Breathing-in epigenetic change with vitamin C

EMBO Reports

Volumn 14, Issue 4, 2013, Pages 337-346

  Monfort, Asun ^a,b   Wutz, Anton ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b ETH ZURICH   (Switzerland)

Author keywords

ascorbate; dioxygenase; DNA methylation; histone demethylase; reprogramming

Indexed keywords

ASCORBIC ACID; DIOXYGENASE; HISTONE DEMETHYLASE; ISOCITRATE DEHYDROGENASE 1; ISOCITRATE DEHYDROGENASE 2; OCTAMER TRANSCRIPTION FACTOR 4;

ARTICLE; BREATHING; CELL DIFFERENTIATION; DNA METHYLATION; DNA REPAIR; EPIGENETICS; GENE CLUSTER; GENE EXPRESSION; GENE MUTATION; HEMATOPOIETIC CELL; HUMAN; NONHUMAN; NUCLEAR REPROGRAMMING; OXIDATION; PRIORITY JOURNAL; RNA INTERFERENCE; RNA REPAIR; SOMATIC CELL;

ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; CELL DIFFERENTIATION; DIOXYGENASES; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; HISTONE DEMETHYLASES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; OXIDATION-REDUCTION; PROTO-ONCOGENE PROTEINS;

EID: 84876463939     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1038/embor.2013.29     Document Type: Article

References (109)

