Nrf2 is the key to chemotherapy resistance in MCF7 breast cancer cells under hypoxia

Oncotarget

Volumn 7, Issue 12, 2016, Pages 14659-14672

  Syu, Jhih Pu ^a   Chi, Jen Tsan ^b,c   Kung, Hsiu Ni ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b DUKE UNIVERSITY   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antioxidant activity; Breast tumor; Drug resistance; Hypoxia; Nrf2

Indexed keywords

CISPLATIN; GLUTAMATE CYSTEINE LIGASE; GLUTAMATE CYSTEINE LIGASE CATALYTIC SUBUNIT; GLUTAMATE CYSTEINE LIGASE MODIFIER SUBUNIT; GLUTATHIONE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; GCLC PROTEIN, HUMAN; GLUTAMATE-CYSTEINE LIGASE MODIFIER SUBUNIT, HUMAN; NFE2L2 PROTEIN, HUMAN; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER RESISTANCE; CANCER SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; HUMAN; HYPOXIA; IN VIVO STUDY; MALE; MCF 7 CELL LINE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SURVIVAL RATE; ANIMAL; APOPTOSIS; BREAST TUMOR; CELL PROLIFERATION; DRUG RESISTANCE; DRUG SCREENING; FEMALE; GENE EXPRESSION REGULATION; GENETICS; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; TUMOR CELL CULTURE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BIOMARKERS, TUMOR; BREAST NEOPLASMS; CELL PROLIFERATION; CISPLATIN; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUTAMATE-CYSTEINE LIGASE; HUMANS; HYPOXIA; MICE; MICE, INBRED ICR; NF-E2-RELATED FACTOR 2; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84962788166     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7406     Document Type: Article

References (42)

