MKP1 mediates chemosensitizer effects of E1a in response to cisplatin in non-small cell lung carcinoma cell

Oncotarget

Volumn 6, Issue 42, 2015, Pages 44095-44107

  Cimas, Francisco ^a   Callejas Valera, Juan ^b   Pascual Serra, Raquel ^a   García Cano, Jesus ^a   Garcia Gil, Elena ^a   De La Cruz Morcillo, Miguel ^a   Ortega Muelas, Marta ^a   Serrano Oviedo, Leticia ^a   Silvio Gutkind, J ^b   Sánchez Prieto, Ricardo ^a  

^a University of Castilla La Mancha   (Spain)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Chemotherapy; Cisplatin; E1a; Lung cancer; MKP1

Indexed keywords

CISPLATIN; E1A PROTEIN; LENTIVIRUS VECTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; ANTINEOPLASTIC AGENT; DUSP1 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1;

APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER RESISTANCE; CONTROLLED STUDY; DRUG SENSITIVITY; HUMAN; HUMAN CELL; LUNG CANCER CELL LINE; NON SMALL CELL LUNG CANCER; PROTEIN EXPRESSION; UPREGULATION; CARCINOMA, NON-SMALL-CELL LUNG; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECTS; DRUG RESISTANCE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; LUNG NEOPLASMS; METABOLISM; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTOR; TUMOR CELL LINE;

ADENOVIRUS E1A PROTEINS; ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; DUAL SPECIFICITY PHOSPHATASE 1; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; LUNG NEOPLASMS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 84953394606     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6574     Document Type: Article

References (65)