1. Drouin G, Godin JR, Pagé B (2011) The genetics of vitamin C loss in vertebrates. Curr Genomics 12: 371-378
2. Peterkofsky B (1991) Ascorbate requirement for hydroxylation and secretion of procollagen: relationship to inhibition of collagen synthesis in scurvy. Am J Clin Nutr 54: 1135S-1140S
3. Baron JH (2009) Sailors' scurvy before and after James Lind-a reassessment. Nutr Rev 67: 315-332
4. Nelson PJ, Pruitt RE, Henderson LL, Jenness R, Henderson LM (1981) Effect of ascorbic acid deficiency on the in vivo synthesis of carnitine. Biochim Biophys Acta 672: 123-127 (Pubitemid 11175945)
5. Nytko KJ, Maeda N, Schläfli P, Spielmann P, Wenger RH, Stiehl DP (2011) Vitamin C is dispensable for oxygen sensing in vivo. Blood 117: 5485-5493
6. Esteban MA et al (2010) Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 6: 71-79
7. Stadtfeld M et al (2012) Ascorbic acid prevents loss of Dlk1-Dio3 imprinting and facilitates generation of all-iPS cell mice from terminally differentiated B cells. Nat Genet 44: 398-405
8. Clifton IJ, McDonough MA, Ehrismann D, Kershaw NJ, Granatino N, Schofield CJ (2006) Structural studies on 2-oxoglutarate oxygenases and related double-stranded beta-helix fold proteins. J Inorg Biochem 100: 644-669
9. Tahiliani M et al (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935
10. Aravind L, Koonin EV (2001) The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate-and iron-dependent dioxygenases. Genome Biol 2: RESEARCH0007
11. Tsukada Y, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, Tempst P, Zhang Y (2006) Histone demethylation by a family of JmjC domain-containing proteins. Nature 439: 811-816 (Pubitemid 43255695)
12. Yamane K, Toumazou C, Tsukada Y, Erdjument-Bromage H, Tempst P, Wong J, Zhang Y (2006) JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125: 483-495
13. Sinha KM, Yasuda H, Coombes MM, Dent SY, de Crombrugghe B (2010) Regulation of the osteoblast-specific transcription factor Osterix by NO66, a Jumonji family histone demethylase. EMBO J 29: 68-79
14. He J, Kallin EM, Tsukada Y, Zhang Y (2008) The H3K36 demethylase Jhdm1b/Kdm2b regulates cell proliferation and senescence through p15(Ink4b). Nat Struct Mol Biol 15: 1169-1175
15. Kim JY et al (2012) KDM3B is the H3K9 demethylase involved in transcriptional activation of lmo2 in leukemia. Mol Cell Biol 32: 2917-2933
16. Kim SM et al (2010) Regulation of mouse steroidogenesis by WHISTLE and JMJD1C through histone methylation balance. Nucleic Acids Res 38: 6389-6403
17. Wen H, Li J, Song T, Lu M, Kan PY, Lee MG, Sha B, Shi X (2010) Recognition of histone H3K4 trimethylation by the plant homeodomain of PHF2 modulates histone demethylation. J Biol Chem 285: 9322-9326
18. Yu L et al (2010) Structural insights into a novel histone demethylase PHF8. Cell Res 20: 166-173
19. Qi HH et al (2010) Histone H4K20/H3K9 demethylase PHF8 regulates zebrafish brain and craniofacial development. Nature 466: 503-507
20. Horton JR et al (2010) Enzymatic and structural insights for substrate specificity of a family of jumonji histone lysine demethylases. Nat Struct Mol Biol 17: 38-43
21. Hsia DA et al (2010) KDM8, a H3K36me2 histone demethylase that acts in the cyclin A1 coding region to regulate cancer cell proliferation. Proc Natl Acad Sci USA 107: 9671-9676
22. Klose RJ, Yamane K, Bae Y, Zhang D, Erdjument-Bromage H, Tempst P, Wong J, Zhang Y (2006) The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 442: 312-316 (Pubitemid 44114907)
23. Fodor BD et al (2006) Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev 20: 1557-1562 (Pubitemid 43901094)
24. Cloos PA, Christensen J, Agger K, Majolica A, Rappsilber J, Antal T, Hansen KH, Helin K (2006) The putative oncogene GASC1 demethylates tri-and dimethylated lysine 9 on histone H3. Nature 442: 307-311 (Pubitemid 44114906)
25. Whetstine JR et al (2006) Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125: 467-481
26. Klose RJ, Yan Q, Tothova Z, Yamane K, Erdjument-Bromage H, Tempst P, Gilland DG, Zhang Y, Kaelin WG Jr (2007) The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell 128: 889-900 (Pubitemid 46341416)
27. Seward DJ, Cubberley G, Kim S, Schonewald M, Zhang L, Tripet B, Bentley DL (2007) Demethylation of trimethylated histone H3 Lys4 in vivo by JARID1 JmjC proteins. Nat Struct Mol Biol 14: 240-242 (Pubitemid 46355570)
28. Iwase S et al (2007) The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128: 1077-1088 (Pubitemid 46437259)
29. Agger K et al (2007) UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449: 731-734 (Pubitemid 47552088)
30. Hong S, Cho YW, Yu LR, Yu H, Veenstra TD, Ge K (2007) Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci USA 104: 18439-18444 (Pubitemid 350210715)
31. Klose RJ, Kallin EM, Zhang Y (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7: 715-727 (Pubitemid 44260007)
32. Upadhyay AK, Horton JR, Zhang X, Cheng X (2011) Coordinated methyl-lysine erasure: structural and functional linkage of a Jumonji demethylase domain and a reader domain. Curr Opin Struct Biol 21: 750-760
33. Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M (2007) Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445: 214-218 (Pubitemid 46095726)
34. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333: 1300-1303
