Vitamin C-induced epigenomic remodelling in IDH1 mutant acute myeloid leukaemia

Leukemia

Volumn 32, Issue 1, 2018, Pages 11-20

  Mingay, M ^a   Chaturvedi, A ^b   Bilenky, M ^c   Cao, Q ^a   Jackson, L ^a   Hui, T ^a   Moksa, M ^a   Heravi Moussavi, A ^c   Humphries, R K ^d   Heuser, M ^b   Hirst, M ^a,c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c BRITISH COLUMBIA CANCER AGENCY   (Canada)

^d BRITISH COLUMBIA CANCER AGENCY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBIC ACID; CCAAT ENHANCER BINDING PROTEIN BETA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; ISOCITRATE DEHYDROGENASE 1; TEN ELEVEN TRANSLOCATION 2 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; IDH1 PROTEIN, MOUSE; ISOCITRATE DEHYDROGENASE;

ACUTE MYELOID LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME INHIBITION; EPIGENETICS; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; DRUG EFFECT; GENETIC EPIGENESIS; GENETICS; MUTATION; PROCEDURES;

ANIMALS; ASCORBIC ACID; CELL DIFFERENTIATION; CELL PROLIFERATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; EPIGENOMICS; ISOCITRATE DEHYDROGENASE; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, INBRED C57BL; MUTATION; TRANSCRIPTION FACTORS;

EID: 85041483586     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2017.171     Document Type: Article

References (58)

