Differential outcome of MEK1/2 inhibitor-platinum combinations in platinum-sensitive and -resistant ovarian carcinoma cells

Cancer Letters

Volumn 347, Issue 2, 2014, Pages 212-224

  Cossa, Giacomo ^a,b   Lanzi, Cinzia ^a   Cassinelli, Giuliana ^a   Carenini, Nives ^a   Arrighetti, Noemi ^a   Gatti, Laura ^a   Corna, Elisabetta ^a   Zunino, Franco ^a   Zaffaroni, Nadia ^a   Perego, Paola ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Drug resistance; FOXO1; MEK inhibitors; Ovarian carcinoma; Platinum compounds

Indexed keywords

DRUG RESISTANCE; FOXO1; MEK INHIBITORS; OVARIAN CARCINOMA; PLATINUM COMPOUNDS;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; ENZYME ACTIVATION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; HUMANS; IN SITU NICK-END LABELING; MAP KINASE KINASE KINASES; ORGANOPLATINUM COMPOUNDS; OVARIAN NEOPLASMS;

EID: 84898457102     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.02.016     Document Type: Article

References (55)

1. Vaughan S., Coward J.I., Bast R.C., Berchuck A., Berek J.S., Brenton J.D., Coukos G., Crum C.C., Drapkin R., Etemadmoghadam D., Friedlander M., Gabra H., Kaye S.B., Lord C.J., Lengyel E., Levine D.A., McNeish I.A., Menon U., Mills G.B., Nephew K.P., Oza A.M., Sood A.K., Stronach E.A., Walczak H., Bowtell D.D., Balkwill F.R. Rethinking ovarian cancer: recommendations for improving outcomes. Nat. Rev. Cancer 2011, 11:719-725.
2. Markman M. Antineoplastic agents in the management of ovarian cancer: current status and emerging therapeutic strategies. Trends Pharmacol. Sci. 2008, 29:515-519.
3. Cossa G., Gatti L., Zunino F., Perego P. Strategies to improve the efficacy of platinum compounds. Curr. Med. Chem. 2009, 16:2355-2365.
4. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
5. Cossa G., Gatti L., Cassinelli G., Lanzi C., Zaffaroni N., Perego P. Modulation of sensitivity to antitumor agents by targeting the MAPK survival pathway. Curr. Pharm. Des. 2013, 19:883-894.
6. Cassinelli G., Zuco V., Gatti L., Lanzi C., Zaffaroni N., Colombo D., Perego P. Targeting the Akt kinase to modulate drug resistance of cancer cells. Curr. Med. Chem. 2013, 20:1923-1945.
7. Nunes-Xavier C., Romá-Mateo C., Ríos P., Tárrega C., Cejudo-Marín R., Tabernero L., Pulido R. Dual-specificity MAP kinase phosphatases as targets of cancer treatment. Anticancer Agents Med. Chem. 2011, 11:109-132.
8. Ohren J.F., Chen H., Pavlovsky A., Whitehead C., Zhang E., Kuffa P., Yan C., McConnell P., Spessard C., Banotai C., Mueller W.T., Delaney A., Omer C., Sebolt-Leopold J., Dudley D.T., Leung I.K., Flamme C., Warmus J., Kaufman M., Barrett S., Tecle H., Hasemann C.A. Structures of human MAP kinase kinase 1 (MEK1) and MEK2 describe novel noncompetitive kinase inhibition. Nat. Struct. Mol. Biol. 2004, 11:1192-1197.
9. Opar A. New class of kinase inhibitors poised to join the anticancer arsenal. Nat. Rev. Drug Discov. 2012, 11:819-820.
10. Brozovic A., Osmak M. Activation of mitogen-activated protein kinases by cisplatin and their role in cisplatin-resistance. Cancer Lett. 2007, 251:1-16.
11. Cagnol S., Chambard J.C. ERK and cell death: mechanisms of ERK-induced cell death-apoptosis, autophagy and senescence. FEBS J. 2010, 277:2-21.
12. Benedetti V., Perego P., Luca Beretta G., Corna E., Tinelli S., Righetti S.C., Leone R., Apostoli P., Lanzi C., Zunino F. Modulation of survival pathways in ovarian carcinoma cell lines resistant to platinum compounds. Mol. Cancer Ther. 2008, 7:679-687.