1. Chakraborty AA, Tansey WP. Adenoviral E1A function through Myc. Cancer Res. 2009; 69:6-9.
2. Yu D, Hamada J, Zhang H, Nicolson GL, Hung MC. Mechanisms of c-erbB2/neu oncogene-induced metastasis and repression of metastatic properties by adenovirus 5 E1A gene products. Oncogene. 1992; 7:2263-2270.
3. Deng J, Xia W, Hung MC. Adenovirus 5 E1A-mediated tumor suppression associated with E1A-mediated apoptosis in vivo. Oncogene. 1998; 17:2167-2175.
4. Chang YW, Hung MC, Su JL. The anti-tumor activity of E1A and its implications in cancer therapy. Arch Immunol Ther Exp. 2014; 62:195-204.
5. Frisch SM, Mymryk JS. Adenovirus-5 E1A: paradox and paradigm. Nat Rev Mol Cell Biol. 2002; 3:441-452.
6. Sanchez-Prieto R, Quintanilla M, Cano A, Leonart ML, Martin P, Anaya A, Cajal S. Carcinoma cell lines become sensitive to DNA-damaging agents by the expression of the adenovirus E1A gene. Oncogene. 1996; 13:1083-1092.
7. Yamaguchi H, Chen CT, Chou CK, Pal A, Bornmann W, Hortobagyi GN, Hung MC. Adenovirus 5 E1A enhances histone deacetylase inhibitors-induced apoptosis through Egr-1-mediated Bim upregulation. Oncogene. 2010; 29:5619-5629.
8. Stiewe T, Parssanedjad K, Esche H, Opalka B, Putzer BM. E1A overcomes the apoptosis block in BCR-ABL+ leukemia cells, renders cells susceptible to induction of apoptosis by chemotherapeutic agents. Cancer Res. 2000; 60:3957-3964.
9. Valero ML, Cimas FJ, Arias L, Melgar-Rojas P, Garcia E, Callejas-Valera JL, Garcia-Cano J, Serrano-Oviedo L, de la Cruz-Morcillo MA, Sanchez-Perez I, Sanchez-Prieto R. E1a promotes c-Myc-dependent replicative stress: implications in glioblastoma radiosensitization. Cell Cycle. 2014; 13:52-61.
10. Viniegra JG, Losa JH, Sanchez-Arevalo VJ, Parada CC, Soria VM, Cajal S, Sanchez-Prieto R. Modulation of PI3K/Akt pathway by E1a mediates sensitivity to cisplatin. Oncogene. 2002; 21:7131-7136.
11. Liao Y, Hung MC. Regulation of the activity of p38 mitogen-activated protein kinase by Akt in cancer and adenoviral protein E1A-mediated sensitization to apoptosis. Mol Cell Biol. 2003; 23:6836-6848.
12. Stanchina de E, McCurrach ME, Zindy F, Shieh SY, Ferbeyre G, Samuelson AV, Prives C, Roussel MF, Sherr CJ, Lowe SW. E1A signaling to p53 involves the p19(ARF) tumor suppressor. Genes Dev. 1998; 12:2434-2442.
13. Li Z, Day CP, Yang JY, Tsai WB, Lozano G, Shih HM, Hung MC. Adenoviral E1A targets Mdm4 to stabilize tumor suppressor p53. Cancer Res. 2004; 64:9080-9085.
14. Sanchez-Prieto R, Lleonart M, Ramony Cajal S. Lack of correlation between p53 protein level and sensitivity of DNA-damaging agents in keratinocytes carrying adenovirus E1a mutants. Oncogene. 1995; 11:675-682.
15. Samuelson AV, Lowe SW. Selective induction of p53 and chemosensitivity in RB-deficient cells by E1A mutants unable to bind the RB-related proteins. Proc Natl Acad Sci USA. 1997; 94:12094-12099.
16. Ueno NT, Bartholomeusz C, Herrmann JL, Estrov Z, Shao R, reeff M, Price J, Paul RW, Anklesaria P, Yu D, Hung MC. E1A-mediated paclitaxel sensitization in HER-2/neu-overexpressing ovarian cancer SKOV3.ip1 through apoptosis involving the caspase-3 pathway. Clin Cancer Res. 2000; 6:250-259.
17. Putzer BM, Stiewe T, Parssanedjad K, Rega S, Esche H. E1A is sufficient by itself to induce apoptosis independent of p53 and other adenoviral gene products. Cell Death Differ. 2000; 7:177-188.
18. McCurrach ME, Connor TM, Knudson CM, Korsmeyer SJ, Lowe SW. bax-deficiency promotes drug resistance and oncogenic transformation by attenuating p53-dependent apoptosis. Proc Natl Acad of Sci USA. 1997; 94:2345-2349.
