Role of NF-E2 related factor 2 (Nrf2) on chemotherapy resistance in acute myeloid leukemia (AML) and the effect of pharmacological inhibition of Nrf2

PLoS ONE

Volumn 12, Issue 5, 2017, Pages

  Karathedath, Sreeja ^a   Rajamani, Bharathi M ^a   Aalam, Syed Mohammed Musheer ^a   Abraham, Ajay ^a   Varatharajan, Savitha ^a   Krishnamurthy, Partha ^b   Mathews, Vikram ^a   Velayudhan, Shaji Ramachandran ^a   Balasubramanian, Poonkuzhali ^a  

^a CHRISTIAN MEDICAL COLLEGE   (India)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC TRIOXIDE; BRUSATOL; CYTARABINE; DAUNORUBICIN; DOXYCYCLINE; GENOMIC DNA; REACTIVE OXYGEN METABOLITE; RNA; TRANSCRIPTION FACTOR NRF2; ANTINEOPLASTIC AGENT; ANTIOXIDANT; KELCH LIKE ECH ASSOCIATED PROTEIN 1;

ACUTE MYELOID LEUKEMIA; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CELLULAR DISTRIBUTION; CLONOGENESIS; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; EX VIVO STUDY; FLOW CYTOMETRY; GENE MUTATION; HUMAN; HUMAN CELL; IC50; IMMUNOFLUORESCENCE; IN VITRO STUDY; MONONUCLEAR CELL; OVERALL SURVIVAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; SOLID MALIGNANT NEOPLASM; TREATMENT OUTCOME; ANTAGONISTS AND INHIBITORS; APOPTOSIS; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION; GENE SILENCING; GENETICS; LEUKEMIA, MYELOID, ACUTE; METABOLISM; MUTATION; PROTEIN TRANSPORT; TUMOR CELL CULTURE; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; ANTIOXIDANTS; APOPTOSIS; CELL LINE, TUMOR; CYTARABINE; DAUNORUBICIN; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HUMANS; INHIBITORY CONCENTRATION 50; KELCH-LIKE ECH-ASSOCIATED PROTEIN 1; LEUKEMIA, MYELOID, ACUTE; MUTATION; NF-E2-RELATED FACTOR 2; PROTEIN TRANSPORT; RESPONSE ELEMENTS; TUMOR CELLS, CULTURED;

EID: 85019486203     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0177227     Document Type: Article

References (37)