13. Macleod K., Mullen P., Sewell J., Rabiasz G., Lawrie S., Miller E., Smyth J.F., Langdon S.P. Altered ErbB receptor signaling and gene expression in cisplatin-resistant ovarian cancer. Cancer Res. 2005, 65:6789-6800.
14. Ohta T., Ohmichi M., Shibuya T., Takahashi T., Tsutsumi S., Takahashi K., Kurachi H. Gefitinib (ZD1839) increases the efficacy of cisplatin in ovarian cancer cells. Cancer Biol. Ther. 2012, 13:408-416.
15. Yue P., Zhang X., Paladino D., Sengupta B., Ahmad S., Holloway R.W., Ingersoll S.B., Turkson J. Hyperactive EGF receptor, Jaks and Stat3 signaling promote enhanced colony-forming ability, motility and migration of cisplatin-resistant ovarian cancer cells. Oncogene 2012, 31:2309-2322.
16. van der Vos K.E., Coffer P.J. The extending network of FOXO transcriptional target genes. Antioxid. Redox Signal. 2011, 14:579-592.
17. Yang J.Y., Zong C.S., Xia W., Yamaguchi H., Ding Q., Xie X., Lang J.Y., Lai C.C., Chang C.J., Huang W.C., Huang H., Kuo H.P., Lee D.F., Li L.Y., Lien H.C., Cheng X., Chang K.J., Hsiao C.D., Tsai F.J., Tsai C.H., Sahin A.A., Muller W.J., Mills G.B., Yu D., Hortobagyi G.N., Hung M.C. ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat. Cell Biol. 2008, 10:138-148.
18. Zhang X., Gan L., Pan H., Guo S., He X., Olson S.T., Mesecar A., Adam S., Unterman T.G. Phosphorylation of serine 256 suppresses transactivation by FKHR (FOXO1) by multiple mechanisms. Direct and indirect effects on nuclear/cytoplasmic shuttling and DNA binding. J. Biol. Chem. 2002, 277:45276-45284.
19. Chiang C.W., Kanies C., Kim K.W., Fang W.B., Parkhurst C., Xie M., Henry T., Yang E. Protein phosphatase 2A dephosphorylation of phosphoserine 112 plays the gatekeeper role for BAD-mediated apoptosis. Mol. Cell Biol. 2003, 23:6350-6362.
20. Lomonosova E., Chinnadurai G. BH3-only proteins in apoptosis and beyond: an overview. Oncogene 2008, 27(Suppl 1):S2-S19.
21. You H., Pellegrini M., Tsuchihara K., Yamamoto K., Hacker G., Erlacher M., Villunger A., Mak T.W. FOXO3a-dependent regulation of Puma in response to cytokine/growth factor withdrawal. J. Exp. Med. 2006, 203:1657-1663.
22. Perego P., Romanelli S., Carenini N., Magnani I., Leone R., Bonetti A., Paolicchi A., Zunino F. Ovarian cancer cisplatin-resistant cell lines: multiple changes including collateral sensitivity to Taxol. Ann. Oncol. 2008, 9:423-430.
23. Perego P., Giarola M., Righetti S.C., Supino R., Caserini C., Delia D., Pierotti M.A., Miyashita T., Reed J.C., Zunino F. Association between cisplatin resistance and mutation of p53 gene and reduced bax expression in ovarian carcinoma cell systems. Cancer Res. 1996, 56:556-562.
24. Perego P., Righetti S.C., Supino R., Delia D., Caserini C., Carenini N., Bedogné B., Broome E., Krajewski S., Reed J.C., Zunino F. Role of apoptosis and apoptosis-related proteins in the cisplatin-resistant phenotype of human tumor cell lines. Apoptosis 1997, 2:540-548.
25. Beretta G.L., Benedetti V., Cossa G., Assaraf Y.G., Bram E., Gatti L., Corna E., Carenini N., Colangelo D., Howell S.B., Zunino F., Perego P. Increased levels and defective glycosylation of MRPs in ovarian carcinoma cells resistant to oxaliplatin. Biochem. Pharmacol. 2010, 79:1108-1117.
26. Rinehart J., Adjei A.A., Lorusso P.M., Waterhouse D., Hecht J.R., Natale R.B., Hamid O., Varterasian M., Asbury P., Kaldjian E.P., Gulyas S., Mitchell D.Y., Herrera R., Sebolt-Leopold J.S., Meyer M.B. Multicenter phase II study of the oral MEK inhibitor, CI-1040, in patients with advanced non-small-cell lung, breast, colon, and pancreatic cancer. J. Clin. Oncol. 2004, 22:4456-4462.