1. Chan SM, Majeti R. Role of DNMT3A, TET2, and IDH1/2 mutations in pre-leukemic stem cells in acute myeloid leukemia. Int J Hematol 2013; 98: 648-657.
2. Losman J, Kaelin WG. What a difference a hydroxyl makes: Mutant IDH,(R)-2-hydroxyglutarate, and cancer. Genes Dev 2013; 27: 836-852.
3. Chaturvedi A, Cruz MA, Jyotsana N, Sharma A, Goparaju R, Schwarzer A et al. Enantiomer-specific and paracrine leukemogenicity of mutant IDH metabolite 2-hydroxyglutarate. Leukemia 2016; 30: 1708-1715.
4. Losman JA, Looper RE, Koivunen P, Lee S, Schneider RK, McMahon C et al. (R)-2-hydroxyglutarate is sufficient to promote leukemogenesis and its effects are reversible. Science 2013; 339: 1621-1625.
5. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 2010; 18: 553-567.
6. Gaidzik VI, Paschka P, Spath D, Habdank M, Kohne CH, Germing U et al. TET2 mutations in acute myeloid leukemia (AML): Results from a comprehensive genetic and clinical analysis of the AML study group. J Clin Oncol 2012; 30: 1350-1357.
7. Abbas S, Lugthart S, Kavelaars FG, Schelen A, Koenders JE, Zeilemaker A et al. Acquired mutations in the genes encoding IDH1 and IDH2 both are recurrent aberrations in acute myeloid leukemia: Prevalence and prognostic value. Blood 2010; 116: 2122-2126.
8. Argiropoulos B, Humphries R. Hox genes in hematopoiesis and leukemogenesis. Oncogene 2007; 26: 6766-6776.
9. Chaturvedi A, Cruz MMA, Jyotsana N, Sharma A, Yun H, Grlich K et al. Mutant IDH1 promotes leukemogenesis in vivo and can be specifically targeted in human AML. Blood 2013; 122: 2877-2887.
10. Calvo KR, Sykes DB, Pasillas M, Kamps MP. Hoxa9 immortalizes a granulocytemacrophage colony-stimulating factor-dependent promyelocyte capable of biphenotypic differentiation to neutrophils or macrophages, independent of enforced meis expression. Mol Cell Biol 2000; 20: 3274-3285.
11. Thorsteinsdottir U, Mamo A, Kroon E, Jerome L, Bijl J, Lawrence HJ et al. Overexpression of the myeloid leukemia-associated Hoxa9 gene in bone marrow cells induces stem cell expansion. Blood 2002; 99: 121-129.
12. Monfort A, Wutz A. Breathing-in epigenetic change with Vitamin C. EMBO Rep 2013; 14: 337-346.
13. Yin R, Mao S, Zhao B, Chong Z, Yang Y, Zhao C et al. Ascorbic acid enhances Tetmediated 5-methylcytosine oxidation and promotes DNA demethylation in mammals. J Am Chem Soc 2013; 135: 10396-10403.
14. Chen J, Liu H, Liu J, Qi J, Wei B, Yang J et al. H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat Genet 2013; 45: 34-42.
15. Blaschke K, Ebata KT, Karimi MM, Zepeda-Martnez JA, Goyal P, Mahapatra S et al. Vitamin C induces Tet-dependent DNA demethylation and a blastocyst-like state in ES cells. Nature 2013; 500: 222-226.
16. Chen Q, Espey MG, Krishna MC, Mitchell JB, Corpe CP, Buettner GR et al. Pharmacologic ascorbic acid concentrations selectively kill cancer cells: Action as a pro-drug to deliver hydrogen peroxide to tissues. Proc Natl Acad Sci USA 2005; 102: 13604-13609.
17. Kawada H, Kaneko M, Sawanobori M, Uno T, Matsuzawa H, Nakamura Y et al. High concentrations of L-ascorbic acid specifically inhibit the growth of human leukemic cells via downregulation of HIF-1α transcription. PLoS One 2013; 8: E62717.
18. Takamizawa S, Maehata Y, Imai K, Senoo H, Sato S, Hata R. Effects of ascorbic acid and ascorbic acid 2-phosphate, a long-acting Vitamin C derivative, on the proliferation and differentiation of human osteoblast-like cells. Cell Biol Int 2004; 28: 255-265.
19. Taiwo O, Wilson GA, Morris T, Seisenberger S, Reik W, Pearce D et al. Methylome analysis using MeDIP-seq with low DNA concentrations. Nat Protoc 2012; 7: 617-636.
20. Lorzadeh A, Bilenky M, Hammond C, Knapp DJ, Li L, Miller PH et al. Nucleosome density ChIP-Seq identifies distinct chromatin modification signatures associated with MNase accessibility. Cell Rep 2016; 17: 2112-2124.
21. Schmidt D, Wilson MD, Spyrou C, Brown GD, Hadfield J, Odom DT. ChIP-seq: Using high-throughput sequencing to discover protein-DNA interactions. Methods 2009; 48: 240-248.
22. Austria R, Semenzato A, Bettero A. Stability of Vitamin C derivatives in solution and topical formulations. J Pharm Biomed Anal 1997; 15: 795-801.
23. de Groot RP, Coffer PJ, Koenderman L. Regulation of proliferation, differentiation and survival by the IL-3/IL-5/GM-CSF receptor family. Cell Signal 1998; 10: 619-628.
24. Tavor S, Vuong PT, Park DJ, Gombart AF, Cohen AH, Koeffler HP. Macrophage functional maturation and cytokine production are impaired in C/EBP epsilondeficient mice. Blood 2002; 99: 1794-1801.
25. Wang Q, Li N, Wang X, Shen J, Hong X, Yu H et al. Membrane protein hMYADM preferentially expressed in myeloid cells is up-regulated during differentiation of stem cells and myeloid leukemia cells. Life Sci 2007; 80: 420-429.
26. Yue X, Trifari S, Aijo T, Tsagaratou A, Pastor WA, Zepeda-Martinez JA et al. Control of Foxp3 stability through modulation of TET activity. J Exp Med 2016; 213: 377-397.
27. Network CGAR. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med 2013; 368: 2059.
28. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE et al. Modelbased analysis of ChIP-Seq (MACS). Genome Biol 2008; 9: 1.
29. Lienhard M, Grimm C, Morkel M, Herwig R, Chavez L. MEDIPS: Genome-wide differential coverage analysis of sequencing data derived from DNA enrichment experiments. Bioinformatics 2014; 30: 284-286.
30. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB et al. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 2010; 28: 495-501.
31. Ogawara Y, Katsumoto T, Aikawa Y, Shima Y, Kagiyama Y, Soga T et al. IDH2 and NPM1 mutations cooperate to activate Hoxa9/Meis1 and hypoxia pathways in acute myeloid leukemia. Cancer Res 2015; 75: 2005-2016.
32. Argiropoulos B, Yung E, Humphries RK. Unraveling the crucial roles of Meis1 in leukemogenesis and normal hematopoiesis. Genes Dev 2007; 21: 2845-2849.
33. Radomska HS, Alberich-Jorda M, Will B, Gonzalez D, Delwel R, Tenen DG. Targeting CDK1 promotes FLT3-activated acute myeloid leukemia differentiation through C/EBPalpha. J Clin Invest 2012; 122: 2955-2966.
34. Domcke S, Bardet AF, Ginno PA, Hartl D, Burger L, Schbeler D. Competition between DNA methylation and transcription factors determines binding of NRF1. Nature 2015; 528: 575-579.
35. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010; 38: 576-589.
36. Goode DK, Obier N, Vijayabaskar M, Lie-A-Ling M, Lilly AJ, Hannah R et al. Dynamic gene regulatory networks drive hematopoietic specification and differentiation. Dev Cell 2016; 36: 572-587.
37. Lara-Astiaso D, Weiner A, Lorenzo-Vivas E, Zaretsky I, Jaitin DA, David E et al. Chromatin state dynamics during blood formation. Science 2014; 345: 943-949.
38. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008; 133: 1106-1117.
39. Nitzsche A, Paszkowski-Rogacz M, Matarese F, Janssen-Megens EM, Hubner NC, Schulz H et al. RAD21 cooperates with pluripotency transcription factors in the maintenance of embryonic stem cell identity. PLoS One 2011; 6: E19470.
40. Rasmussen KD, Jia G, Johansen JV, Pedersen MT, Rapin N, Bagger FO et al. Loss of TET2 in hematopoietic cells leads to DNA hypermethylation of active enhancers and induction of leukemogenesis. Genes Dev 2015; 29: 910-922.
41. Wiench M, John S, Baek S, Johnson TA, Sung MH, Escobar T et al. DNA methylation status predicts cell type-specific enhancer activity. EMBO J 2011; 30: 3028-3039.
42. Feng R, Desbordes SC, Xie H, Tillo ES, Pixley F, Stanley ER et al. PU.1 and C/EBPalpha/beta convert fibroblasts into macrophage-like cells. Proc Natl Acad Sci USA 2008; 105: 6057-6062.
43. Zhou J, Wu J, Li B, Liu D, Yu J, Yan X et al. PU. 1 is essential for MLL leukemia partially via crosstalk with the MEIS/HOX pathway. Leukemia 2014; 28: 1436-48v.
44. Okuda T, Nishimura M, Nakao M, Fujitaa Y. RUNX1/AML1: A central player in hematopoiesis. Int J Hematol 2001; 74: 252-257.
45. Wang L, Gural A, Sun XJ, Zhao X, Perna F, Huang G et al. The leukemogenicity of AML1-ETO is dependent on site-specific lysine acetylation. Science 2011; 333: 765-769.
46. de la Rica L, Rodríguez-Ubreva J, García M, Islam AB, Urquiza JM, Hernando H et al. PU. 1 target genes undergo Tet2-coupled demethylation and DNMT3b-mediated methylation in monocyte-to-osteoclast differentiation. Genome Biol 2013; 14: 1.
47. Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim S et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of α-ketoglutarate-dependent dioxygenases. Cancer Cell 2011; 19: 17-30.
48. Stephens DC, Poon GM. Differential sensitivity to methylated DNA by ETS-family transcription factors is intrinsically encoded in their DNA-binding domains. Nucleic Acids Res 2016; 44: 8671-8681.
49. Hu Z, Gu X, Baraoidan K, Ibanez V, Sharma A, Kadkol S et al. RUNX1 regulates corepressor interactions of PU.1. Blood 2011; 117: 6498-6508.
50. Cameron E, Campbell A. The orthomolecular treatment of cancer II. Clinical trial of high-dose ascorbic acid supplements in advanced human cancer. Chem Biol Interact 1974; 9: 285-315.
51. Cameron E, Pauling L. Supplemental ascorbate in the supportive treatment of cancer: Prolongation of survival times in terminal human cancer. Proc Natl Acad Sci USA 1976; 73: 3685-3689.
52. Cameron E, Pauling L. Supplemental ascorbate in the supportive treatment of cancer: Reevaluation of prolongation of survival times in terminal human cancer. Proc Natl Acad Sci USA 1978; 75: 4538-4542.
53. Creagan ET, Moertel CG, O'Fallon JR, Schutt AJ, O'Connell MJ, Rubin J et al. Failure of high-dose Vitamin C (ascorbic acid) therapy to benefit patients with advanced cancer: A controlled trial. N Engl J Med 1979; 301: 687-690.
54. Moertel CG, Fleming TR, Creagan ET, Rubin J, O'Connell MJ, Ames MM. High-dose Vitamin C versus placebo in the treatment of patients with advanced cancer who have had no prior chemotherapy: A randomized double-blind comparison. N Engl J Med 1985; 312: 137-141.
55. Levine M, Padayatty SJ, Espey MG. Vitamin C: A concentration-function approach yields pharmacology and therapeutic discoveries. Adv Nutr 2011; 2: 78-88.
56. Liu M, Ohtani H, Zhou W, Orskov AD, Charlet J, Zhang YW et al. Vitamin C increases viral mimicry induced by 5-aza-2'-deoxycytidine. Proc Natl Acad Sci USA 2016; 113: 10238-10244.
57. Schleicher RL, Carroll MD, Ford ES, Lacher DA. Serum Vitamin C and the prevalence of Vitamin C deficiency in the United States: 2003-2004 National Health and Nutrition Examination Survey (NHANES). Am J Clin Nutr 2009; 90: 1252-1263.
58. Padayatty SJ, Sun H, Wang Y, Riordan HD, Hewitt SM, Katz A et al. Vitamin C pharmacokinetics: Implications for oral and intravenous use. Ann Intern Med 2004; 140: 533-537.