NRF2-driven miR-125B1 and miR-29B1 transcriptional regulation controls a novel anti-apoptotic miRNA regulatory network for AML survival

Cell Death and Differentiation

Volumn 22, Issue 4, 2015, Pages 654-664

  Shah, N M ^a,b   Zaitseva, L ^a   Bowles, K M ^a,c   MacEwan, D J ^b   Rushworth, S A ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c NORFOLK AND NORWICH UNIVERSITY HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTAGOMIR; DAUNORUBICIN; IMMUNOGLOBULIN G; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MESSENGER RNA; MICRORNA; MICRORNA 100; MICRORNA 125B; MICRORNA 125B1; MICRORNA 154; MICRORNA 221; MICRORNA 222; MICRORNA 223; MICRORNA 29A; MICRORNA 29B; MICRORNA 29B1; PROTEIN BAK; PROTEIN KINASE B BETA; PROTEIN MCL 1; STAT3 PROTEIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; KEAP1 PROTEIN, HUMAN; MIRN29 MICRORNA, HUMAN; NFE2L2 PROTEIN, HUMAN; PROTEIN BINDING; SIGNAL PEPTIDE; SMALL INTERFERING RNA;

5' UNTRANSLATED REGION; ACUTE MYELOBLASTIC LEUKEMIA; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; BINDING SITE; CANCER RESISTANCE; CELL SURVIVAL; CELL VIABILITY; CHEMOSENSITIVITY; CHROMOSOME 1; CHROMOSOME 11; CHROMOSOME 21; CHROMOSOME 7; CONTROLLED STUDY; DOWN REGULATION; GENE SILENCING; GENETIC CODE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING; ADULT; AGED; ANTAGONISTS AND INHIBITORS; FEMALE; GENE REGULATORY NETWORK; GENETICS; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; TUMOR CELL CULTURE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS; BINDING SITES; DOWN-REGULATION; FEMALE; GENE REGULATORY NETWORKS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LEUKEMIA, MYELOID, ACUTE; MALE; MICRORNAS; MIDDLE AGED; NF-E2-RELATED FACTOR 2; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 84925488511     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2014.152     Document Type: Article

References (42)