19. Liao Y, Hung MC. A new role of protein phosphatase 2a in adenoviral E1A protein-mediated sensitization to anticancer drug-induced apoptosis in human breast cancer cells. Cancer Res. 2004; 64:5938-5942.
20. Callejas-Valera JL, Guinea-Viniegra J, Ramirez-Castillejo C, Recio JA, Galan-Moya E, Martinez N, Rojas JM, Cajal S, Sanchez-Prieto R. E1a gene expression blocks the ERK1/2 signaling pathway by promoting nuclear localization and MKP up-regulation: implication in v-H-Ras-induced senescence. J Biol Chem. 2008; 283:13450-13458.
21. Romanov VS, Brichkina AI, Morrison H, Pospelova TV, Pospelov VA, Herrlich P. Novel mechanism of JNK pathway activation by adenoviral E1A. Oncotarget. 2014; 5:2176-2186.
22. Mountzios G, Dimopoulos MA, Soria JC, Sanoudou D, Papadimitriou CA. Histopathologic and genetic alterations as predictors of response to treatment and survival in lung cancer: a review of published data. Crit Rev Oncol Hematol. 2010; 75:94-109.
23. Ishida S, McCormick F, Smith-McCune K, Hanahan D. Enhancing tumor-specific uptake of the anticancer drug cisplatin with a copper chelator. Cancer Cell. 2010; 17:574-583.
24. Girnun GD, Chen L, Silvaggi J, Drapkin R, Chirieac LR, Padera RF, Upadhyay R, Vafai SB, Weissleder R, Mahmood U, Naseri E, Buckley S, Li D, et al. Regression of drug-resistant lung cancer by the combination of rosiglitazone and carboplatin. Clinical cancer research: an official journal of the American Association for Clin Cancer Res. 2008; 14:6478-6486.
25. Girnun GD, Naseri E, Vafai SB, Qu L, Szwaya JD, Bronson R, Alberta JA, Spiegelman BM. Synergy between PPARgamma ligands and platinum-based drugs in cancer. Cancer Cell. 2007; 11:395-406.
26. Fang JY, Richardson BC. The MAPK signalling pathways and colorectal cancer. Lancet Oncol. 2005; 6:322-327.
27. Lochhead PA, Gilley R, Cook SJ. ERK5 and its role in tumour development. Biochem Soc Trans. 2012; 40:251-256.
28. Huang CY, Tan TH. DUSPs, to MAP kinases and beyond. Cell Biosci. 2012; 2:24.
29. Vicent S, Garayoa M, Lopez-Picazo JM, Lozano MD, Toledo G, Thunnissen FB, Manzano RG, Montuenga LM. Mitogen-activated protein kinase phosphatase-1 is overexpressed in non-small cell lung cancer and is an independent predictor of outcome in patients. Clin Cancer Res. 2004; 10:3639-3649.
30. Blanco R, Iwakawa R, Tang M, Kohno T, Angulo B, Pio R, Montuenga LM, Minna JD, Yokota J, Sanchez-Cespedes M. A gene-alteration profile of human lung cancer cell lines. Hum Mutat. 2009; 30:1199-1206.
31. Caserta TM, Smith AN, Gultice AD, Reedy MA, Brown TL. Q-VD-OPh, a broad spectrum caspase inhibitor with potent antiapoptotic properties. Apoptosis. 2003; 8:345-352.
32. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012; 8:445-544.
33. Brozovic A, Osmak M. Activation of mitogen-activated protein kinases by cisplatin and their role in cisplatin-resistance. Cancer Lett. 2007; 251:1-16.
34. Chattopadhyay S, Machado-Pinilla R, Manguan-Garcia C, Belda-Iniesta C, Moratilla C, Cejas P, Fresno-Vara JA, de Castro-Carpeno J, Casado E, Nistal M, Gonzalez-Baron M, Perona R. MKP1/CL100 controls tumor growth and sensitivity to cisplatin in non-small-cell lung cancer. Oncogene. 2006; 25:3335-3345.
35. Beltman J, McCormick F, Cook SJ. The selective protein kinase C inhibitor, Ro-31-8220, inhibits mitogen-activated protein kinase phosphatase-1 (MKP-1) expression, induces c-Jun expression, and activates Jun N-terminal kinase. J Biol Chem. 1996; 271:27018-27024.
