MEK1 is associated with carboplatin resistance and is a prognostic biomarker in epithelial ovarian cancer

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Pénzváltó, Zsófia ^a   Lánczky, András ^a   Lénárt, Julianna ^a   Meggyesházi, Nóra ^a,b   Krenács, Tibor ^a,b   Szoboszlai, Norbert ^c   Denkert, Carsten ^d   Pete, Imre ^e   Gyorffy, Balázs ^a,f  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e NATIONAL INSTITUTE OF ONCOLOGY   (Hungary)

^f SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Carboplatin; Chemotherapy; MEK; Ovarian cancer

Indexed keywords

CARBOPLATIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; PLATINUM DERIVATIVE; ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; MAP2K1 PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; SMALL INTERFERING RNA;

APOPTOSIS ASSAY; ARTICLE; CANCER PROGNOSIS; CANCER RESISTANCE; CAOV 3 CELL LINE; CCT3 GENE; CELL VIABILITY ASSAY; CNOT8 GENE; COHORT ANALYSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CSDE1 GENE; DRUG POTENTIATION; DRUG SENSITIZATION; ES 2 CELL LINE; FEMALE; FUBP1 GENE; GENE; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; JRK GENE; MAJOR CLINICAL STUDY; NFAT2CIP GENE; OVARIAN CANCER CELL LINE; OVARY CARCINOMA; OVCAR 3 CELL LINE; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; RECURRENCE FREE SURVIVAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RTF1 GENE; SKOV 3 CELL LINE; SURVIVAL TIME; TRANSCRIPTOMICS; TREATMENT RESPONSE; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BIOLOGY; CELL SURVIVAL; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; INFORMATION PROCESSING; MORTALITY; NEOPLASMS, GLANDULAR AND EPITHELIAL; NUCLEIC ACID DATABASE; OVARIAN NEOPLASMS; PROGNOSIS; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BIOMARKERS; CARBOPLATIN; CELL LINE, TUMOR; CELL SURVIVAL; COHORT STUDIES; COMPUTATIONAL BIOLOGY; DATABASES, NUCLEIC ACID; DATASETS AS TOPIC; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE SILENCING; HUMANS; MAP KINASE KINASE 1; NEOPLASMS, GLANDULAR AND EPITHELIAL; OVARIAN NEOPLASMS; PROGNOSIS; PROTEIN KINASE INHIBITORS; RNA, SMALL INTERFERING;

EID: 84965092679     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-837     Document Type: Article

References (46)

