduction in Raf kinase inhibitor protein expression is associated with increased Ras-extracellular signal-regulated kinase signaling in melanoma cell lines. Cancer Res 2004;64:5186-92. (Pubitemid 39006537)
33. Jilaveanu LB, Zito CR, Aziz SA, Conrad PJ, Schmitz JC, Sznol M, et al. C-Raf is associated with disease progression and cell proliferation in a subset of melanomas. Clin Cancer Res 2009;15:5704-13.
34. Deryugina EI, Zijlstra A, Partridge JJ, Kupriyanova TA, Madsen MA, Papagiannakopoulos T, et al. Unexpected effect of matrix metalloproteinase down-regulation on vascular intravasation and metastasis of human fibrosarcoma cells selected in vivo for high rates of dissemination. Cancer Res 2005;65:10959-69. (Pubitemid 41713365)
35. Hung AY, Sheng M. PDZ domains: structural modules for protein complex assembly. J Biol Chem 2002;277:5699-702. (Pubitemid 34968344)
36. Dash R, Dmitriev I, Su ZZ, Bhutia SK, Azab B, Vozhilla N, et al. Enhanced delivery of MDA-7/IL-24 using a serotype chimeric adenovirus (Ad.5/3) improves therapeutic efficacy in low CAR prostate cancer cells. Cancer Gene Ther 2010;17:447-56.
37. Kim J, Yu W, Kovalski K, Ossowski L. Requirement for specific proteases in cancer cell intravasation as revealed by a novel semiquantitative PCR-based assay. Cell 1998;94:353-62. (Pubitemid 28376079)
38. Zijlstra A, Mellor R, Panzarella G, Aimes RT, Hooper JD, Marchenko ND, et al. A quantitative analysis of rate-limiting steps in the metastatic cascade using human-specific real-time polymerase chain reaction. Cancer Res 2002;62:7083-92. (Pubitemid 35424104)
39. Beach S, Tang H, Park S, Dhillon AS, Keller ET, Kolch W, et al. Snail is a repressor of RKIP transcription in metastatic prostate cancer cells. Oncogene 2008;27:2243-8. (Pubitemid 351483382)
40. Lin K, Baritaki S, Militello L, Malaponte G, Bevelacqua Y, Bonavida B. The role of B-RAF mutations in melanoma and the induction of EMT via dysregulation of the NF-kappaB/Snail/RKIP/PTEN circuit. Genes Cancer 2010;1:409-20.
41. Hwangbo C, Kim J, Lee JJ, Lee JH. Activation of the integrin effector kinase focal adhesion kinase in cancer cells is regulated by crosstalk between protein kinase C alpha and the PDZ adapter protein MDA-9/Syntenin. Cancer Res 2010;70:1645-55.
42. Chatterjee D, Bai Y, Wang Z, Beach S, Mott S, Roy R, et al. RKIP sensitizes prostate and breast cancer cells to drug-induced apoptosis. J Biol Chem 2004;279:17515-23. (Pubitemid 38560515)
43. Chimura T, Launey T, Ito M. Evolutionarily conserved bias of aminoacid usage refines the definition of PDZ-binding motif. BMC Genomics 2011;12:300-12.
44. Trejo J. Internal PDZ ligands: novel endocytic recycling motifs for G protein-coupled receptors. Mol Pharmacol 2005;67:1388-90. (Pubitemid 40594135)
45. Kudo-Saito C, Shirako H, Takeuchi T, Kawakami Y. Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell 2009;15:195-206.
46. Herzinger T, Wolf DA. Snail puts melanoma on the fast track. Pigment Cell Melanoma Res 2009;22:150-1.
47. Meerschaert K, Bruyneel E, De Wever O, Vanloo B, Boucherie C, Bracke M, et al. The tandem PDZ domains of syntenin promote cell invasion. Exp Cell Res. 2007;313:1790-804. (Pubitemid 46653876)
48. Wu K, Bonavida B. The activated NF-kappaB-Snail-RKIP circuitry in cancer regulates both the metastatic cascade and resistance to apoptosis by cytotoxic drugs. Crit Rev Immunol 2009;29:241-54.
49. Su ZZ, Sarkar D, Emdad L, Duigou GJ, Young CS, Ware J, et al. Targeting gene expression selectively in cancer cells by using the progression-elevated gene-3 promoter. Proc Natl Acad Sci U S A 2005;102:1059-64. (Pubitemid 40170725)
50. Su ZZ, Shi Y, Fisher PB. Subtraction hybridization identifies a transformation progression-associated gene PEG-3 with sequence homology to a growth arrest and DNA damage-inducible gene. Proc Natl Acad Sci U S A 1997;94:9125-30.