1. Pulte D, Gondos A, Brenner H. Expected long-term survival of patients diagnosed with acute myeloblastic leukemia during 2006-2010.Ann Oncol Off J Eur Soc Med Oncol ESMO.2010; 21: 335-341.
2. Ofran Y, Tallman MS, Rowe JM. How I treat acute myeloid leukemia presenting with preexisting comorbidities. Blood. 2016; 128: 488-496. https://doi.org/10.1182/blood-2016-01-635060 PMID: 27235136
3. Walter RB, Othus M, Borthakur G, Ravandi F, Cortes JE, Pierce SA, et al. Prediction of early death after induction therapy for newly diagnosed acute myeloid leukemia with pretreatment risk scores: a novel paradigm for treatment assignment. J Clin Oncol Off J Am Soc Clin Oncol. 2011; 29: 4417-4423.
4. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994; 367: 645-648. https://doi.org/10.1038/367645a0 PMID: 7509044
5. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer. 2005; 5: 275-284. https://doi.org/10.1038/nrc1590 PMID: 15803154
6. Furukawa Y. Cell cycle regulation of hematopoietic stem cells. Hum Cell. 1998; 11: 81-92. PMID: 9777402
7. Hole PS, Zabkiewicz J, Munje C, Newton Z, Pearn L, White P, et al. Overproduction of NOX-derived ROS in AML promotes proliferation and is associated with defective oxidative stress signaling. Blood. 2013; 122: 3322-3330. https://doi.org/10.1182/blood-2013-04-491944 PMID: 24089327
8. Uras IZ, Walter GJ, Scheicher R, Bellutti F, Prchal-Murphy M, Tigan AS, et al. Palbociclib treatment of FLT3-ITD+ AML cells uncovers a kinase-dependent transcriptional regulation of FLT3 and PIM1 by CDK6. Blood. 2016;
9. Lagadinou ED, Sach A, Callahan K, Rossi RM, Neering SJ, Minhajuddin M, et al. BCL-2 inhibition targets oxidative phosphorylation and selectively eradicates quiescent human leukemia stem cells. Cell Stem Cell. 2013; 12: 329-341. https://doi.org/10.1016/j.stem.2012.12.013 PMID: 23333149
10. Bhullar J, Natarajan K, Shukla S, Mathias TJ, Sadowska M, Ambudkar SV, et al. The FLT3 inhibitor quizartinib inhibits ABCG2 at pharmacologically relevant concentrations, with implications for both chemosensitization and adverse drug interactions. PloS One. 2013; 8: e71266. https://doi.org/10.1371/journal.pone.0071266 PMID: 23967177
11. Townsend DM, Findlay VL, Tew KD. Glutathione S-transferases as regulators of kinase pathways and anticancer drug targets. Methods Enzymol. 2005; 401: 287-307. https://doi.org/10.1016/S0076-6879 (05)01019-0 PMID: 16399394
12. Rushmore TH, Morton MR, Pickett CB. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem. 1991; 266: 11632-11639. PMID: 1646813
13. Hu X-F, Yao J, Gao S-G, Wang X-S, Peng X-Q, Yang Y-T, et al. Nrf2 overexpression predicts prognosis and 5-FU resistance in gastric cancer. Asian Pac J Cancer Prev APJCP. 2013; 14: 5231-5235. PMID: 24175806
14. Gao A-M, Ke Z-P, Wang J-N, Yang J-Y, Chen S-Y, Chen H. Apigenin sensitizes doxorubicin-resistant hepatocellular carcinoma BEL-7402/ADM cells to doxorubicin via inhibiting PI3K/Akt/Nrf2 pathway. Carcinogenesis. 2013; 34: 1806-1814. https://doi.org/10.1093/carcin/bgt108 PMID: 23563091
15. Ohta T, Iijima K, Miyamoto M, Nakahara I, Tanaka H, Ohtsuji M, et al. Loss of Keap1 function activates Nrf2 and provides advantages for lung cancer cell growth. Cancer Res.2008; 68: 1303-1309. https://doi.org/10.1158/0008-5472.CAN-07-5003 PMID: 18316592
16. Hanada N, Takahata T, Zhou Q, Ye X, Sun R, Itoh J, et al. Methylation of the KEAP1 gene promoter region in human colorectal cancer. BMC Cancer. 2012; 12: 66. https://doi.org/10.1186/1471-2407-12-66 PMID: 22325485
17. Tao S, Wang S, Moghaddam SJ, Ooi A, Chapman E, Wong PK, et al. Oncogenic KRAS confers chemoresistance by upregulating NRF2. Cancer Res. 2014; 74: 7430-7441. https://doi.org/10.1158/0008-5472.CAN-14-1439 PMID: 25339352
18. Li M-H, Cha Y-N, Surh Y-J. Peroxynitrite induces HO-1 expression via PI3K/Akt-dependent activation of NF-E2-related factor 2 in PC12 cells. Free Radic Biol Med. 2006; 41: 1079-1091. https://doi.org/10.1016/j.freeradbiomed.2006.06.010 PMID: 16962933
19. Rushworth SA, Macewan DJ. The role of nrf2 and cytoprotection in regulating chemotherapy resistance of human leukemia cells. Cancers. 2011; 3: 1605-1621. https://doi.org/10.3390/cancers3021605 PMID: 24212776
20. Liu Q, Zhang H, Smeester L, Zou F, Kesic M, Jaspers I, et al. The NRF2-mediated oxidative stress response pathway is associated with tumor cell resistance to arsenic trioxide across the NCI-60 panel. BMC Med Genomics.2010; 3: 37. https://doi.org/10.1186/1755-8794-3-37 PMID: 20707922
