Reduction of RKIP expression promotes nasopharyngeal carcinoma invasion and metastasis by activating Stat3 signaling

Oncotarget

Volumn 6, Issue 18, 2015, Pages 16422-16436

  He, Qiu Yan ^a   Yi, Hong Mei ^a   Yi, Hong ^a   Xiao, Ta ^a   Qu, Jia Quan ^a   Yuan, Li ^a   Zhu, Jin Feng ^a   Li, Jiao Yang ^a   Wang, Yuan Yuan ^a   Li, Li Na ^a   Feng, Juan ^a   Lu, Shan Shan ^a   Xiao, Zhi Qiang ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Metastasis; Metastatic suppressor; Nasopharyngeal carcinoma; RKIP; Stat3

Indexed keywords

PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; STAT3 PROTEIN; PEBP1 PROTEIN, HUMAN; SMALL INTERFERING RNA; STAT3 PROTEIN, HUMAN;

ADULT; ARTICLE; CANCER CELL LINE; CANCER PROGNOSIS; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; METASTASIS; NASOPHARYNX CARCINOMA; OVERALL SURVIVAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR INVASION; ANIMAL; BIOSYNTHESIS; CANCER TRANSPLANTATION; CELL MOTION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; LYMPH NODE METASTASIS; METABOLISM; MIDDLE AGED; MORTALITY; MOUSE; NASOPHARYNX TUMOR; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; RNA INTERFERENCE; SECONDARY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; DOWN-REGULATION; ENZYME ACTIVATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; LUNG NEOPLASMS; LYMPHATIC METASTASIS; MALE; MICE; MICE, NUDE; MIDDLE AGED; NASOPHARYNGEAL NEOPLASMS; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; PHOSPHATIDYLETHANOLAMINE BINDING PROTEIN; PHOSPHORYLATION; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84937943759     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3847     Document Type: Article

References (41)

