Downregulation of miRNA-31 induces taxane resistance in ovarian cancer cells through increase of receptor tyrosine kinase MET

Oncogenesis

Volumn 2, Issue , 2013, Pages

  Mitamura, T ^a   Watari, H ^a   Wang, L ^a   Kanno, H ^a   Hassan, M K ^a,b   Miyazaki, M ^a   Katoh, Y ^a   Kimura, T ^a   Tanino, M ^a   Nishihara, H ^a   Tanaka, S ^a   Sakuragi, N ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b Port Said University   (Egypt)

Author keywords

chemoresistance; MET; microRNA; ovarian cancer; paclitaxel

Indexed keywords

MESSENGER RNA; MICRORNA 31; PACLITAXEL; SCATTER FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER PROGNOSIS; CANCER RESISTANCE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

EID: 84880554542     PISSN: None     EISSN: 21579024     Source Type: Journal    
DOI: 10.1038/oncsis.2013.3     Document Type: Article

References (46)

1. Boyle P, Levin B. World cancer report 2008. World Health Organization: Lyon, 2008, 2008.
2. Landis SH, Murray T, Bolden S, Wingo PA. Cancer statistics, 1999. CA Cancer J Clin 1999; 49: 8-31. (Pubitemid 29094959)
3. Cannistra SA. Cancer of the ovary. N Engl J Med 2004; 351: 2519-2529.
4. Kristensen GB, Trope C. Epithelial ovarian carcinoma. Lancet 1997; 349: 113-117. (Pubitemid 127700347)
5. Vaughan S, Coward JI, Bast Jr RC, Berchuck A, Berek JS, Brenton JD et al. Rethinking ovarian cancer: recommendations for improving outcomes. Nat Rev Cancer 2011; 11: 719-725.
6. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-233.
7. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E et al. Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 2002; 99: 15524-15529. (Pubitemid 35403967)
8. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 2006; 103: 2257-2261. (Pubitemid 43271657)
9. Garzon R, Marcucci G, Croce CM. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov 2010; 9: 775-789.
10. Zhou M, Liu Z, Zhao Y, Ding Y, Liu H, Xi Y et al. MicroRNA-125b confers the resistance of breast cancer cells to paclitaxel through suppression of pro-apoptotic Bcl-2 antagonist killer 1 (Bak1) expression. J Biol Chem 2010; 285: 21496-21507.
11. Fornari F, Milazzo M, Chieco P, Negrini M, Calin GA, Grazi GL et al. MiR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 2010; 70: 5184-5193.
12. Yang N, Kaur S, Volinia S, Greshock J, Lassus H, Hasegawa K et al. MicroRNA microarray identifies Let-7i as a novel biomarker and therapeutic target in human epithelial ovarian cancer. Cancer Res 2008; 68: 10307-10314.
13. Valastyan S, Reinhardt F, Benaich N, Calogrias D, Szasz AM, Wang ZC et al. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 2009; 137: 1032-1046.
14. Jeffers M, Taylor GA, Weidner KM, Omura S, Vande Woude GF. Degradation of the Met tyrosine kinase receptor by the ubiquitin-proteasome pathway. Mol Cell Biol 1997; 17: 799-808. (Pubitemid 27044379)
15. Ciechanover A, Shkedy D, Oren M, Bercovich B. Degradation of the tumor suppressor protein p53 by the ubiquitin-mediated proteolytic system requires a novel species of ubiquitin-carrier protein, E2. J Biol Chem 1994; 269: 9582-9589. (Pubitemid 24196554)
16. Benedet JL, Bender H, Jones 3rd H, Ngan HY, Pecorelli S. FIGO staging classifications and clinical practice guidelines in the management of gynecologic cancers. FIGO Committee on Gynecologic Oncology. Int J Gynaecol Obstet 2000; 70: 209-262.
17. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009; 45: 228-247.
18. van der Burg ME, van Lent M, Buyse M, Kobierska A, Colombo N, Favalli G et al. Gynecological Cancer Cooperative Group of the European Organization for Research and Treatment of Cancer. The effect of debulking surgery after induction chemotherapy on the prognosis in advanced epithelial ovarian cancer. N Engl J Med 1995; 332: 629-634.
19. Eisenkop SM, Spirtos NM. What are the current surgical objectives, strategies, and technical capabilities of gynecologic oncologists treating advanced epithelial ovarian cancer? Gynecol Oncol 2001; 82: 489-497. (Pubitemid 32826449)
20. Horwitz SB. Mechanism of action of taxol. Trends Pharmacol Sci 1992; 13: 134-136.
21. Wahl AF, Donaldson KL, Fairchild C, Lee FY, Foster SA, Demers GW et al. Loss of normal p53 function confers sensitization to Taxol by increasing G2/M arrest and apoptosis. Nat Med 1996; 2: 72-79. (Pubitemid 26029571)
22. Patel N, Chatterjee SK, Vrbanac V, Chung I, Mu CJ, Olsen RR et al. Rescue of paclitaxel sensitivity by repression of Prohibitin1 in drug-resistant cancer cells. Proc Natl Acad Sci USA 2010; 107: 2503-2508.
23. Tan M, Jing T, Lan KH, Neal CL, Li P, Lee S et al. Phosphorylation on tyrosine-15 of p34(Cdc2) by ErbB2 inhibits p34(Cdc2) activation and is involved in resistance to taxol-induced apoptosis. Mol Cell 2002; 9: 993-1004. (Pubitemid 34626669)