35. He YF et al (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333: 1303-1307
36. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y (2010) Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466: 1129-1133
37. Pastor WA et al (2011) Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 473: 394-397
38. Xu Y et al (2011) Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol Cell 42: 451-464
39. Koh KP et al (2011) Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 8: 200-213
40. Williams K, Christensen J, Pedersen MT, Johansen JV, Cloos PA, Rappsilber J, Helin K (2011) TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473: 343-348
41. Wu H, D'Alessio AC, Ito S, Wang Z, Cui K, Zhao K, Sun YE, Zhang Y (2011) Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev 25: 679-684
42. Dawlaty MM et al (2011) Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. Cell Stem Cell 9: 166-175
43. Dawlaty MM et al (2013) Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev Cell 24: 310-323
44. Delhommeau F et al (2009) Mutation in TET2 in myeloid cancers. N Engl J Med 360: 2289-2301
45. Hackett JA, Sengupta R, Zylicz JJ, Murakami K, Lee C, Down TA, Surani MA (2012) Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 339: 448-452
46. Gu TP et al (2011) The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477: 606-610
47. Nakamura T et al (2012) PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 486: 415-419
48. Ko M et al (2011) Ten-eleven-translocation 2 (TET2) negatively regulates homeostasis and differentiation of hematopoietic stem cells in mice. Proc Natl Acad Sci USA 108: 14566-14571
49. Li Z et al (2011) Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood 118: 4509-4518
50. Moran-Crusio K et al (2011) Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 20: 11-24
51. Kurowski MA, Bhagwat AS, Papaj G, Bujnicki JM (2003) Phylogenomic identification of five new human homologs of the DNA repair enzyme AlkB. BMC Genomics 4: 48
52. Gerken T et al (2007) The obesity-associated FTO gene encodes a 2-oxoglutarate-dependent nucleic acid demethylase. Science 318: 1469-1472 (Pubitemid 350208961)
53. Duncan T et al (2002) Reversal of DNA alkylation damage by two human dioxygenases. Proc Natl Acad Sci USA 99: 16660-16665 (Pubitemid 36034029)
54. Ringvoll J et al (2006) Repair deficient mice reveal mABH2 as the primary oxidative demethylase for repairing 1meA and 3meC lesions in DNA. EMBO J 25: 2189-2198
55. Falnes PØ, Johansen RF, Seeberg E (2002) AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 419: 178-182 (Pubitemid 35025447)
56. Trewick SC, Henshaw TF, Hausinger RP, Lindahl T, Sedgwick B (2002) Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 419: 174-178 (Pubitemid 35025446)
57. Sundheim O et al (2008) AlkB demethylases flip out in different ways. DNA Repair (Amst) 7: 1916-1923
58. Aas PA et al (2003) Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421: 859-863 (Pubitemid 36258356)
59. -/- mice. Dev Dyn 237: 316-327 (Pubitemid 351312105)
60. Ougland R et al (2012) ALKBH1 is a histone H2A dioxygenase involved in neural differentiation. Stem Cells 30: 2672-2682
61. Church C et al (2009) A mouse model for the metabolic effects of the human fat mass and obesity associated FTO gene. PLoS Genet 5: e1000599
62. Gao X, Shin YH, Li M, Wang F, Tong Q, Zhang P (2006) The fat mass and obesity associated gene FTO functions in the brain to regulate postnatal growth in mice. PLoS ONE 5: e14005
63. Fischer J, Kock L, Emmerling C, Vierkotten J, Peters T, Brüning JC, Rüther U (2009) Inactivation of the Fto gene protects from obesity. Nature 458: 894-898
64. Li H, Collado M, Villasante A, Strati K, Ortega S, Cañamero M, Blasco MA, Serrano M (2009) The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 460: 1136-1139
65. Utikal J, Polo JM, Stadtfeld M, Maherali N, Kulalert W, Walsh RM, Khalil A, Rheinwald JG, Hochedlinger K (2009) Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 460: 1145-1148
66. Kawamura T, Suzuki J, Wang YV, Menendez S, Morera LB, Raya A, Wahl GM, Izpisúa Belmonte JC (2009) Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 460: 1140-1144
67. Wang T et al (2011) The histone demethylases Jhdm1a/1b enhance somatic cell reprogramming in a vitamin-C-dependent manner. Cell Stem Cell 9: 575-587
68. Tzatsos A, Pfau R, Kampranis SC, Tsichlis PN (2009) Ndy1/KDM2B immortalizes mouse embryonic fibroblasts by repressing the Ink4a/Arf locus. Proc Natl Acad Sci USA 106: 2641-2646
69. Kim WY, Sharpless NE (2006) The regulation of INK4/ARF in cancer and aging. Cell 127: 265-275 (Pubitemid 44572384)
70. Agherbi H, Gaussman-Wenger A, Verthuy C, Chasson L, Serrano M, Djabali M (2009) Polycomb mediated epigenetic silencing and replication timing at the INK4a/ARF locus during senescence. PLoS ONE 4: e5622
71. Houbaviy HB, Murray MF, Sharp PA (2003) Embryonic stem cell-specific MicroRNAs. Dev Cell 5: 351-358 (Pubitemid 37006477)
72. Card DA, Hebbar PB, Li L, Trotter KW, Komatsu Y, Mishina Y, Archer TK (2008) Oct4/Sox2-regulated miR-302 targets cyclin D1 in human embryonic stem cells. Mol Cell Biol 28: 6426-6438
73. Marson A et al (2008) Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134: 521-533
74. Suh MR et al (2004) Human embryonic stem cells express a unique set of microRNAs. Dev Biol 270: 488-498