1. Estey E, Dohner H. Acute myeloid leukaemia. Lancet 2006; 368: 1894-1907.
2. Kvinlaug BT, Chan WI, Bullinger L, Ramaswami M, Sears C, Foster D et al. Common and overlapping oncogenic pathways contribute to the evolution of acute myeloid leukemias. Cancer Res 2011; 71: 4117-4129.
3. Moi P, Chan K, Asunis I, Cao A, Kan YW. Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc Natl Acad Sci USA 1994; 91: 9926-9930.
4. Alam J, Stewart D, Touchard C, Boinapally S, Choi AMK, Cook JL. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 1999; 274: 26071-26078.
5. Venugopal R, Jaiswal AK. Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc Natl Acad Sci USA 1996; 93: 14960-14965.
6. Ooi A, Dykema K, Ansari A, Petillo D, Snider J, Kahnoski R et al. CUL3 and NRF2 mutations confer an NRF2 activation phenotype in a sporadic form of papillary renal cell carcinoma. Cancer Res 2013; 73: 2044-2051.
7. 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.
8. Kim YR, Oh JE, Kim MS, Kang MR, Park SW, Han JY et al. Oncogenic NRF2 mutations in squamous cell carcinomas of oesophagus and skin. J Pathol 2011; 220: 446-451.
9. Konstantinopoulos PA, Spentzos D, Fountzilas E, Francoeur N, Sanisetty S, Grammatikos AP et al. Keap1 mutations and Nrf2 pathway activation in epithelial ovarian cancer. Cancer Res 2011; 71: 5081-5089.
10. 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 chemoresistance. Blood 2012; 120: 5188-5198.
11. Sporn MB, Liby KT. NRF2 and cancer: the good, the bad and the importance of context. Nat Rev Cancer 2012; 12: 564-571.
12. Rushworth SA, Bowles KM, MacEwan DJ. High basal nuclear levels of Nrf2 in acute myeloid leukemia reduces sensitivity to proteasome inhibitors. Cancer Res 2011; 71: 1999-2009.
13. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11: 228-234.
14. Garzon R, Marcucci G, Croce CM. Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discovery 2010; 9: 775-789.
15. Chorley BN, Campbell MR, Wang X, Karaca M, Sambandan D, Bangura F et al. Identification of novel NRF2-regulated genes by ChIP-Seq: influence on retinoid X receptor alpha. Nucleic Acids Res 2012; 40: 7416-7429.
16. Devling TWP, Lindsay CD, McLellan LI, McMahon M, Hayes JD. Utility of siRNA against Keap1 as a strategy to stimulate a cancer chemopreventive phenotype. Proc Natl Acad Sci USA 2005; 102: 7280-7285.
17. Zhao CR, Gao ZH, Qu XJ. Nrf2-ARE signaling pathway and natural products for cancer chemoprevention. Cancer Epidemiol 2010; 34: 523-533.
18. Garzon R, Heaphy CE, Havelange V, Fabbri M, Volinia S, Tsao T et al. MicroRNA 29b functions in acute myeloid leukemia. Blood 2009; 114: 5331-5341.
19. Bousquet M, Harris MH, Zhou B, Lodish HF. MicroRNA miR-125b causes leukemia. Proc Natl Acad Sci USA 2010; 107: 21558-21563.
20. Gong J, Zhang JP, Li B, Zeng C, You K, Chen MX et al. MicroRNA-125b promotes apoptosis by regulating the expression of Mcl-1, Bcl-w and IL-6R. Oncogene 2013; 32: 3071-3079.
21. Zhang H, Luo XQ, Feng DD, Zhang XJ, Wu J, Zheng YS et al. Upregulation of microRNA-125b contributes to leukemogenesis and increases drug resistance in pediatric acute promyelocytic leukemia. Mol Cancer 2011; 10: 108.
22. Garzon R, Liu S, Fabbri M, Liu Z, Heaphy CE, Callegari E et al. MicroRNA-29b induces global DNA hypomethylation and tumor suppressor gene reexpression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood 2009; 113: 6411-6418.
23. Zhao JJ, Lin J, Lwin T, Yang H, Guo J, Kong W et al. microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma. Blood 2010; 115: 2630-2639.
24. Bousquet M, Nguyen D, Chen C, Shields L, Lodish HF. MicroRNA-125b transforms myeloid cell lines by repressing multiple mRNA. Haematologica 2012; 97: 1713-1721.
25. Ooi AG, Sahoo D, Adorno M, Wang Y, Weissman IL, Park CY. MicroRNA-125b expands hematopoietic stem cells and enriches for the lymphoid-balanced and lymphoid-biased subsets. Proc Natl Acad Sci USA 2010; 107: 21505-21510.
26. Tan G, Niu J, Shi Y, Ouyang H, Wu ZH. NF-kappaB-dependent microRNA-125b up-regulation promotes cell survival by targeting p38alpha upon ultraviolet radiation. J Biol Chem 2012; 287: 33036-33047.
27. Surdziel E, Cabanski M, Dallmann I, Lyszkiewicz M, Krueger A, Ganser A et al. Enforced expression of miR-125b affects myelopoiesis by targeting multiple signaling pathways. Blood 2011; 117: 4338-4348.
28. Luna C, Li G, Qiu J, Epstein DL, Gonzalez P. Cross-talk between miR-29 and transforming growth factor-betas in trabecular meshwork cells. Invest Ophthalmol Vis Sci 2011; 52: 3567-3572.
29. Anderson JE, Kopecky KJ, Willman CL, Head D, O'Donnell MR, Luthardt FW et al. Outcome after induction chemotherapy for older patients with acute myeloid leukemia is not improved with mitoxantrone and etoposide compared to cytarabine and daunorubicin: a Southwest Oncology Group study. Blood 2002; 100: 3869-3876.
30. Wang H, Tan G, Dong L, Cheng L, Li K, Wang Z et al. Circulating MiR-125b as a Marker Predicting Chemoresistance in Breast Cancer. PLoS One 2012; 7: e34210.
31. Okamoto K, Miyoshi K, Murawaki Y. miR-29b, miR-205 and miR-221 Enhance Chemosensitivity to Gemcitabine in HuH28 Human Cholangiocarcinoma Cells. PLoS One 2013; 8: e77623.
32. Blum W, Garzon R, Klisovic RB, Schwind S, Walker A, Geyer S et al. Clinical response and miR-29b predictive significance in older AML patients treated with a 10-day schedule of decitabine. Proc Natl Acad Sci USA 2010; 107: 7473-7478.
33. Liu S, Wu LC, Pang J, Santhanam R, Schwind S, Wu YZ et al. Sp1/NFkappaB/HDAC/miR-29b regulatory network in KIT-driven myeloid leukemia. Cancer Cell 2010; 17: 333-347.
34. Gong JN, Yu J, Lin HS, Zhang XH, Yin XL, Xiao Z et al. The role, mechanism and potentially therapeutic application of microRNA-29 family in acute myeloid leukemia. Cell Death Differ 2014; 21: 100-112.
35. DeNicola GM, Karreth FA, Humpton TJ, Gopinathan A, Wei C, Frese K et al. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 2011; 475: 106-109.
36. Kong F, Sun C, Wang Z, Han L, Weng D, Lu Y et al. miR-125b confers resistance of ovarian cancer cells to cisplatin by targeting pro-apoptotic Bcl-2 antagonist killer 1. J Huazhong Univ Sci Technolog Med Sci 2011; 31: 543-549.
37. Wang Y, Li Z, He C, Wang D, Yuan X, Chen J et al. MicroRNAs expression signatures are associated with lineage and survival in acute leukemias. Blood CellsMol Dis 2010; 44: 191-197.
38. Spinello I, Quaranta MT, Riccioni R, Riti V, Pasquini L, Boe A et al. MicroRNA-146a and AMD3100, two ways to control CXCR4 expression in acute myeloid leukemias. Blood Cancer J 2011; 1: e26.
39. Tsai JJ, Dudakov JA, Takahashi K, Shieh J-H, Velardi E, Holland AM et al. Nrf2 regulates haematopoietic stem cell function. Nat Cell Biol 2013; 15: 309-316.
40. Murray MY, Rushworth SA, Zaitseva L, Bowles KM, MacEwan DJ. Attenuation of dexamethasone-induced cell death in multiple myeloma is mediated by miR-125b expression. Cell Cycle 2013; 12: 2144-2153.
41. Zaitseva L, Rushworth SA, MacEwan DJ. Silencing FLIPL modifies TNF-induced apoptotic protein expression. Cell Cycle 2011; 10: 1067-72.
42. Rushworth SA, MacEwan DJ. HO-1 underlies resistance of AML cells to TNF-induced apoptosis. Blood 2008; 111: 3793-3801.