miR-634 restores drug sensitivity in resistant ovarian cancer cells by targeting the Ras-MAPK pathway

Molecular Cancer

Volumn 14, Issue 1, 2015, Pages

  van Jaarsveld, Marijn T M ^a,c   van Kuijk, Patricia F ^a   Boersma, Antonius W M ^a   Helleman, Jozien ^a   van IJcken, Wilfred F ^b   Mathijssen, Ron H J ^a   Pothof, Joris ^b   Berns, Els M J J ^a   Verweij, Jaap ^a   Wiemer, Erik A C ^a  

^a ERASMUS MC CANCER INSTITUTE   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

Chemotherapy; Cisplatin; Drug resistance; MicroRNA; miR 634; MiRNA; Ovarian cancer; Ras MAPK pathway; RPS6KA3; RSK2

Indexed keywords

CARBOPLATIN; CCND1 PROTEIN; CISPLATIN; DOXORUBICIN; GEMCITABINE; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; IFOSFAMIDE; MICRORNA; MICRORNA 634; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE INHIBITOR; OLAPARIB; PACLITAXEL; RAS PROTEIN; REGULATOR PROTEIN; RSK2 PROTEIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; MIRN-634 MICRORNA, HUMAN;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER RESISTANCE; CELL CYCLE PROGRESSION; CELL VIABILITY; CHEMOSENSITIVITY; CHEMOSENSITIZATION; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; GENE OVEREXPRESSION; GENE REPRESSION; GENE TARGETING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; MIR 634 GENE; OVARIAN CANCER CELL LINE; OVARY CANCER; PHENOTYPE; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; OVARY TUMOR; PHYSIOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CISPLATIN; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; OVARIAN NEOPLASMS; PACLITAXEL;

EID: 84947233973     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/s12943-015-0464-4     Document Type: Article

References (57)