1. Lo KW, To KF, Huang DP. Focus on nasopharyngeal carcinoma. Cancer Cell. 2004; 5:423-428.
2. Chan AT. Current treatment of nasopharyngeal carcinoma. Eur J Cancer. 2011; 47:S302-S303.
3. Lee AW, Poon YF, Foo W, Law SC, Cheung FK, Chan DK, Tung SY, Thaw M, Ho JH. Retrospective analysis of 5037 patients with nasopharyngeal carcinoma treated during 1976-1985: overall survival and patterns of failure. Int J Radiat Oncol Biol Phys. 1992; 23: 261-270.
4. Bernier I, Tresca JP, Jollés P. Ligand-binding studies with a 23 kDa protein purified from bovine brain cytosol. Biochim Biophys Acta.1986; 871:19-23.
5. Yeung K, Seitz T, Li S, Janosch P, McFerran B, Kaiser C, Fee F, Katsanakis KD, Rose DW, Mischak H, Sedivy JM, Kolch W. Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature. 1999; 401:173-177.
6. Yeung KC, Rose DW, Dhillon AS, Yaros D, Gustafsson M, Chatterjee D, McFerran B, Wyche J, Kolch W, Sedivy JM. Raf kinase inhibitor protein interacts with NF-kappaBinducing kinase and TAK1 and inhibits NF-kappaB activation. Mol Cell Biol. 2001; 21:7207-7217.
7. Goel R, Baldassare JJ. Killing two birds with one RKIP. Trends Endocrinol Metab. 2004; 15:91-92.
8. Al-Mulla F, Bitar MS, Al-Maghrebi M, Behbehani AI, Al-Ali W, Rath O, Doyle B, Tan KY, Pitt A, Kolch W. Raf kinase inhibitor protein RKIP enhances signaling by glycogen synthase kinase-3β. Cancer Res. 2011; 71:1334-1343.
9. Yousuf S, Duan M, Moen EL, Cross-Knorr S, Brilliant K, Bonavida B, LaValle T, Yeung KC, Al-Mulla F, Chin E, Chatterjee D. Raf kinase inhibitor protein (RKIP) blocks signal transducer and activator of transcription 3 (STAT3) activation in breast and prostate cancer. PLoS One. 2014; 9:e92478.
10. Escara-Wilke J, Yeung K, Keller ET. Raf kinase inhibitor protein (RKIP) in cancer. Cancer Metastasis Rev. 2012; 31:615-620.
11. Keller ET, Fu Z, Brennan M. The role of Raf kinase inhibitor protein (RKIP) in health and disease. Biochem Pharmacol. 2004; 68:1049-1053.
12. Fu Z, Smith PC, Zhang L, Rubin MA, Dunn RL, Yao Z, Keller ET. Effects of raf kinase inhibitor protein expression on suppression of prostate cancer metastasis. J Natl Cancer Inst. 2003; 95: 878-889.
13. Keller ET, Fu Z, Yeung K, Brennan M. Raf kinase inhibitor protein: a prostate cancer metastasis suppressor gene. Cancer Lett. 2004; 207: 131-137.
14. Fu Z, Kitagawa Y, Shen R, Shah R, Mehra R, Rhodes D, Keller PJ, Mizokami A, Dunn R, Chinnaiyan AM, Yao Z, Keller ET. Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer. Prostate 2006; 66:248-256.
15. Hagan S1, Al-Mulla F, Mallon E, Oien K, Ferrier R, Gusterson B, García JJ, Kolch W. Reduction of Raf-1 kinase inhibitor protein expression correlates with breast cancer metastasis. Clin Cancer Res. 2005; 11: 7392-7397.
16. Li HZ, Wang Y, Gao Y, Shao J, Zhao XL, Deng WM, Liu YX, Yang J, Yao Z. Effects of raf kinase inhibitor protein expression on metastasis and progression of human epithelial ovarian cancer. Mol Cancer Res. 2008; 6:917-928.
17. Al-Mulla F, Hagan S, Behbehani AI, Bitar MS, George SS, Going JJ, García JJ, Scott L, Fyfe N, Murray GI, Kolch W. Raf kinase inhibitor protein expression in a survival analysis of colorectal cancer patients. J Clin Oncol. 2006; 24: 5672-5679.
18. Minoo P, Zlobec I, Baker K, Tornillo L, Terracciano L, Jass JR, Lugli A. Loss of raf-1 kinase inhibitor protein expression is associated with tumor progression and metastasis in colorectal cancer. Am J Clin Pathol. 2007; 127: 820-827.
19. Liu H, Li P, Li B, Sun P, Zhang J, Wang B, Jia B. RKIP suppresses gastric cancer cell proliferation and invasion and enhances apoptosis regulated by microRNA-224. Tumour Biol. 2014; 35:10095-10103.
20. Schuierer MM, Bataille F, Hagan S, Kolch W, BosserhoffAK. 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: 5186-5192.
21. Woods Ignatoski KM, Grewal NK, Markwart SM, Vellaichamy A, Chinnaiyan AM, Yeung K, Ray ME, Keller ET. Loss of Raf kinase inhibitory protein induces radioresistance in prostate cancer. Int J Radiat Oncol Biol Phys. 2008; 72:153-160.
22. Li J, Wang Y, Song Y, Fu Z, Yu W. miR-27a regulates cisplatin resistance and metastasis by targeting RKIP in human lung adenocarcinoma cells. Mol Cancer. 2014;13:193
