Oxaliplatin activates the Keap1/Nrf2 antioxidant system conferring protection against the cytotoxicity of anticancer drugs

Free Radical Biology and Medicine

Volumn 70, Issue , 2014, Pages 68-77

  Wang, Xiu Jun ^a   Li, Yinyan ^a   Luo, Lin ^a   Wang, Hongyan ^a   Chi, Zhexu ^a   Xin, Ai ^a   Li, Xin ^a   Wu, Jiaguo ^b   Tang, Xiuwen ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

Antioxidant enzymes; Chemoresistance; Colon cancer cells; Free radicals; Nrf2; Oxaliplatin

Indexed keywords

ACTIN; ANTIOXIDANT; CARBOPLATIN; CISPLATIN; DICHLORO(1,2 DIAMINOCYCLOHEXANE); DRUG METABOLITE; ETOPOSIDE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; HEME OXYGENASE 1; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 3; OXALIPLATIN; PLATINUM DERIVATIVE; PROTEIN; PROTEIN AKR1C1; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CYTOSKELETON PROTEIN; FREE RADICAL; KEAP1 PROTEIN, MOUSE; NFE2L2 PROTEIN, MOUSE; PLATINUM COMPLEX; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CANCER CELL CULTURE; CELL PROTECTION; CHEMOSENSITIVITY; CONTROLLED STUDY; CYTOTOXICITY; GENE ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; LARGE INTESTINE; LUNG NON SMALL CELL CANCER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SOMATIC MUTATION; UPREGULATION; WILD TYPE; ANIMAL; BIOSYNTHESIS; COLONIC NEOPLASMS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTINEOPLASTIC AGENTS; ANTIOXIDANT RESPONSE ELEMENTS; ANTIOXIDANTS; COLONIC NEOPLASMS; CYTOSKELETAL PROTEINS; FREE RADICALS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; NF-E2-RELATED FACTOR 2; ORGANOPLATINUM COMPOUNDS; SIGNAL TRANSDUCTION;

EID: 84896123587     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.02.010     Document Type: Article

References (52)