1. Berns EM, Bowtell DD. The changing view of high-grade serous ovarian cancer. Cancer Res. 2012;72(11):2701-4.
2. Ledermann JA, Marth C, Carey MS, Birrer M, Bowtell DD, Kaye S, et al. Role of molecular agents and targeted therapy in clinical trials for women with ovarian cancer. Int J Gynecol Cancer. 2011;21(4):763-70.
3. Vergote I, Trope CG, Amant F, Kristensen GB, Ehlen T, Johnson N, et al. Neoadjuvant chemotherapy or primary surgery in stage IIIC or IV ovarian cancer. N Engl J Med. 2010;363(10):943-53.
4. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin. 2010;60(5):277-300.
5. Ozols RF. Epithelial Ovarian Cancer. In: Hoskins WJYR, Markman M, Perez CA, Barakat R, Randall M, editors. Principles and Practice of Gynaecologic Oncology. Philadelphia, PA: Lippincott Williams & Wilkins; 2005. p. 895-985.
6. Zhang W, Liu HT. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 2002;12(1):9-18.
7. Li W, Melton DW. Cisplatin regulates the MAPK kinase pathway to induce increased expression of DNA repair gene ERCC1 and increase melanoma chemoresistance. Oncogene. 2012;31(19):2412-22.
8. Dhillon AS, Hagan S, Rath O, Kolch W. MAP kinase signalling pathways in cancer. Oncogene. 2007;26(22):3279-90.
9. MacCorkle RA, Tan TH. Mitogen-activated protein kinases in cell-cycle control. Cell Biochem Biophys. 2005;43(3):451-61.
10. Cagnol S, Chambard JC. ERK and cell death: mechanisms of ERK-induced cell death--apoptosis, autophagy and senescence. Febs J. 2010;277(1):2-21.
11. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215-33.
12. van Jaarsveld MT, Helleman J, Berns EM, Wiemer EA. MicroRNAs in ovarian cancer biology and therapy resistance. Int J Biochem Cell Biol. 2010;42(8):1282-90.
13. van Jaarsveld MT, Helleman J, Boersma AW, van Kuijk PF, van Ijcken WF, Despierre E, et al. miR-141 regulates KEAP1 and modulates cisplatin sensitivity in ovarian cancer cells. Oncogene. 2013;32(36):4284-93.
14. Kool M, de Haas M, Scheffer GL, Scheper RJ, van Eijk MJ, Juijn JA, et al. Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res. 1997;57(16):3537-47.
15. Schmidt W, Chaney SG. Role of carrier ligand in platinum resistance of human carcinoma cell lines. Cancer Res. 1993;53(4):799-805.
16. Dunfield LD, Shepherd TG, Nachtigal MW. Primary culture and mRNA analysis of human ovarian cells. Biol Proced Online. 2002;4:55-61.
17. Shepherd TG, Theriault BL, Campbell EJ, Nachtigal MW. Primary culture of ovarian surface epithelial cells and ascites-derived ovarian cancer cells from patients. Nat Protoc. 2006;1(6):2643-9.
18. Ayhan A, Kurman RJ, Yemelyanova A, Vang R, Logani S, Seidman JD, et al. Defining the cut point between low-grade and high-grade ovarian serous carcinomas: a clinicopathologic and molecular genetic analysis. Am J Surg Pathol. 2009;33(8):1220-4.
19. Brozovic A, Osmak M. Activation of mitogen-activated protein kinases by cisplatin and their role in cisplatin-resistance. Cancer Lett. 2007;251(1):1-16.
20. van Jaarsveld MT, Blijdorp IC, Boersma AW, Pothof J, Mathijssen RH, Verweij J, et al. The kinase RSK2 modulates the sensitivity of ovarian cancer cells to cisplatin. Eur J Cancer. 2013;49(2):345-51.
21. Cummins JM, He Y, Leary RJ, Pagliarini R, Diaz Jr LA, Sjoblom T, et al. The colorectal microRNAome. Proc Natl Acad Sci U S A. 2006;103(10):3687-92.
22. Ostling P, Leivonen SK, Aakula A, Kohonen P, Makela R, Hagman Z, et al. Systematic analysis of microRNAs targeting the androgen receptor in prostate cancer cells. Cancer Res. 2011;71(5):1956-67.
23. Li Y, Choi PS, Casey SC, Dill DL, Felsher DW. MYC through miR-17-92 suppresses specific target genes to maintain survival, autonomous proliferation, and a neoplastic state. Cancer Cell. 2014;26(2):262-72.
24. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, et al. RAS is regulated by the let-7 microRNA family. Cell. 2005;120(5):635-47.
25. Lee YS, Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 2007;21(9):1025-30.
26. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008;10(5):593-601.
27. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 2008;22(7):894-907.
28. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, Spaderna S, et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 2008;9(6):582-9.
29. Liu YN, Yin JJ, Abou-Kheir W, Hynes PG, Casey OM, Fang L, et al. MiR-1 and miR-200 inhibit EMT via Slug-dependent and tumorigenesis via Slug-independent mechanisms. Oncogene. 2013;32(3):296-306.