1. Siegel R, Naishadham D, Jemal A: Cancer statistics, 2013. CA Cancer J Clin 2013, 63:11-30.
2. Burger RA, Brady MF, Bookman MA, Fleming GF, Monk BJ, Huang H, Mannel RS, Homesley HD, Fowler J, Greer BE, Boente M, Birrer MJ, Liang SX: Incorporation of bevacizumab in the primary treatment of ovarian cancer. N Engl J Med 2011, 365:2473-2483.
3. Perren TJ, Swart AM, Pfisterer J, Ledermann JA, Pujade-Lauraine E, Kristensen G, Carey MS, Beale P, Cervantes A, Kurzeder C, du Bois A, Sehouli J, Kimmig R, Stahle A, Collinson F, Essapen S, Gourley C, Lortholary A, Selle F, Mirza MR, Leminen A, Plante M, Stark D, Qian W, Parmar MK, Oza AM: A phase 3 trial of bevacizumab in ovarian cancer. N Engl J Med 2011, 365:2484-2496.
4. Miller DS, Blessing JA, Krasner CN, Mannel RS, Hanjani P, Pearl ML, Waggoner SE, Boardman CH: Phase II evaluation of pemetrexed in the treatment of recurrent or persistent platinum-resistant ovarian or primary peritoneal carcinoma: a study of the gynecologic oncology group. J Clin Oncol 2009, 27:2686-2691.
5. Agarwal R, Kaye SB: Ovarian cancer: strategies for overcoming resistance to chemotherapy. Nat Rev Cancer 2003, 3:502-516.
6. Siddik ZH: Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene 2003, 22:7265-7279.
7. Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M, Kroemer G: Molecular mechanisms of cisplatin resistance. Oncogene 2012, 31:1869-1883.
8. Halon A, Nowak-Markwitz E, Maciejczyk A, Pudelko M, Gansukh T, Gyorffy B, Donizy P, Murawa D, Matkowski R, Spaczynski M, Lage H, Surowiak P: Loss of estrogen receptor beta expression correlates with shorter overall survival and lack of clinical response to chemotherapy in ovarian cancer patients. Anticancer Res 2011, 31:711-718.
9. Gyorffy B, Dietel M, Fekete T, Lage H: A snapshot of microarray-generated gene expression signatures associated with ovarian carcinoma. Int J Gynecol Cancer 2008, 18:1215-1233.
10. Hartmann LC, Lu KH, Linette GP, Cliby WA, Kalli KR, Gershenson D, Bast RC, Stec J, Iartchouk N, Smith DI, Ross JS, Hoersch S, Shridhar V, Lillie J, Kaufmann SH, Clark EA, Damokosh AI: Gene expression profiles predict early relapse in ovarian cancer after platinum-paclitaxel chemotherapy. Clin Canc Res 2005, 11:2149-2155.
11. Spentzos D, Levine DA, Ramoni MF, Joseph M, Gu X, Boyd J, Libermann TA, Cannistra SA: Gene expression signature with independent prognostic significance in epithelial ovarian cancer. J Clin Oncol 2004, 22:4700-4710.
12. Denkert C, Budczies J, Darb-Esfahani S, Gyorffy B, Sehouli J, Konsgen D, Zeillinger R, Weichert W, Noske A, Buckendahl AC, Muller BM, Dietel M, Lage H: A prognostic gene expression index in ovarian cancer-validation across different independent data sets. J Pathol 2009, 218:273-280.
13. Konstantinopoulos PA, Spentzos D, Cannistra SA: Gene-expression profiling in epithelial ovarian cancer. Nat Clin Pract Oncol 2008, 5:577-587.
14. Gautier L, Moller M, Friis-Hansen L, Knudsen S: Alternative mapping of probes to genes for Affymetrix chips. BMC Bioinformatics 2004, 5:111.
15. Sims AH, Smethurst GJ, Hey Y, Okoniewski MJ, Pepper SD, Howell A, Miller CJ, Clarke RB: The removal of multiplicative, systematic bias allows integration of breast cancer gene expression datasets-improving meta-analysis and prediction of prognosis. BMC Med Genet 2008, 1:42.
16. Gyorffy B, Lanczky A, Szallasi Z: Implementing an online tool for genomewide validation of survival-associated biomarkers in ovarian-cancer using microarray data from 1287 patients. Endocr Relat Cancer 2012, 19:197-208.
17. Fekete T, Raso E, Pete I, Tegze B, Liko I, Munkacsy G, Sipos N, Rigo J Jr, Gyorffy B: Meta-analysis of gene expression profiles associated with histological classification and survival in 829 ovarian cancer samples. Int J Cancer 2012, 131:95-105.
18. Li Q, Birkbak NJ, Gyorffy B, Szallasi Z, Eklund AC: Jetset: selecting the optimal microarray probe set to represent a gene. BMC Bioinformatics 2011, 12:474.
19. Sebolt-Leopold JS, Herrera R: Targeting the mitogen-activated protein kinase cascade to treat cancer. Nat Rev Cancer 2004, 4:937-947.
20. Akinleye A, Furqan M, Mukhi N, Ravella P, Liu D: MEK and the inhibitors: from bench to bedside. J Hematol Oncol 2013, 6:27.
21. Yap TA, Carden CP, Kaye SB: Beyond chemotherapy: targeted therapies in ovarian cancer. Nat Rev Cancer 2009, 9:167-181.
22. Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG: Cancer drug resistance: an evolving paradigm. Nat Rev Cancer 2013, 13:714-726.
23. Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton L, Chan E, Peng J, Lin E, Wang Y, Sosman J, Ribas A, Li J, Moffat J, Sutherlin DP, Koeppen H, Merchant M, Neve R, Settleman J: Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012, 487:505-509.
24. Rahman MT, Nakayama K, Rahman M, Katagiri H, Katagiri A, Ishibashi T, Ishikawa M, Sato E, Iida K, Nakayama N, Ishikawa N, Miyazaki K: KRAS and MAPK1 gene amplification in type II ovarian carcinomas. Int J Mol Sci 2013, 14:13748-13762.
