An increase in reactive oxygen species by deregulation of ARNT enhances chemotherapeutic drug-induced cancer cell death

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Shieh, Jiunn Min ^a,b   Shen, Chih Jie ^c   Chang, Wei Chiao ^d   Cheng, Hung Chi ^c   Chan, Ya Yi ^e   Huang, Wan Chen ^c   Chang, Wen Chang ^f   Chen, Ben Kuen ^c,e,f  

^a CHI MEI MEDICAL CENTER   (Taiwan)

^b CHIA NAN UNIVERSITY OF PHARMACY AND SCIENCE   (Taiwan)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^e NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^f TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; CISPLATIN; HYPOXIA INDUCIBLE FACTOR 1BETA; REACTIVE OXYGEN METABOLITE; ANTINEOPLASTIC AGENT; CASPASE 3; SMALL INTERFERING RNA;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL LINE; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENCY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM; TUMOR MICROENVIRONMENT; CELL TRANSFORMATION; DRUG EFFECTS; DRUG RESISTANCE; ENZYME ACTIVATION; GENE SILENCING; METABOLISM; NEOPLASM; PATHOLOGY; TUMOR CELL LINE; TUMOR INVASION;

ANTINEOPLASTIC AGENTS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; CASPASE 3; CELL DEATH; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CISPLATIN; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; GENE KNOCKDOWN TECHNIQUES; HUMANS; NEOPLASM INVASIVENESS; NEOPLASMS; PROTEOLYSIS; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING;

EID: 84903386157     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099242     Document Type: Article

References (34)