30. Weinstein IB, Joe A. Oncogene addiction. Cancer Res. 2008;68(9):3077-80.
31. Ewings KE, Wiggins CM, Cook SJ. Bim and the pro-survival Bcl-2 proteins: opposites attract. ERK repels Cell Cycle. 2007;6(18):2236-40.
32. Romeo Y, Zhang X, Roux PP. Regulation and function of the RSK family of protein kinases. Biochem J. 2012;441(2):553-69.
33. Ray-David H, Romeo Y, Lavoie G, Deleris P, Tcherkezian J, Galan JA, et al. RSK promotes G2 DNA damage checkpoint silencing and participates in melanoma chemoresistance. Oncogene. 2013;32(38):4480-9.
34. Sulzmaier FJ, Ramos JW. RSK isoforms in cancer cell invasion and metastasis. Cancer Res. 2013;73(20):6099-105.
35. Chen C, Zhang L, Huang NJ, Huang B, Kornbluth S. Suppression of DNA-damage checkpoint signaling by Rsk-mediated phosphorylation of Mre11. Proc Natl Acad Sci U S A. 2013;110(51):20605-10.
36. Santarpia L, Lippman SM, El-Naggar AK. Targeting the MAPK-RAS-RAF signaling pathway in cancer therapy. Expert Opin Ther Targets. 2012;16(1):103-19.
37. Pritchard AL, Hayward NK. Molecular pathways: mitogen-activated protein kinase pathway mutations and drug resistance. Clin Cancer Res. 2013;19(9):2301-9.
38. Seton-Rogers S. Therapeutics: Delving deeper into resistance. Nat Rev Cancer. 2013;14(1):7.
39. Shan W, Liu J. Epithelial ovarian cancer: focus on genetics and animal models. Cell Cycle. 2009;8(5):731-5.
40. Karst AM, Drapkin R. The new face of ovarian cancer modeling: better prospects for detection and treatment. F1000 Med Rep. 2011;3:22.
41. Leivonen SK, Sahlberg KK, Makela R, Due EU, Kallioniemi O, Borresen-Dale AL, et al. High-throughput screens identify microRNAs essential for HER2 positive breast cancer cell growth. Mol Oncol. 2014;8(1):93-104.
42. Rainer J, Ploner C, Jesacher S, Ploner A, Eduardoff M, Mansha M, et al. Glucocorticoid-regulated microRNAs and mirtrons in acute lymphoblastic leukemia. Leukemia. 2009;23(4):746-52.
43. Bach D, Fuereder J, Karbiener M, Scheideler M, Ress AL, Neureiter D, et al. Comprehensive analysis of alterations in the miRNome in response to photodynamic treatment. J Photochem Photobiol B. 2013;120:74-81.
44. Peng X, Cao P, He D, Han S, Zhou J, Tan G, et al. MiR-634 sensitizes nasopharyngeal carcinoma cells to paclitaxel and inhibits cell growth both in vitro and in vivo. Int J Clin Exp Pathol. 2014;7(10):6784-91.
45. Yamamoto S, Inoue J, Kawano T, Kozaki K, Omura K, Inazawa J. The impact of miRNA-based molecular diagnostics and treatment of NRF2-stabilized tumors. Mol Cancer Res. 2014;12(1):58-68.
46. Newman MA, Mani V, Hammond SM. Deep sequencing of microRNA precursors reveals extensive 3' end modification. RNA. 2011;17(10):1795-803.
47. Wyman SK, Knouf EC, Parkin RK, Fritz BR, Lin DW, Dennis LM, et al. Post-transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. Genome Res. 2011;21(9):1450-61.
48. Kotoh S, Naito S, Yokomizo A, Kumazawa J, Asakuno K, Kohno K, et al. Increased expression of DNA topoisomerase I gene and collateral sensitivity to camptothecin in human cisplatin-resistant bladder cancer cells. Cancer Res. 1994;54(12):3248-52.
49. Goto S, Yoshida K, Morikawa T, Urata Y, Suzuki K, Kondo T. Augmentation of transport for cisplatin-glutathione adduct in cisplatin-resistant cancer cells. Cancer Res. 1995;55(19):4297-301.
50. Beaufort CM, Helmijr JC, Piskorz AM, Hoogstraat M, Ruigrok-Ritstier K, Besselink N, et al. Ovarian cancer cell line panel (OCCP): clinical importance of in vitro morphological subtypes. PLoS One. 2014;9(9):e103988.
51. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101-8.
52. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, Mitchell JB. Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res. 1987;47(4):936-42.
53. Burger H, Zoumaro-Djayoon A, Boersma AW, Helleman J, Berns EM, Mathijssen RH, et al. Differential transport of platinum compounds by the human organic cation transporter hOCT2 (hSLC22A2). Br J Pharmacol. 2010;159(4):898-908.
54. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A. 2001;98(9):5116-21.
55. Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science. 1999;286(5443):1358-62.
56. Ewings KE, Hadfield-Moorhouse K, Wiggins CM, Wickenden JA, Balmanno K, Gilley R, et al. ERK1/2-dependent phosphorylation of BimEL promotes its rapid dissociation from Mcl-1 and Bcl-xL. Embo J. 2007;26(12):2856-67.
57. Dehan E, Bassermann F, Guardavaccaro D, Vasiliver-Shamis G, Cohen M, Lowes KN, et al. betaTrCP- and Rsk1/2-mediated degradation of BimEL inhibits apoptosis. Mol Cell. 2009;33(1):109-16.