36. Pang L, Sawada T, Decker SJ, Saltiel AR. Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J Biol Chem. 1995; 270:13585-13588.
37. Cuenda A, Rouse J, Doza YN, Meier R, Cohen P, Gallagher TF, Young PR, Lee JC. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 1995; 364:229-233.
38. Brader KR, Wolf JK, Hung MC, Yu D, Crispens MA, van Golen KL, Price JE. Adenovirus E1A expression enhances the sensitivity of an ovarian cancer cell line to multiple cytotoxic agents through an apoptotic mechanism. Clin Cancer Res. 1997; 3:2017-2024.
39. Rusch V, Klimstra D, Venkatraman E, Oliver J, Martini N, Gralla R, Kris M, Dmitrovsky E. Aberrant p53 expression predicts clinical resistance to cisplatin-based chemotherapy in locally advanced non-small cell lung cancer. Cancer Res. 1995; 55:5038-5042.
40. Mandic R, Schamberger CJ, Muller JF, Geyer M, Zhu L, Carey TE, Grenman R, Dunne AA, Werner JA. Reduced cisplatin sensitivity of head and neck squamous cell carcinoma cell lines correlates with mutations affecting the COOH-terminal nuclear localization signal of p53. Clin Cancer Res. 2005; 11:6845-6852.
41. Perrone F, Bossi P, Cortelazzi B, Locati L, Quattrone P, Pierotti MA, Pilotti S, Licitra L. TP53 mutations and pathologic complete response to neoadjuvant cisplatin and fluorouracil chemotherapy in resected oral cavity squamous cell carcinoma. J Clin Oncol. 2010; 28:761-766.
42. Tsao MS, Aviel-Ronen S, Ding K, Lau D, Liu N, Sakurada A, Whitehead M, Zhu CQ, Livingston R, Johnson DH, Rigas J, Seymour L, Winton T, Shepherd FA. Prognostic and predictive importance of p53 and RAS for adjuvant chemotherapy in non small-cell lung cancer. J Clin Oncol. 2007; 25:5240-5247.
43. Aviel-Ronen S, Blackhall FH, Shepherd FA, Tsao MS. K-ras mutations in non-small-cell lung carcinoma: a review. Clin Lung Cancer. 2006; 8:30-38.
44. Sklar MD. Increased resistance to cis-diamminedichloro platinum(II) in NIH 3T3 cells transformed by ras oncogenes. Cancer Res. 1988; 48:793-797.
45. Yoon YK, Kim HP, Han SW, Oh do Y, Im SA, Bang YJ, Kim TY. KRAS mutant lung cancer cells are differentially responsive to MEK inhibitor due to AKT or STAT3 activation: implication for combinatorial approach. Mol Carcinog. 2010; 49:353-362.
46. Denkert C, Schmitt WD, Berger S, Reles A, Pest S, Siegert A, Lichtenegger W, Dietel M, Hauptmann S. Expression of mitogen-activated protein kinase phosphatase-1 (MKP-1) in primary human ovarian carcinoma. Int J Cancer. 2002; 102:507-513.
47. Sanchez-Perez I, Martinez-Gomariz M, Williams D, Keyse SM, Perona R. CL100/MKP-1 modulates JNK activation and apoptosis in response to cisplatin. Oncogene. 2000; 19:5142-5152.
48. Wang J, Zhou JY, Zhang L, Wu GS. Involvement of MKP-1 and Bcl-2 in acquired cisplatin resistance in ovarian cancer cells. Cell Cycle. 2009; 8:3191-3198.
49. Wang Z, Xu J, Zhou JY, Liu Y, Wu GS. Mitogen-activated protein kinase phosphatase-1 is required for cisplatin resistance. Cancer Res. 2006; 66:8870-8877.
50. Pereira L, Igea A, Canovas B, Dolado I, Nebreda AR. Inhibition of p38 MAPK sensitizes tumour cells to cisplatin-induced apoptosis mediated by reactive oxygen species and JNK. EMBO Mol Med. 2013; 5:1759-1774.
51. Bartholomeusz C, Itamochi H, Nitta M, Saya H, Ginsberg MH, Ueno NT. Antitumor effect of E1A in ovarian cancer by cytoplasmic sequestration of activated ERK by PEA15. Oncogene. 2006; 25:79-90.
52. Wang X, Martindale JL, Holbrook NJ. Requirement for ERK activation in cisplatin-induced apoptosis. J Biol Chem. 2000; 275:39435-39443.