25. Yang JY, Yoshihara K, Tanaka K, Hatae M, Masuzaki H, Itamochi H, Takano M, Ushijima K, Tanyi JL, Coukos G, Lu Y, Mills GB, Verhaak RG: Predicting time to ovarian carcinoma recurrence using protein markers. J Clin Invest 2013, 123:3740-3750.
26. Ciuffreda L, Del Bufalo D, Desideri M, Di Sanza C, Stoppacciaro A, Ricciardi MR, Chiaretti S, Tavolaro S, Benassi B, Bellacosa A, Foa R, Tafuri A, Cognetti F, Anichini A, Zupi G, Milella M: Growth-inhibitory and antiangiogenic activity of the MEK inhibitor PD0325901 in malignant melanoma with or without BRAF mutations. Neoplasia 2009, 11:720-731.
27. Henderson YC, Chen Y, Frederick MJ, Lai SY, Clayman GL: MEK inhibitor PD0325901 significantly reduces the growth of papillary thyroid carcinoma cells in vitro and in vivo. Mol Cancer Ther 2010, 9:1968-1976.
28. Boasberg PD, Redfern CH, Daniels GA, Bodkin D, Garrett CR, Ricart AD: Pilot study of PD-0325901 in previously treated patients with advanced melanoma, breast cancer, and colon cancer. Cancer Chemother Pharmacol 2011, 68:547-552.
29. Fung MK, Cheung HW, Ling MT, Cheung AL, Wong YC, Wang X: Role of MEK/ERK pathway in the MAD2-mediated cisplatin sensitivity in testicular germ cell tumour cells. Br J Cancer 2006, 95:475-484.
30. Schweyer S, Soruri A, Meschter O, Heintze A, Zschunke F, Miosge N, Thelen P, Schlott T, Radzun HJ, Fayyazi A: Cisplatin-induced apoptosis in human malignant testicular germ cell lines depends on MEK/ERK activation. Br J Cancer 2004, 91:589-598.
31. Wang X, Martindale JL, Holbrook NJ: Requirement for ERK activation in cisplatin-induced apoptosis. J Biol Chem 2000, 275:39435-39443.
32. Yeh PY, Chuang SE, Yeh KH, Song YC, Ea CK, Cheng AL: Increase of the resistance of human cervical carcinoma cells to cisplatin by inhibition of the MEK to ERK signaling pathway partly via enhancement of anticancer drug-induced NF kappa B activation. Biochem Pharmacol 2002, 63:1423-1430.
33. Persons DL, Yazlovitskaya EM, Cui W, Pelling JC: Cisplatin-induced activation of mitogen-activated protein kinases in ovarian carcinoma cells: inhibition of extracellular signal-regulated kinase activity increases sensitivity to cisplatin. Clin Canc Res 1999, 5:1007-1014.
34. Cui W, Yazlovitskaya EM, Mayo MS, Pelling JC, Persons DL: Cisplatin-induced response of c-jun N-terminal kinase 1 and extracellular signal-regulated protein kinases 1 and 2 in a series of cisplatin-resistant ovarian carcinoma cell lines. Mol Carcinog 2000, 29:219-228.
35. Aksamitiene E, Kiyatkin A, Kholodenko BN: Cross-talk between mitogenic Ras/MAPK and survival PI3K/Akt pathways: a fine balance. Biochem Soc Trans 2012, 40:139-146.
36. Cheng JQ, Lindsley CW, Cheng GZ, Yang H, Nicosia SV: The Akt/PKB pathway: molecular target for cancer drug discovery. Oncogene 2005, 24:7482-7492.
37. Page C, Lin HJ, Jin Y, Castle VP, Nunez G, Huang M, Lin J: Overexpression of Akt/AKT can modulate chemotherapy-induced apoptosis. Anticancer Res 2000, 20:407-416.
38. Stronach EA, Chen M, Maginn EN, Agarwal R, Mills GB, Wasan H, Gabra H: DNA-PK mediates AKT activation and apoptosis inhibition in clinically acquired platinum resistance. Neoplasia 2011, 13:1069-1080.
39. Meloche S, Pouyssegur J: The ERK1/2 mitogen-activated protein kinase pathway as a master regulator of the G1-to S-phase transition. Oncogene 2007, 26:3227-3239.
40. Mirmohammadsadegh A, Mota R, Gustrau A, Hassan M, Nambiar S, Marini A, Bojar H, Tannapfel A, Hengge UR: ERK1/2 is highly phosphorylated in melanoma metastases and protects melanoma cells from cisplatinmediated apoptosis. J Investig Dermatol 2007, 127:2207-2215.
41. 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, 31:2412-2422.
42. Singer G, Oldt R 3rd, Cohen Y, Wang BG, Sidransky D, Kurman RJ, Shih Ie M: Mutations in BRAF and KRAS characterize the development of low-grade ovarian serous carcinoma. J Natl Cancer Inst 2003, 95:484-486.
43. Lassus H, Sihto H, Leminen A, Joensuu H, Isola J, Nupponen NN, Butzow R: Gene amplification, mutation, and protein expression of EGFR and mutations of ERBB2 in serous ovarian carcinoma. J MolMed 2006, 84:671-681.
44. Gershenson DM, Sun CC, Bodurka D, Coleman RL, Lu KH, Sood AK, Deavers M, Malpica AL, Kavanagh JJ: Recurrent low-grade serous ovarian carcinoma is relatively chemoresistant. Gynecol Oncol 2009, 114:48-52.
45. Farley J, Brady WE, Vathipadiekal V, Lankes HA, Coleman R, Morgan MA, Mannel R, Yamada SD, Mutch D, Rodgers WH, Birrer M, Gershenson DM: Selumetinib in women with recurrent low-grade serous carcinoma of the ovary or peritoneum: an open-label, single-arm, phase 2 study. Lancet Oncol 2013, 14:134-140.
46. Hayat MJ, Howlader N, Reichman ME, Edwards BK: Cancer statistics, trends, and multiple primary cancer analyses from the Surveillance, Epidemiology, and End Results (SEER) program. Oncologist 2007, 12:20-37.