1. T. Andre, C. Boni, L. Mounedji-Boudiaf, M. Navarro, J. Tabernero, T. Hickish, C. Topham, M. Zaninelli, P. Clingan, J. Bridgewater, I. Tabah-Fisch, and A. de Gramont Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer N. Engl. J. Med. 350 2004 2343 2351 (Pubitemid 38702845)
2. D.E. Baker Oxaliplatin: a new drug for the treatment of metastatic carcinoma of the colon or rectum Rev. Gastroenterol. Disord 3 2003 31 38 (Pubitemid 36335935)
3. D. Screnci, M.J. McKeage, P. Galettis, T.W. Hambley, B.D. Palmer, and B.C. Baguley Relationships between hydrophobicity, reactivity, accumulation and peripheral nerve toxicity of a series of platinum drugs Br. J. Cancer 82 2000 966 972 (Pubitemid 30085253)
4. J.J. Marin, M.R. Romero, A.G. Blazquez, E. Herraez, E. Keck, and O. Briz Importance and limitations of chemotherapy among the available treatments for gastrointestinal tumours Anticancer Agents Med. Chem 9 2009 162 184
5. H. Masuda, R.F. Ozols, G.M. Lai, A. Fojo, M. Rothenberg, and T.C. Hamilton Increased DNA repair as a mechanism of acquired resistance to cis-diamminedichloroplatinum(II) in human ovarian cancer cell lines Cancer Res. 48 1988 5713 5716
6. R.P. Perez, T.C. Hamilton, and R.F. Ozols Resistance to alkylating agents and cisplatin: insights from ovarian carcinoma model systems Pharmacol. Ther. 48 1990 19 27 (Pubitemid 20322215)
7. V.M. Richon, N. Schulte, and A. Eastman Multiple mechanisms of resistance to cis-diamminedichloroplatinum(II) in murine leukemia L1210 cells Cancer Res. 47 1987 2056 2061 (Pubitemid 17074608)
8. E. Herraez, E. Gonzalez-Sanchez, J. Vaquero, M.R. Romero, M.A. Serrano, J.J. Marin, and O. Briz Cisplatin-induced chemoresistance in colon cancer cells involves FXR-dependent and FXR-independent up-regulation of ABC proteins Mol. Pharm. 9 2012 2565 2576
9. D. Wang, and S.J. Lippard Cellular processing of platinum anticancer drugs Nat. Rev. Drug Discovery 4 2005 307 320 (Pubitemid 41130944)
10. O. Rixe, W. Ortuzar, M. Alvarez, R. Parker, E. Reed, K. Paull, and T. Fojo Oxaliplatin, tetraplatin, cisplatin, and carboplatin: spectrum of activity in drug-resistant cell lines and in the cell lines of the National Cancer Institute×s Anticancer Drug Screen panel Biochem. Pharmacol. 52 1996 1855 1865 (Pubitemid 26419675)
11. A.T. Dinkova-Kostova, W.D. Holtzclaw, R.N. Cole, K. Itoh, N. Wakabayashi, Y. Katoh, M. Yamamoto, and P. Talalay Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants Proc. Natl. Acad. Sci. USA 99 2002 11908 11913 (Pubitemid 34994497)
12. K. Itoh, J. Mimura, and M. Yamamoto Discovery of the negative regulator of Nrf2, Keap1: a historical overview Antioxid. Redox Signaling 13 2010 1665 1678
13. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J.D. Engel, and M. Yamamoto Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev. 13 1999 76 86 (Pubitemid 29045117)
14. M. Kobayashi, L. Li, N. Iwamoto, Y. Nakajima-Takagi, H. Kaneko, Y. Nakayama, M. Eguchi, Y. Wada, Y. Kumagai, and M. Yamamoto The antioxidant defense system Keap1-Nrf2 comprises a multiple sensing mechanism for responding to a wide range of chemical compounds Mol. Cell. Biol. 29 2009 493 502
15. K. Takaya, T. Suzuki, H. Motohashi, K. Onodera, S. Satomi, T.W. Kensler, and M. Yamamoto Validation of the multiple sensor mechanism of the Keap1-Nrf2 system Free Radic. Biol. Med. 53 2012 817 827
16. D.D. Zhang, and M. Hannink Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress Mol. Cell. Biol 23 2003 8137 8151 (Pubitemid 37377505)
17. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, M. Yamamoto, and Y. Nabeshima An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236 1997 313 322 (Pubitemid 27373291)
18. M.S. Yates, and T.W. Kensler Chemopreventive promise of targeting the Nrf2 pathway Drug News Perspect. 20 2007 109 117 (Pubitemid 46917234)
19. A. Hayashi, H. Suzuki, K. Itoh, M. Yamamoto, and Y. Sugiyama Transcription factor Nrf2 is required for the constitutive and inducible expression of multidrug resistance-associated protein 1 in mouse embryo fibroblasts Biochem. Biophys. Res. Commun. 310 2003 824 829 (Pubitemid 37188696)