27. Skehan P., Storeng R., Scudiero D., Monks A., McMahon J., Vistica D., Warren J.T., Bokesch H., Kenney S., Boyd M.R. New colorimetric cytotoxicity assay for anticancer-drug screening. J. Natl. Cancer Inst. 1990, 82:1107-1112.
28. Chou T.C., Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul. 1984, 22:27-55.
29. Peters G.J., van der Wilt C.L., van Moorsel C.J., Kroep J.R., Bergman A.M., Ackland S.P. Basis for effective combination cancer chemotherapy with antimetabolites. Pharmacol. Ther. 2000, 87:227-253.
30. Stommel J.M., Marchenko N.D., Jimenez G.S., Moll U.M., Hope T.J., Wahl G.M. A leucine-rich nuclear export signal in the p53 tetramerization domain: regulation of subcellular localization and p53 activity by NES masking. EMBO J. 1999, 18:1660-1672.
31. Perego P., Cossa G., Tinelli S., Corna E., Carenini N., Gatti L., De Cesare M., Ciusani E., Zunino F., Luison E., Canevari S., Zaffaroni N., Beretta G.L. Role of tyrosyl-DNA phosphodiesterase 1 and inter-players in regulation of tumour cell sensitivity to topoisomerase I inhibition. Biochem. Pharmacol. 2012, 83:27-36.
32. Cancer Genome Atlas Research Network Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474(7353):609-615.
33. Anjum R., Blenis J. The RSK family of kinases: emerging roles in cellular signalling. Nat. Rev. Mol. Cell Biol. 2008, 9:747-758.
34. Hayakawa J., Ohmichi M., Kurachi H., Kanda Y., Hisamoto K., Nishio Y., Adachi K., Tasaka K., Kanzaki T., Murata Y. Inhibition of BAD phosphorylation either at serine 112 via extracellular signal-regulated protein kinase cascade or at serine 136 via Akt cascade sensitizes human ovarian cancer cells to cisplatin. Cancer Res. 2000, 60:5988-5994.
35. Marchion D.C., Cottrill H.M., Xiong Y., Chen N., Bicaku E., Fulp W.J., Bansal N., Chon H.S., Stickles X.B., Kamath S.G., Hakam A., Li L., Su D., Moreno C., Judson P.L., Berchuck A., Wenham R.M., Apte S.M., Gonzalez-Bosquet J., Bloom G.C., Eschrich S.A., Sebti S., Chen D.T., Lancaster J.M. BAD phosphorylation determines ovarian cancer chemosensitivity and patient survival. Clin. Cancer Res. 2011, 17:6356-6366.
36. Tzivion G., Hay N. PI3K-AKT-FoxO axis in cancer and aging. Biochim. Biophys. Acta 2011, 1813:1925.
37. Yuan Z., Cao K., Lin C., Li L., Liu H.Y., Zhao X.Y., Liu L., Deng H.X., Li J., Nie C.L., Wei Y.Q. The p53 upregulated modulator of apoptosis (PUMA) chemosensitizes intrinsically resistant ovarian cancer cells to cisplatin by lowering the threshold set by Bcl-x(L) and Mcl-1. Mol. Med. 2011, 17:1262-1274.
38. Ueda K., Arakawa H., Nakamura Y. Dual-specificity phosphatase 5 (DUSP5) as a direct transcriptional target of tumor suppressor p53. Oncogene 2003, 22:5586-5591.
39. Seifert A., Taubert H., Hombach-Klonisch S., Fischer B., Navarrete A. Santos, TCDD mediates inhibition of p53 and activation of ERalpha signaling in MCF-7 cells at moderate hypoxic conditions. Int. J. Oncol. 2009, 35:417-424.
40. Chan D.W., Liu V.W., Tsao G.S., Yao K.M., Furukawa T., Chan K.K., Ngan H.Y. Loss of MKP3 mediated by oxidative stress enhances tumorigenicity and chemoresistance of ovarian cancer cells. Carcinogenesis 2008, 29:1742-1750.
41. Lorusso P.M., Adjei A.A., Varterasian M., Gadgeel S., Reid J., Mitchell D.Y., Hanson L., DeLuca P., Bruzek L., Piens J., Asbury P., Van Becelaere K., Herrera R., Sebolt-Leopold J., Meyer M.B. Phase I and pharmacodynamic study of the oral MEK inhibitor CI-1040 in patients with advanced malignancies. J. Clin. Oncol. 2005, 23:5281-5293.