1. Bell EL, Klimova TA, Eisenbart J, Schumacker PT and Chandel NS. Mitochondrial reactive oxygen species trigger hypoxia-inducible factor-dependent extension of the replicative life span during hypoxia. Mol Cell Biol. 2007; 27:5737-5745.
2. Chi JT, Wang Z, Nuyten DS, Rodriguez EH, Schaner ME, Salim A, Wang Y, Kristensen GB, Helland A, Borresen-Dale AL, Giaccia A, Longaker MT, Hastie T, Yang GP, van de Vijver MJ and Brown PO. Gene expression programs in response to hypoxia: cell type specificity and prognostic significance in human cancers. PLoS Med. 2006; 3:e47.
3. Dang CV. Links between metabolism and cancer. Genes Dev. 2012; 26:877-890.
4. Gatza ML, Kung HN, Blackwell KL, Dewhirst MW, Marks JR and Chi JT. Analysis of tumor environmental response and oncogenic pathway activation identifies distinct basal and luminal features in HER2-related breast tumor subtypes. Breast Cancer Res. 2011; 13:R62.
5. Tang X, Lucas JE, Chen JL, LaMonte G, Wu J, Wang MC, Koumenis C and Chi JT. Functional interaction between responses to lactic acidosis and hypoxia regulates genomic transcriptional outputs. Cancer Res. 2012; 72:491-502.
6. Postovit LM, Adams MA, Lash GE, Heaton JP and Graham CH. Oxygen-mediated regulation of tumor cell invasiveness. Involvement of a nitric oxide signaling pathway. J Biol Chem. 2002; 277:35730-35737.
7. Frederiksen LJ, Siemens DR, Heaton JP, Maxwell LR, Adams MA and Graham CH. Hypoxia induced resistance to doxorubicin in prostate cancer cells is inhibited by low concentrations of glyceryl trinitrate. J Urol. 2003; 170:1003-1007.
8. Teicher BA. Hypoxia and drug resistance. Cancer Metastasis Rev. 1994; 13:139-168.
9. Li C, Lu HJ, Na FF, Deng L, Xue JX, Wang JW, Wang YQ, Li QL and Lu Y. Prognostic role of hypoxic inducible factor expression in non-small cell lung cancer: a meta-analysis. Asian Pac J Cancer Prev. 2013; 14:3607-3612.
10. Zheng SS, Chen XH, Yin X and Zhang BH. Prognostic significance of HIF-1alpha expression in hepatocellular carcinoma: a meta-analysis. PLoS One. 2013; 8:e65753.
11. Song X, Liu X, Chi W, Liu Y, Wei L, Wang X and Yu J. Hypoxia-induced resistance to cisplatin and doxorubicin in non-small cell lung cancer is inhibited by silencing of HIF-1alpha gene. Cancer Chemother Pharmacol. 2006; 58:776-784.
12. Ogiso Y, Tomida A, Lei S, Omura S and Tsuruo T. Proteasome inhibition circumvents solid tumor resistance to topoisomerase II-directed drugs. Cancer Res. 2000; 60:2429-2434.
13. Sullivan R, Pare GC, Frederiksen LJ, Semenza GL and Graham CH. Hypoxia-induced resistance to anticancer drugs is associated with decreased senescence and requires hypoxia-inducible factor-1 activity. Mol Cancer Ther. 2008; 7:1961-1973.
14. Friesen C, Kiess Y and Debatin KM. A critical role of glutathione in determining apoptosis sensitivity and resistance in leukemia cells. Cell Death Differ. 2004; 11:S73-85.
15. McLellan LI and Wolf CR. Glutathione and glutathione-dependent enzymes in cancer drug resistance. Drug Resist Updat. 1999; 2:153-164.
16. Townsend DM and Tew KD. The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene. 2003; 22:7369-7375.
17. Wang XJ, Hayes JD and Wolf CR. 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. 2006; 66:10983-10994.
18. Marengo B, De Ciucis C, Verzola D, Pistoia V, Raffaghello L, Patriarca S, Balbis E, Traverso N, Cottalasso D, Pronzato MA, Marinari UM and Domenicotti C. Mechanisms of BSO (L-buthionine-S,R-sulfoximine)-induced cytotoxic effects in neuroblastoma. Free Radic Biol Med. 2008; 44:474-482.
19. Palomares T, Carames M, Garcia-Alonso I and Alonso-Varona A. Glutathione modulation reverses the growth-promoting effect of growth factors, improving the 5-fluorouracil antitumour response in WiDr colon cancer cells. Anticancer Res. 2009; 29:3957-3965.
20. Kolamunne RT, Dias IH, Vernallis AB, Grant MM and Griffiths HR. Nrf2 activation supports cell survival during hypoxia and hypoxia/reoxygenation in cardiomyoblasts; the roles of reactive oxygen and nitrogen species. Redox Biol. 2013; 1:418-426.
21. Jaiswal AK. Regulation of genes encoding NAD(P)H:quinone oxidoreductases. Free Radic Biol Med. 2000; 29:254-262.
22. Solis WA, Dalton TP, Dieter MZ, Freshwater S, Harrer JM, He L, Shertzer HG and Nebert DW. Glutamate-cysteine ligase modifier subunit: mouse Gclm gene structure and regulation by agents that cause oxidative stress. Biochem Pharmacol. 2002; 63:1739-1754.
23. Tang X, Wang H, Fan L, Wu X, Xin A, Ren H and Wang XJ. 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. 2011; 50:1599-1609.
24. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM and Schumacker PT. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem. 2000; 275:25130-25138.
25. Guzy RD, Hoyos B, Robin E, Chen H, Liu L, Mansfield KD, Simon MC, Hammerling U and Schumacker PT. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 2005; 1:401-408.
26. Jiang H, Xie J, Xu G, Su Y, Li J, Zhu M and Wang M. Hypoxia regulates reactive oxygen species levels in SHG-44 glioma cells. Neural Regen Res. 2013; 8:554-560.
27. Reczek CR and Chandel NS. ROS-dependent signal transduction. Curr Opin Cell Biol. 2014; 33C:8-13.
28. Hagen T. Oxygen versus Reactive Oxygen in the Regulation of HIF-1alpha: The Balance Tips. Biochem Res Int. 2012; 2012:436981.
29. Dasari S and Tchounwou PB. Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol. 2014; 740:364-378.
30. Arlt A, Sebens S, Krebs S, Geismann C, Grossmann M, Kruse ML, Schreiber S and Schafer H. Inhibition of the Nrf2 transcription factor by the alkaloid trigonelline renders pancreatic cancer cells more susceptible to apoptosis through decreased proteasomal gene expression and proteasome activity. Oncogene. 2013; 32:4825-4835.
31. Wind NS and Holen I. Multidrug resistance in breast cancer: from in vitro models to clinical studies. Int J Breast Cancer. 2011; 2011:967419.
32. Buelna-Chontal M and Zazueta C. Redox activation of Nrf2 & NF-kappaB: a double end sword? Cell Signal. 2013; 25:2548-2557.
33. Apopa PL, He X and Ma Q. Phosphorylation of Nrf2 in the transcription activation domain by casein kinase 2 (CK2) is critical for the nuclear translocation and transcription activation function of Nrf2 in IMR-32 neuroblastoma cells. J Biochem Mol Toxicol. 2008; 22:63-76.
34. Geismann C, Arlt A, Sebens S and Schafer H. Cytoprotection "gone astray": Nrf2 and its role in cancer. Onco Targets Ther. 2014; 7:1497-1518.
35. Jaramillo MC and Zhang DD. The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev. 2013; 27:2179-2191.
36. Shelton P and Jaiswal AK. The transcription factor NF-E2-related factor 2 (Nrf2): a protooncogene? FASEB J. 2013; 27:414-423.
37. Sporn MB and Liby KT. NRF2 and cancer: the good, the bad and the importance of context. Nat Rev Cancer. 2012; 12:564-571.
38. Griffiths CL and Olin JL. Triple negative breast cancer: a brief review of its characteristics and treatment options. J Pharm Pract. 2012; 25:319-323.
39. Sledge GW, Jr., Loehrer PJ, Sr., Roth BJ and Einhorn LH. Cisplatin as first-line therapy for metastatic breast cancer. J Clin Oncol. 1988; 6:1811-1814.
40. Kim JW, Tchernyshyov I, Semenza GL and Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006; 3:177-185.
41. Warfel NA and El-Deiry WS. HIF-1 signaling in drug resistance to chemotherapy. Curr Med Chem. 2014; 21:3021-3028.
42. Yang SH, Wang SM, Syu JP, Chen Y, Wang SD, Peng YS, Kuo MF and Kung HN. Andrographolide induces apoptosis of C6 glioma cells via the ERK-p53-caspase 7-PARP pathway. Biomed Res Int. 2014; 2014:312847.