1. Chang KY, Shen MR, Lee MY, Wang WL, Su WC, et al. (2009) Epidermal growth factor-activated aryl hydrocarbon receptor nuclear translocator/HIF-1{beta} signal pathway up-regulates cyclooxygenase-2 gene expression associated with squamous cell carcinoma. J Biol Chem 284: 9908-9916.
2. Tian H, McKnight SL, Russell DW (1997) Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev 11: 72-82. (Pubitemid 27043825)
3. Kobayashi A, Sogawa K, Fujii-Kuriyama Y (1996) Cooperative interaction between AhR.Arnt and Sp1 for the drug-inducible expression of CYP1A1 gene. J B Chem 271: 12310-12316. (Pubitemid 26160895)
4. Kallio PJ, Pongratz I, Gradin K, McGuire J, Poellinger L (1997) Activation of hypoxia-inducible factor 1alpha: posttranscriptional regulation and conformational change by recruitment of the Arnt transcription factor. Proc Natl Acad Sci U S A 94: 5667-5672. (Pubitemid 27241827)
5. Ivan M, Kondo K, Yang H, Kim W, Valiando J, et al. (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292: 464-468. (Pubitemid 32335941)
6. Schofield CJ, Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5: 343-354. (Pubitemid 38579472)
7. Maltepe E, Schmidt JV, Baunoch D, Bradfield CA, Simon MC (1997) Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386: 403-407. (Pubitemid 27154481)
8. Mimura J, Fujii-Kuriyama Y (2003) Functional role of AhR in the expression of toxic effects by TCDD. Biochim Biophys Acta 1619: 263-268. (Pubitemid 36160604)
9. Chan YY, Kalpana S, Chang WC, Chang WC, Chen BK (2013) Expression of aryl hydrocarbon receptor nuclear translocator enhances cisplatin resistance by upregulating MDR1 expression in cancer cells. Mol Pharmacol 84: 591-602.
10. Kang HJ, Kim HJ, Kim SK, Barouki R, Cho CH, et al. (2006) BRCA1 modulates xenobiotic stress-inducible gene expression by interacting with ARNT in human breast cancer cells. J Biol Chem 281: 14654-14662. (Pubitemid 43855169)
11. Suzuki H, Tomida A, Tsuruo T (2001) Dephosphorylated hypoxia-inducible factor 1alpha as a mediator of p53-dependent apoptosis during hypoxia. Oncogene 20: 5779-5788. (Pubitemid 32937947)
12. Giaccia A, Siim BG, Johnson RS (2003) HIF-1 as a target for drug development. Nat Rev Drug Discov 2: 803-811. (Pubitemid 37361812)
13. Huang WC, Chen ST, Chang WC, Chang KY, Chen BK (2010) Involvement of aryl hydrocarbon receptor nuclear translocator in EGF-induced c-Jun/Sp1-mediated gene expression. Cell Mol Life Sci 67: 3523-3533.
14. Lebwohl D, Canetta R (1998) Clinical development of platinum complexes in cancer therapy: an historical perspective and an update. Eur J Cancer 34: 1522-1534. (Pubitemid 28446332)
15. Ohndorf UM, Rould MA, He Q, Pabo CO, Lippard SJ (1999) Basis for recognition of cisplatin-modified DNA by high-mobility-group proteins. Nature 399: 708-712. (Pubitemid 29289069)
16. Sedletska Y, Giraud-Panis MJ, Malinge JM (2005) Cisplatin is a DNA-damaging antitumour compound triggering multifactorial biochemical responses in cancer cells: importance of apoptotic pathways. Curr Med Chem Anticancer Agents 5: 251-265. (Pubitemid 40655276)
17. Bragado P, Armesilla A, Silva A, Porras A (2007) Apoptosis by cisplatin requires p53 mediated p38alpha MAPK activation through ROS generation. Apoptosis 12: 1733-1742. (Pubitemid 47106882)
18. Dickinson BC, Chang CJ (2011) Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat Chem Biol 7: 504-511.
19. Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, et al. (1997) Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275: 1649-1652. (Pubitemid 27120541)
20. Gros P, Dhir R, Croop J, Talbot F (1991) A single amino acid substitution strongly modulates the activity and substrate specificity of the mouse mdr1 and mdr3 drug efflux pumps. Proc Natl Acad Sci U S A 88: 7289-7293. (Pubitemid 21915136)
21. Ueda K, Cardarelli C, Gottesman MM, Pastan I (1987) Expression of a full-length cDNA for the human "MDR1" gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc Natl Acad Sci U S A 84: 3004-3008. (Pubitemid 17064766)
22. Wang Q, Zheng XL, Yang L, Shi F, Gao LB, et al. (2010) Reactive oxygen species-mediated apoptosis contributes to chemosensitization effect of saikosaponins on cisplatin-induced cytotoxicity in cancer cells. J Exp Clin Can Res 29: 159.
23. Nogueira V, Park Y, Chen CC, Xu PZ, Chen ML, et al. (2008) Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer cell 14: 458-470.
24. DeNicola GM, Karreth FA, Humpton TJ, Gopinathan A, Wei C, et al. (2011) Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 475: 106-109.
25. Gu C, Gonzalez J, Zhang T, Kamel-Reid S, Wells RA (2013) The aryl hydrocarbon receptor nuclear translocator (ARNT) modulates the antioxidant response in AML cells. Leuk Res 37: 1750-1756.
26. Joo MS, Lee CG, Koo JH, Kim SG (2013) miR-125b transcriptionally increased by Nrf2 inhibits AhR repressor, which protects kidney from cisplatin-induced injury. Cell Death Dis 4: e899.
27. Choi H, Chun YS, Kim SW, Kim MS, Park JW (2006) Curcumin inhibits hypoxia-inducible factor-1 by degrading aryl hydrocarbon receptor nuclear translocator: a mechanism of tumor growth inhibition. Mol Pharmacol 70: 1664-1671.
28. Park SJ, Wu CH, Gordon JD, Zhong X, Emami A, et al. (2004) Taxol induces caspase-10-dependent apoptosis. J Biol Chem 279: 51057-51067. (Pubitemid 40017847)
29. Wang S, Konorev EA, Kotamraju S, Joseph J, Kalivendi S, et al. (2004) Doxorubicin induces apoptosis in normal and tumor cells via distinctly different mechanisms. intermediacy of H(2)O(2)- and p53-dependent pathways. J Biol Chem 279: 25535-25543. (Pubitemid 38756813)
30. Oda Y, Nakajima M, Mohri T, Takamiya M, Aoki Y, et al. (2012) Aryl hydrocarbon receptor nuclear translocator in human liver is regulated by miR-24. Toxicol Appl Pharmacol 260: 222-231.
31. Dalton TP, Puga A, Shertzer HG (2002) Induction of cellular oxidative stress by aryl hydrocarbon receptor activation. Chem Biol Interact 141: 77-95. (Pubitemid 35223206)
32. Chang KY, Tsai SY, Wu CM, Yen CJ, Chuang BF, et al. (2011) Novel phosphoinositide 3-kinase/mTOR dual inhibitor, NVP-BGT226, displays potent growth-inhibitory activity against human head and neck cancer cells in vitro and in vivo. Clin Cancer Res 17: 7116-7126.
33. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
34. Ko SC, Huang CR, Shieh JM, Yang JH, Chang WC, et al. (2013) Epidermal growth factor protects squamous cell carcinoma against cisplatin-induced cytotoxicity through increased interleukin-1beta expression. PLoS One 8: e55795.