75. Anokye-Danso F et al (2011) Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8: 376-388
76. Chen J et al (2012) H3K9 methylation is a barrier during somatic cell reprogramming into iPSCs. Nat Genet 45: 34-42
77. Mansour AA et al (2012) The H3K27 demethylase Utx regulates somatic and germ cell epigenetic reprogramming. Nature 488: 409-413
78. Ward PS et al (2010) The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell 17: 225-234
79. Dang L et al (2009) Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462: 739-744
80. Figueroa ME et al (2010) Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 18: 553-567
81. Xu W et al (2011) Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 19: 17-30
82. Sasaki M et al (2012) IDH1(R132H) mutation increases murine haematopoietic progenitors and alters epigenetics. Nature 488: 656-659
83. Lu C et al (2012) IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 483: 474-478
84. Turcan S et al (2012) IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 483: 479-483
85. Chowdhury R et al (2011) The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. EMBO Rep 12: 463-469
86. Grassian AR et al (2012) Isocitrate dehydrogenase (IDH) mutations promote a reversible ZEB1/microRNA (miR)-200-dependent epithelial-mesenchymal transition (EMT). J Biol Chem 287: 42180-42194
87. Chung TL, Brena RM, Kolle G, Grimmond SM, Berman BP, Laird PW, Pera MF, Wolvetang EJ (2010) Vitamin C promotes widespread yet specific DNA demethylation of the epigenome in human embryonic stem cells. Stem Cells 28: 1848-1855
88. Carey BW et al (2011) Reprogramming factor stoichiometry influences the epigenetic state and biological properties of induced pluripotent stem cells. Cell Stem Cell 9: 588-598
89. Stadtfeld M, Apostolou E, Akutsu H, Fukuda A, Follett P, Natesan S, Kono T, Shioda T, Hochedliner K (2010) Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 465: 175-181
90. Doege CA et al (2012) Early-stage epigenetic modification during somatic cell reprogramming by Parp1 and Tet2. Nature 488: 652-655
91. Costa Y et al (2013) NANOG-dependent function of TET1 and TET2 in establishment of pluripotency. Nature [Epub ahead of print] doi:10.1038/ nature11925
92. Mikkelsen TS et al (2008) Dissecting direct reprogramming through integrative genomic analysis. Nature 454: 49-55 (Pubitemid 351931978)
93. Du J, Cullen JJ, Buettner GR (2012) Ascorbic acid: chemistry, biology and the treatment of cancer. Biochim Biophys Acta 1826: 443-457
94. Knowles HJ, Raval RR, Harris AL, Ratcliffe PJ (2003) Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells. Cancer Res 63: 1764-1768 (Pubitemid 36460834)
95. Yang M, Soga T, Pollard PJ, Adam J (2012) The emerging role of fumarate as an oncometabolite. Front Oncol 2: 85
96. Antequera F, Boyes J, Bird A (1990) High levels of de novo methylation and altered chromatin structure at CpG islands in cell lines. Cell 62: 503-514
97. Kuo SM, Burl LR, Hu Z (2012) Cellular phenotype-dependent and-independent effects of vitamin C on the renewal and gene expression of mouse embryonic fibroblasts. PLoS ONE 7: e32957
98. Chen Y et al (2008) NS21: re-defined and modified supplement B27 for neuronal cultures. J Neurosci Methods 171: 239-247
99. Fukuda T, Tokunaga A, Sakamoto R, Yoshida N (2011) Fbxl10/Kdm2b deficiency accelerates neural progenitor cell death and leads to exencephaly. Mol Cell Neurosci 46: 614-624
100. Okada Y, Scott G, Ray MK, Mishina Y, Zhang Y (2007) Histone demethylase JHDM2A is critical for Tnp1 and Prm1 transcription and spermatogenesis. Nature 450: 119-123 (Pubitemid 350070569)
101. Iwamori N, Zhao M, Meistrich ML, Matzuk MM (2011) The testis-enriched histone demethylase, KDM4D, regulates methylation of histone H3 lysine 9 during spermatogenesis in the mouse but is dispensable for fertility. Biol Reprod 84: 1225-1234
102. Catchpole S et al (2011) PLU-1/JARID1B/KDM5B is required for embryonic survival and contributes to cell proliferation in the mammary gland and in ER+ breast cancer cells. Int J Oncol 38: 1267-1277
103. Schmitz SU, Albert M, Malatesta M, Morey L, Johansen JV, Bak M, Tommerup N, Abarratequi I, Helin K (2011) Jarid1b targets genes regulating development and is involved in neural differentiation. EMBO J 30: 4586-4600
104. Thieme S et al (2013) The histone demethylase UTX regulates stem cell migration and hematopoiesis. Blood [Epub ahead of print] doi: 10.1182/blood-2012-08-452003
105. Wang C, Lee JE, Cho YW, Xiao Y, Jin Q, Liu C, Ge K (2012) UTX regulates mesoderm differentiation of embryonic stem cells independent of H3K27 demethylase activity. Proc Natl Acad Sci USA 109: 15324-15329
106. Satoh T et al (2010) The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol 11: 936-944
107. Okuno Y et al (2012) Epigenetic regulation of adipogenesis by PHF2 histone demethylase. Diabetes [Epub ahead of print] doi:10.2337/db12-0628
108. Loenarz C, Ge W, Coleman ML, Rose NR, Cooper CD, Klose RJ, Ratcliffe PJ, Schofield CJ (2010) PHF8, a gene associated with cleft lip/palate and mental retardation, encodes for an Nepsilon-dimethyl lysine demethylase. Hum Mol Genet 19: 217-222
109. Ishimura A, Minehata K, Terashima M, Kondogh G, Hara T, Suzuki T (2012) Jmjd5, an H3K36me2 histone demethylase, modulates embryonic cell proliferation through the regulation of Cdkn1a expression. Development 139: 749-759