20. C.M. Mahaffey, H. Zhang, A. Rinna, W. Holland, P.C. Mack, and H.J. Forman Multidrug-resistant protein-3 gene regulation by the transcription factor Nrf2 in human bronchial epithelial and non-small-cell lung carcinoma Free Radic. Biol. Med. 46 2009 1650 1657
21. V. Vollrath, A.M. Wielandt, M. Iruretagoyena, and J. Chianale Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene Biochem. J. 395 2006 599 609
22. J.D. Hayes, and M. McMahon NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer Trends Biochem. Sci. 34 2009 176 188
23. D.M. Townsend, and K.D. Tew The role of glutathione-S-transferase in anti-cancer drug resistance Oncogene 22 2003 7369 7375
24. S. Homma, Y. Ishii, Y. Morishima, T. Yamadori, Y. Matsuno, N. Haraguchi, N. Kikuchi, H. Satoh, T. Sakamoto, N. Hizawa, K. Itoh, and M. Yamamoto Nrf2 enhances cell proliferation and resistance to anticancer drugs in human lung cancer Clin. Cancer Res. 15 2009 3423 3432
25. A. Singh, V. Misra, R.K. Thimmulappa, H. Lee, S. Ames, M.O. Hoque, J.G. Herman, S.B. Baylin, D. Sidransky, E. Gabrielson, M.V. Brock, and S. Biswal Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer PLoS Med. 3 2006 e420
26. X.J. Wang, Z. Sun, N.F. Villeneuve, S. Zhang, F. Zhao, Y. Li, W. Chen, X. Yi, W. Zheng, G.T. Wondrak, P.K. Wong, and D.D. Zhang Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2 Carcinogenesis 29 2008 1235 1243 (Pubitemid 351958704)
27. P. Allain, O. Heudi, A. Cailleux, A. Le Bouil, F. Larra, M. Boisdron-Celle, and E. Gamelin Early biotransformations of oxaliplatin after its intravenous administration to cancer patients Drug Metab. Dispos. 28 2000 1379 1384
28. M. McMahon, K. Itoh, M. Yamamoto, S.A. Chanas, C.J. Henderson, L.I. McLellan, C.R. Wolf, C. Cavin, and J.D. Hayes The Cap×n×Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes Cancer Res. 61 2001 3299 3307 (Pubitemid 32695017)
29. L.G. Higgins, M.O. Kelleher, I.M. Eggleston, K. Itoh, M. Yamamoto, and J.D. Hayes Transcription factor Nrf2 mediates an adaptive response to sulforaphane that protects fibroblasts in vitro against the cytotoxic effects of electrophiles, peroxides and redox-cycling agents Toxicol. Appl. Pharmacol. 237 2009 267 280
30. X.J. Wang, J.D. Hayes, and C.R. Wolf Generation of a stable antioxidant response element-driven reporter gene cell line and its use to show redox-dependent activation of nrf2 by cancer chemotherapeutic agents Cancer Res 66 2006 10983 10994 (Pubitemid 44876998)
31. X.J. Wang, M. Chamberlain, O. Vassieva, C.J. Henderson, and C.R. Wolf Relationship between hepatic phenotype and changes in gene expression in cytochrome P450 reductase (POR) null mice Biochem. J. 388 2005 857 867 (Pubitemid 40941573)
32. X. Tang, H. Wang, L. Fan, X. Wu, A. Xin, and X.J. Wang Luteolin inhibits NRF2 leading to negative regulation of the NRF2/ARE pathway and sensitization of human lung carcinoma A549 cells to therapeutic drugs Free Radic. Biol. Med 50 2011 1599 1609
33. S.A. Chanas, Q. Jiang, M. McMahon, G.K. McWalter, L.I. McLellan, C.R. Elcombe, C.J. Henderson, C.R. Wolf, G.J. Moffat, K. Itoh, M. Yamamoto, and J.D. Hayes Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gsta1, Gsta2, Gstm1, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice Biochem. J. 365 2002 405 416 (Pubitemid 36135312)
34. H. Kamencic, A. Lyon, P.G. Paterson, and B.H. Juurlink Monochlorobimane fluorometric method to measure tissue glutathione Anal. Biochem. 286 2000 35 37
35. H. Wang, K. Liu, M. Geng, P. Gao, X. Wu, Y. Hai, Y. Li, L. Luo, J.D. Hayes, X.J. Wang, and X. Tang RXRalpha inhibits the NRF2-ARE signalling pathway through a direct interaction with the Neh7 domain of NRF2 Cancer Res. 73 2013 3097 3108
36. M.A. Graham, G.F. Lockwood, D. Greenslade, S. Brienza, M. Bayssas, and E. Gamelin Clinical pharmacokinetics of oxaliplatin: a critical review Clin. Cancer Res. 6 2000 1205 1218 (Pubitemid 30226200)