53. Wu DW, Wu TC, Wu JY, Cheng YW, Chen YC, Lee MC, Chen CY, Lee H. Phosphorylation of paxillin confers cisplatin resistance in non-small cell lung cancer via activating ERK-mediated Bcl-2 expression. Oncogene. 2014; 33:4385-4395.
54. Li Y, Ahmed F, Ali S, Philip PA, Kucuk O, Sarkar FH. Inactivation of nuclear factor kappaB by soy isoflavone genistein contributes to increased apoptosis induced by chemotherapeutic agents in human cancer cells. Cancer Res. 2005; 65:6934-6942.
55. Ruan HY, Masuda M, Ito A, Umezawa K, Nakashima T, Yasumatsu R, Kuratomi Y, Yamamoto T, Weinstein IB, Komune S. Effects of a novel NF-kappaB inhibitor, dehydroxymethylepoxyquinomicin (DHMEQ), on growth, apoptosis, gene expression, and chemosensitivity in head and neck squamous cell carcinoma cell lines. Head Neck. 2006; 28:158-165.
56. Yang SF, Zhuang TF, Si YM, Qi KY, Zhao J. Coriolus versicolor mushroom polysaccharides exert immunoregulatory effects on mouse B cells via membrane Ig and TLR-4 to activate the MAPK and NF-kappaB signaling pathways. Mol Immunol. 2015; 64:144-151.
57. Shao R, Karunagaran D, Zhou BP, Li K, Lo SS, Deng J, Chiao P, Hung MC. Inhibition of nuclear factor-kappaB activity is involved in E1A-mediated sensitization of radiation-induced apoptosis. J Biol Chem. 1997; 272:32739-32742.
58. Gil-Araujo B, Toledo Lobo MV, Gutierrez-Salmeron M, Gutierrez-Pitalua J, Ropero S, Angulo JC, Chiloeches A, Lasa M. Dual specificity phosphatase 1 expression inversely correlates with NF-kappaB activity and expression in prostate cancer and promotes apoptosis through a p38 MAPK dependent mechanism. Mol Oncol. 2014; 8:27-38.
59. Wang Q, Shi S, He W, Padilla MT, Zhang L, Wang X, Zhang B, Lin Y. Retaining MKP1 expression and attenuating JNK-mediated apoptosis by RIP1 for cisplatin resistance through miR-940 inhibition. Oncotarget. 2014; 5:1304-1314.
60. Maraver A, Fernandez-Marcos PJ, Herranz D, Canamero M, Munoz-Martin M, Gomez-Lopez G, Mulero F, Megias D, Sanchez-Carbayo M, Shen J, Sanchez-Cespedes M, Palomero T, Ferrando A, et al. Therapeutic effect of gamma-secretase inhibition in KrasG12V-driven non-small cell lung carcinoma by derepression of DUSP1 and inhibition of ERK. Cancer Cell. 2012; 22:222-234.
61. Kaminskyy VO, Piskunova T, Zborovskaya IB, Tchevkina EM, Zhivotovsky B. Suppression of basal autophagy reduces lung cancer cell proliferation and enhances caspase-dependent and -independent apoptosis by stimulating ROS formation. Autophagy. 2012; 8:1032-1044.
62. Garcia-Cano J, Ambroise G, Pascual-Serra R, Carrion MC, Serrano-Oviedo L, Ortega-Muelas M, Cimas FJ, Sabater S, Ruiz-Hidalgo MJ, Sanchez Perez I, Mas A, Jalon FA, Vazquez A, et al. Exploiting the potential of autophagy in cisplatin therapy: A new strategy to overcome resistance. Oncotarget. 2015.
63. Rodriguez-Rocha H, Gomez-Gutierrez JG, Garcia-Garcia A, Rao XM, Chen L, McMasters KM, Zhou HS. Adenoviruses induce autophagy to promote virus replication and oncolysis. Virology. 2011; 416:9-15.
64. Galan-Moya EM, de la Cruz-Morcillo MA, Llanos Valero M, Callejas-Valera JL, Melgar-Rojas P, Hernadez Losa J, Salcedo M, Fernandez-Aramburo A, Ramon y Cajal S, Sanchez-Prieto R. Balance between MKK6 and MKK3 mediates p38 MAPK associated resistance to cisplatin in NSCLC. PloS one. 2011; 6:e28406.
65. de la Cruz-Morcillo MA, Valero ML, Callejas-Valera JL, Arias-Gonzalez L, Melgar-Rojas P, Galan-Moya EM, Garcia-Gil E, Garcia-Cano J, Sanchez-Prieto R. P38MAPK is a major determinant of the balance between apoptosis and autophagy triggered by 5-fluorouracil: implication in resistance. Oncogene. 2012; 31:1073-1085.