42. Dry J.R., Pavey S., Pratilas C.A., Harbron C., Runswick S., Hodgson D., Chresta C., McCormack R., Byrne N., Cockerill M., Graham A., Beran G., Cassidy A., Haggerty C., Brown H., Ellison G., Dering J., Taylor B.S., Stark M., Bonazzi V., Ravishankar S., Packer L., Xing F., Solit D.B., Finn R.S., Rosen N., Hayward N.K., French T., Smith P.D. Transcriptional pathway signatures predict MEK addiction and response to selumetinib (AZD6244). Cancer Res. 2010, 70:2264-2273.
43. Rahman M.T., 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.
44. Yeh P.Y., Chuang S.E., Yeh K.H., Song Y.C., Ea C.K., Cheng A.L. 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.
45. Yeh P.Y., Yeh K.H., Chuang S.E., Song Y.C., Cheng A.L. Suppression of MEK/ERK signaling pathway enhances cisplatin-induced NF-kappaB activation by protein phosphatase 4-mediated NF-kappaB p65 Thr dephosphorylation. J. Biol. Chem. 2004, 279:26143-26148.
46. Wang X., Martindale J.L., Holbrook N.J. Requirement for ERK activation in cisplatin-induced apoptosis. J. Biol. Chem. 2000, 275:39435-39443.
47. Lee E.K., Regenold W.T., Shapiro P. Inhibition of aldose reductase enhances HeLa cell sensitivity to chemotherapeutic drugs and involves activation of extracellular signal-regulated kinases. Anticancer Drugs 2002, 13:859-868.
48. Schweyer S., Soruri A., Meschter O., Heintze A., Zschunke F., Miosge N., Thelen P., Schlott T., Radzun H.J., Fayyazi A. Cisplatin-induced apoptosis in human malignant testicular germ cell lines depends on MEK/ERK activation. Br. J. Cancer 2004, 91:589-598.
49. Fung M.K., Cheung H.W., Ling M.T., Cheung A.L., Wong Y.C., 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.
50. Nonaka M., Itamochi H., Kawaguchi W., Kudoh A., Sato S., Uegaki K., Naniwa J., Sato S., Shimada M., Oishi T., Terakawa N., Kigawa J., Harada T. Activation of the mitogen-activated protein kinase kinase/extracellular signal-regulated kinase pathway overcomes cisplatin resistance in ovarian carcinoma cells. Int. J. Gynecol. Cancer 2012, 22:922-929.
51. Lee S., Yoon S., Kim D.H. A high nuclear basal level of ERK2 phosphorylation contributes to the resistance of cisplatin-resistant human ovarian cancer cells. Gynecol. Oncol. 2007, 104:338-344.
52. Persons D.L., Yazlovitskaya E.M., Cui W., Pelling J.C. Cisplatin-induced activation of mitogen-activated protein kinases in ovarian carcinoma cells: inhibition of extracellular signal-regulated kinase activity increases sensitivity to cisplatin. Clin. Cancer Res. 1999, 5:1007-1014.
53. Latifi A., Abubaker K., Castrechini N., Ward A.C., Liongue C., Dobill F., Kumar J., Thompson E.W., Quinn M.A., Findlay J.K., Ahmed N. Cisplatin treatment of primary and metastatic epithelial ovarian carcinomas generates residual cells with mesenchymal stem cell-like profile. J. Cell. Biochem. 2011, 112:2850-2864.
54. Aoki K., Ogawa T., Ito Y., Nakashima S. Cisplatin activates survival signals in UM-SCC-23 squamous cell carcinoma and these signal pathways are amplified in cisplatin-resistant squamous cell carcinoma. Oncol. Rep. 2004, 11:375-379.
55. Ramos A.M., Fernandez C., Amrán D., Esteban D., de Blas E., Palacios M.A., Aller P. Pharmacologic inhibitors of extracellular signal-regulated kinase (ERKs) and c-Jun NH(2)-terminal kinase (JNK) decrease glutathione content and sensitize human promonocytic leukemia cells to arsenic trioxide-induced apoptosis. J. Cell. Physiol. 2006, 209:1006-1015.