37. E. Kansanen, G. Bonacci, F.J. Schopfer, S.M. Kuosmanen, K.I. Tong, H. Leinonen, S.R. Woodcock, M. Yamamoto, C. Carlberg, S. Yla-Herttuala, B.A. Freeman, and A.L. Levonen Electrophilic nitro-fatty acids activate NRF2 by a KEAP1 cysteine 151-independent mechanism J. Biol. Chem. 286 2011 14019 14027
38. S. Mani, M.A. Graham, D.B. Bregman, P. Ivy, and S.G. Chaney Oxaliplatin: a review of evolving concepts Cancer Invest. 20 2002 246 263 (Pubitemid 34207752)
39. F.R. Luo, S.D. Wyrick, and S.G. Chaney Biotransformations of oxaliplatin in rat blood in vitro J. Biochem. Mol. Toxicol. 13 1999 159 169 (Pubitemid 129705388)
40. M. Sakurai, N. Egashira, T. Kawashiri, T. Yano, H. Ikesue, and R. Oishi Oxaliplatin-induced neuropathy in the rat: involvement of oxalate in cold hyperalgesia but not mechanical allodynia Pain 147 2009 165 174
41. B. Desoize, and C. Madoulet Particular aspects of platinum compounds used at present in cancer treatment Crit. Rev. Oncol. Hematol. 42 2002 317 325 (Pubitemid 34615692)
42. L. Kelland The resurgence of platinum-based cancer chemotherapy Nat. Rev. Cancer 7 2007 573 584 (Pubitemid 47106628)
43. H. Satoh, T. Moriguchi, K. Taguchi, J. Takai, J.M. Maher, T. Suzuki, P.T. Winnard Jr, V. Raman, M. Ebina, T. Nukiwa, and M. Yamamoto Nrf2-deficiency creates a responsive microenvironment for metastasis to the lung Carcinogenesis 31 2010 1833 1843
44. X. Ling, M. Konopleva, Z. Zeng, V. Ruvolo, L.C. Stephens, W. Schober, T. McQueen, M. Dietrich, T.L. Madden, and M. Andreeff The novel triterpenoid C-28 methyl ester of 2-cyano-3,12-dioxoolen-1,9-dien-28-oic acid inhibits metastatic murine breast tumor growth through inactivation of STAT3 signaling Cancer Res. 67 2007 4210 4218 (Pubitemid 46815067)
45. J.L. Townson, I.C. Macdonald, K.T. Liby, L. Mackenzie, D.W. Dales, B.D. Hedley, P.J. Foster, M.B. Sporn, and A.F. Chambers The synthetic triterpenoid CDDO-imidazolide suppresses experimental liver metastasis Clin. Exp. Metastasis 28 2011 309 317
46. A. Singh, S. Boldin-Adamsky, R.K. Thimmulappa, S.K. Rath, H. Ashush, J. Coulter, A. Blackford, S.N. Goodman, F. Bunz, W.H. Watson, E. Gabrielson, E. Feinstein, and S. Biswal RNAi-mediated silencing of nuclear factor erythroid-2-related factor 2 gene expression in non-small cell lung cancer inhibits tumor growth and increases efficacy of chemotherapy Cancer Res. 68 2008 7975 7984
47. T. Shibata, A. Kokubu, M. Gotoh, H. Ojima, T. Ohta, M. Yamamoto, and S. Hirohashi Genetic alteration of Keap1 confers constitutive Nrf2 activation and resistance to chemotherapy in gallbladder cancer Gastroenterology 135 2008 (1358-1368, 1368 e1351-1354)
48. A.S. Agyeman, R. Chaerkady, P.G. Shaw, N.E. Davidson, K. Visvanathan, A. Pandey, and T.W. Kensler Transcriptomic and proteomic profiling of KEAP1 disrupted and sulforaphane-treated human breast epithelial cells reveals common expression profiles Breast Cancer Res. Treat. 132 2012 175 187
49. A.K. MacLeod, M. McMahon, S.M. Plummer, L.G. Higgins, T.M. Penning, K. Igarashi, and J.D. Hayes Characterization of the cancer chemopreventive NRF2-dependent gene battery in human keratinocytes: demonstration that the KEAP1-NRF2 pathway, and not the BACH1-NRF2 pathway, controls cytoprotection against electrophiles as well as redox-cycling compounds Carcinogenesis 30 2009 1571 1580
50. G. Eades, M. Yang, Y. Yao, Y. Zhang, and Q. Zhou miR-200a regulates Nrf2 activation by targeting Keap1 mRNA in breast cancer cells J. Biol. Chem. 286 2011 40725 40733
51. Y. Kawai, L. Garduno, M. Theodore, J. Yang, and I.J. Arinze Acetylation-deacetylation of the transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2) regulates its transcriptional activity and nucleocytoplasmic localization J. Biol. Chem. 286 2011 7629 7640
52. F. Crea, S. Nobili, E. Paolicchi, G. Perrone, C. Napoli, I. Landini, R. Danesi, and E. Mini Epigenetics and chemoresistance in colorectal cancer: an opportunity for treatment tailoring and novel therapeutic strategies Drug Resist. Updates 14 2011 280 296