21. Olayanju A, Copple IM, Bryan HK, Edge GT, Sison RL, Wong MW, et al. Brusatol provokes a rapid and transient inhibition of Nrf2 signaling and sensitizes mammalian cells to chemical toxicity-implications for therapeutic targeting of Nrf2. Free Radic Biol Med. 2015; 78: 202-212. https://doi.org/10.1016/j.freeradbiomed.2014.11.003 PMID: 25445704
22. Tang X, Wang H, Fan L, Wu X, Xin A, Ren H, et al. 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. https://doi.org/10.1016/j.freeradbiomed.2011.03.008 PMID: 21402146
23. Liu Y, Chen F, Wang S, Guo X, Shi P, Wang W, et al. Low-dose triptolide in combination with idarubicin induces apoptosis in AML leukemic stem-like KG1a cell line by modulation of the intrinsic and extrinsic factors. Cell Death Dis. 2013; 4: e948. https://doi.org/10.1038/cddis.2013.467 PMID: 24309935
24. Arlt A, Sebens S, Krebs S, Geismann C, Grossmann M, Kruse M-L, et al. 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. https://doi.org/10.1038/onc.2012.493 PMID: 23108405
25. Peng H, Wang H, Xue P, Hou Y, Dong J, Zhou T, et al. Suppression of NRF2-ARE activity sensitizes chemotherapeutic agent-induced cytotoxicity in human acute monocytic leukemia cells. Toxicol Appl Pharmacol. 2016; 292: 1-7. https://doi.org/10.1016/j.taap.2015.12.008 PMID: 26708503
26. Ren D, Villeneuve NF, Jiang T, Wu T, Lau A, Toppin HA, et al. Brusatol enhances the efficacy of chemotherapy by inhibiting the Nrf2-mediated defense mechanism. Proc Natl Acad Sci U S A. 2011; 108: 1433-1438. https://doi.org/10.1073/pnas.1014275108 PMID: 21205897
27. Minocherhomji S, Ying S, Bjerregaard VA, Bursomanno S, Aleliunaite A, Wu W, et al. Replication stress activates DNA repair synthesis in mitosis. Nature. 2015; 528: 286-290. https://doi.org/10.1038/nature16139 PMID: 26633632
28. Lien EC, Lyssiotis CA, Juvekar A, Hu H, Asara JM, Cantley LC, et al. Glutathione biosynthesis is a metabolic vulnerability in PI3K/Akt-driven breast cancer. Nat Cell Biol. 2016; 18: 572-578. https://doi.org/10.1038/ncb3341 PMID: 27088857
29. Yoon DS, Choi Y, Lee JW. Cellular localization of NRF2 determines the self-renewal and osteogenic differentiation potential of human MSCs via the P53-SIRT1 axis. Cell Death Dis. 2016; 7: e2093. https://doi.org/10.1038/cddis.2016.3 PMID: 26866273
30. Wang X-J, Sun Z, Villeneuve NF, Zhang S, Zhao F, Li Y, et al. Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis.2008; 29: 1235-1243. https://doi.org/10.1093/carcin/bgn095 PMID: 18413364
31. Takahashi T, Sonobe M, Menju T, Nakayama E, Mino N, Iwakiri S, et al. Mutations in Keap1 are a potential prognostic factor in resected non-small cell lung cancer. J Surg Oncol.2010; 101: 500-506. https://doi.org/10.1002/jso.21520 PMID: 20213688
32. Rushworth SA, Zaitseva L, Murray MY, Shah NM, Bowles KM, MacEwan DJ. The high Nrf2 expression in human acute myeloid leukemia is driven by NF-κB and underlies its chemo-resistance. Blood. 2012; 120: 5188-5198. https://doi.org/10.1182/blood-2012-04-422121 PMID: 23077289
33. Mitsuishi Y, Taguchi K, Kawatani Y, Shibata T, Nukiwa T, Aburatani H, et al. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell. 2012; 22: 66-79. https://doi.org/10.1016/j.ccr.2012.05.016 PMID: 22789539
34. Biswas C, Shah N, Muthu M, La P, Fernando AP, Sengupta S, et al. Nuclear heme oxygenase-1 (HO-1) modulates subcellular distribution and activation of Nrf2, impacting metabolic and anti-oxidant defenses. J Biol Chem. 2014; 289: 26882-26894. https://doi.org/10.1074/jbc.M114.567685 PMID: 25107906
35. Lister A, Nedjadi T, Kitteringham NR, Campbell F, Costello E, Lloyd B, et al. Nrf2 is overexpressed in pancreatic cancer: implications for cell proliferation and therapy. Mol Cancer. 2011; 10: 37. https://doi.org/10.1186/1476-4598-10-37 PMID: 21489257
36. Kang KA, Piao MJ, Kim KC, Kang HK, Chang WY, Park IC, et al. Epigenetic modification of Nrf2 in 5-fluorouracil-resistant colon cancer cells: involvement of TET-dependent DNA demethylation. Cell Death Dis. 2014; 5: e1183. https://doi.org/10.1038/cddis.2014.149 PMID: 24743738
37. No JH, Kim Y-B, Song YS. Targeting Nrf2 Signaling to Combat Chemoresistance. J Cancer Prev. 2014; 19: 111-117. https://doi.org/10.15430/JCP.2014.19.2.111 PMID: 25337579