24. Goncalves A, Braguer D, Kamath K, Martello L, Briand C, Horwitz S et al. Resistance to Taxol in lung cancer cells associated with increased microtubule dynamics. Proc Natl Acad Sci USA 2001; 98: 11737-11742.
25. Lu J, Tan M, Huang WC, Li P, Guo H, Tseng LM et al. Mitotic deregulation by survivin in ErbB2-overexpressing breast cancer cells contributes to Taxol resistance. Clin Cancer Res 2009; 15: 1326-1334.
26. Kavallaris M, Kuo DY, Burkhart CA, Regl DL, Norris MD, Haber M et al. Taxolresistant epithelial ovarian tumors are associated with altered expression of specific beta-tubulin isotypes. J Clin Invest 1997; 100: 1282-1293. (Pubitemid 27386315)
27. Gottesman MM, Pastan I, Ambudkar SV. P-glycoprotein and multidrug resistance. Curr Opin Genet Dev 1996; 6: 610-617. (Pubitemid 26372158)
28. Valeri N, Gasparini P, Braconi C, Paone A, Lovat F, Fabbri M et al. MicroRNA-21 induces resistance to 5-fluorouracil by down-regulating human DNA MutS homolog 2 (hMSH2). Proc Natl Acad Sci USA 2010; 107: 21098-21103.
29. Sarver AL, Li L, Subramanian S. MicroRNA miR-183 functions as an oncogene by targeting the transcription factor EGR1 and promoting tumor cell migration. Cancer Res 2010; 70: 9570-9580.
30. Miller TE, Ghoshal K, Ramaswamy B, Roy S, Datta J, Shapiro CL et al. MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J Biol Chem 2008; 283: 29897-29903.
31. Nakajima G, Hayashi K, Xi Y, Kudo K, Uchida K, Takasaki K et al. Non-coding microRNAs hsa-let-7g and hsa-miR-181b are associated with chemoresponse to S-1 in colon cancer. Cancer Genomics Proteomics 2006; 3: 317-324. (Pubitemid 44701551)
32. Dai Y, Xie CH, Neis JP, Fan CY, Vural E, Spring PM. MicroRNA expression profiles of head and neck squamous cell carcinoma with docetaxel-induced multidrug resistance. Head Neck 2011; 33: 786-791.
33. Creighton CJ, Fountain MD, Yu Z, Nagaraja AK, Zhu H, Khan M et al. Molecular profiling uncovers a p53-associated role for microRNA-31 in inhibiting the proliferation of serous ovarian carcinomas and other cancers. Cancer Res 2010; 70: 1906-1915.
34. Ivanov SV, Goparaju CM, Lopez P, Zavadil J, Toren-Haritan G, Rosenwald S et al. Pro-tumorigenic effects of miR-31 loss in mesothelioma. J Biol Chem 2010; 285: 22809-22817.
35. Liu CJ, Tsai MM, Hung PS, Kao SY, Liu TY, Wu KJ et al. miR-31 ablates expression of the HIF regulatory factor FIH to activate the HIF pathway in head and neck carcinoma. Cancer Res 2010; 70: 1635-1644.
36. Trusolino L, Bertotti A, Comoglio PM. MET signalling: principles and functions in development, organ regeneration and cancer. Nat Rev Mol Cell Biol 2010; 11: 834-848.
37. Turke AB, Zejnullahu K, Wu YL, Song Y, Dias-Santagata D, Lifshits E et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010; 17: 77-88.
38. Suda K, Murakami I, Katayama T, Tomizawa K, Osada H, Sekido Y et al. Reciprocal and complementary role of MET amplification and EGFR T790M mutation in acquired resistance to kinase inhibitors in lung cancer. Clin Cancer Res 2010; 16: 5489-5498.
39. Bu R, Uddin S, Bavi P, Hussain AR, Al-Dayel F, Ghourab S et al. HGF/c-Met pathway has a prominent role in mediating antiapoptotic signals through AKT in epithelial ovarian carcinoma. Lab Invest 2011; 91: 124-137.
40. Tang MK, Zhou HY, Yam JW, Wong AS. c-Met overexpression contributes to the acquired apoptotic resistance of nonadherent ovarian cancer cells through a cross talk mediated by phosphatidylinositol 3-kinase and extracellular signalregulated kinase 1/2. Neoplasia 2010; 12: 128-138.
41. Zillhardt M, Park SM, Romero IL, Sawada K, Montag A, Krausz T et al. Foretinib (GSK1363089), an orally available multikinase inhibitor of c-Met and VEGFR-2, blocks proliferation, induces anoikis, and impairs ovarian cancer metastasis. Clin Cancer Res 2011; 17: 4042-4051.
42. Sawada K, Radjabi AR, Shinomiya N, Kistner E, Kenny H, Becker AR et al. c-Met overexpression is a prognostic factor in ovarian cancer and an effective target for inhibition of peritoneal dissemination and invasion. Cancer Res 2007; 67: 1670-1679. (Pubitemid 46383393)
43. Kikuchi Y, Miyauchi M, Kizawa I, Oomori K, Kato K. Establishment of a cisplatinresistant human ovarian cancer cell line. J Natl Cancer Inst 1986; 77: 1181-1185. (Pubitemid 17005092)
44. Sato S, Itamochi H, Kigawa J, Oishi T, Shimada M, Sato S et al. Combination chemotherapy of oxaliplatin and 5-fluorouracil may be an effective regimen for mucinous adenocarcinoma of the ovary: a potential treatment strategy. Cancer Sci 2009; 100: 546-551.
45. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA 2006; 103: 12481-12486. (Pubitemid 44267285)
46. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408. (Pubitemid 34164012) Technology Technology