23. Wang Z, Luo F, Li L, Yang L, Hu D, Ma X, Lu Z, Sun L, Cao Y. STAT3 activation induced by Epstein-Barr virus latent membrane protein1 causes vascular endothelial growth factor expression and cellular invasiveness via JAK3 and ERK signaling. Eur J Cancer. 2010; 46:2996-3006.
24. Devarajan E, Huang S. STAT3 as a central regulator of tumor metastases. Curr Mol Med. 2009; 9:626-933.
25. Huang S. Regulation of metastases by signal transducer and activator of transcription 3 signaling pathway: clinical implications. Clin Cancer Res. 2007; 13:1362-1366.
26. Wendt MK, Balanis N, Carlin CR, Schiemann WP. STAT3 and epithelial-mesenchymal transitions in carcinomas. JAKSTAT. 2014; 3:e28975.
27. Germain D, Frank DA. Targeting the cytoplasmic and nuclear functions of signal transducers and activators of transcription 3 for cancer therapy. Clin Cancer Res. 2007, 13:5665-5669.
28. Liao Q, Zeng Z, Guo X, Li X, Wei F, Zhang W, Li X, Chen P, Liang F, Xiang B, Ma J, Wu M, Tang H, et al. LPLUNC1 suppresses IL-6-induced nasopharyngeal carcinoma cell proliferation via inhibiting the Stat3 activation. Oncogene. 2014; 33:2098-2109.
29. Tsang CM, Cheung YC, Lui VW, Yip YL, Zhang G, Lin VW, Cheung KC, Feng Y, Tsao SW. Berberine suppresses tumorigenicity and growth of nasopharyngeal carcinoma cells by inhibiting STAT3 activation induced by tumor associated fibroblasts. BMC Cancer. 2013;13:619.
30. Lin CH, Chao LK, Hung PH, Chen YJ. EGCG inhibits the growth and tumorigenicity of nasopharyngeal tumorinitiating cells through attenuation of STAT3 activation. Int J Clin Exp Pathol. 2014; 7:2372-2381.
31. Ho Y, Tsao SW, Zeng M, Lui VW. STAT3 as a therapeutic target for Epstein-Barr virus (EBV): associated nasopharyngeal carcinoma. Cancer Lett. 2013; 330:141-149.
32. Chen Y, Ouyang GL, Yi H, Li MY, Zhang PF, Li C, Li JL, Liu YF, Chen ZC, Xiao ZQ. Identification of RKIP as an invasion suppressor protein in nasopharyngeal carcinoma by proteomic analysis. J Proteome Res 2008; 7:5254-5262.
33. Ruan L, Wang GL, Yi H, Chen Y, Tang CE, Zhang PF, Li MY, Li C, Peng F, Li JL, Chen ZC, Xiao ZQ. Raf kinase inhibitor protein correlates with sensitivity of nasopharyngeal carcinoma to radiotherapy. J Cell Biochem. 2010; 110:975-981.
34. Li SW, Wang H, Xiang YQ, Zhang HB, Lv X, Xia WX, Zeng MS, Mai HQ, Hong MH, Guo X. Prospective study of prognostic value of Raf kinase inhibitory protein and pretreatment plasma Epstein-Barr virus DNA for distant metastasis in locoregionally advanced nasopharyngeal carcinoma. Head Neck. 2013; 35:579-591.
35. Chatterjee D, Sabo E, Tavares R, Resnick MB. Inverse association between Raf Kinase Inhibitory Protein and signal transducers and activators of transcription 3 expression in gastric adenocarcinoma patients: implications for clinical outcome. Clin Cancer Res. 2008; 14:2994-3001.
36. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial- mesenchymal transitions in development and disease. Cell. 2009; 139: 871-890.
37. Beach S, Tang H, Park S, Dhillon AS, Keller ET, Kolch W, Yeung KC. Snail is a repressor of RKIP transcription in metastatic prostate cancer cells. Oncogene. 2008; 27:2243-2248.
38. Baritaki S, Huerta-Yepez S, Sahakyan A, Karagiannides I, Bakirtzi K, Jazirehi A, Bonavida B. Mechanisms of nitric oxide-mediated inhibition of EMT in cancer: inhibition of the metastasis-inducer Snail and induction of the metastasissuppressor RKIP. Cell Cycle. 2010; 9:4931-4940.
39. Shanmugaratnam K, Sobin LH. The World Health Organization histological classification of tumours of the upper respiratory tract and ear. A commentary on the second edition. Cancer. 1993; 71:2689-2697.
40. Qian CN, Guo X, Cao B, Kort EJ, Lee CC, Chen J, Wang LM, Mai WY, Min HQ, Hong MH, Vande Woude GF, Resau JH, Teh BT. Met protein expression level correlates with survival in patients with late-stage nasopharyngeal carcinoma. Cancer Res. 2002; 62:589-596.
41. Trakul N, Menard RE, Schade GR, Qian Z, Rosner MR. Raf kinase inhibitory protein regulates Raf-1 but not B-Raf kinase activation. J Biol Chem. 2005; 280:24931-24940.