Redox-Active quinones induces genome-wide DNA methylation changes by an iron-mediated and Tet-dependent mechanism

Nucleic Acids Research

Volumn 42, Issue 3, 2014, Pages 1593-1605

  Zhao, Bailin ^a   Yang, Ying ^b   Wang, Xiaoli ^a   Chong, Zechen ^b   Yin, Ruichuan ^a   Song, Shu Hui ^b   Zhao, Chao ^a   Li, Cuiping ^a   Huang, Hua ^a   Sun, Bao Fa ^b   Wu, Danni ^a   Jin, Kang Xuan ^b   Song, Maoyong ^a   Zhu, Ben Zhan ^a   Jiang, Guibin ^a   Rendtlew Danielsen, Jannie M ^b,c   Xu, Guo Liang ^d   Yang, Yun Gui ^a,b   Wang, Hailin ^a  

^a RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^b Chinese Academy of Sciences and China National Center for Bioinformation   (China)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; DNA; FERRITIN; IRON; MESSENGER RNA; OXYGENASE; PROTEIN TET; PROTEIN TET1; PROTEIN TET2; QUINONE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARCINOGENICITY; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; EMBRYO; FETUS; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL;

5-METHYLCYTOSINE; ANIMALS; APOFERRITINS; CELL LINE; CELL LINE, TUMOR; CHLORANIL; CYTOSINE; DIOXYGENASES; DNA METHYLATION; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GENOME; HUMANS; IRON; MICE; OXIDATION-REDUCTION; PROTO-ONCOGENE PROTEINS; QUINONES;

EID: 84896728067     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1090     Document Type: Article

References (61)

1. Bird, A. (2002) DNA methylation patterns and epigenetic memory. Genes Dev., 16, 6-21.
2. Ito, S., DAlessio, A.C., Taranova, O.V., Hong, K., Sowers, L.C. and 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.
3. Kriaucionis, S. and Heintz, N. (2009) The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science, 324, 929-930.
4. Tahiliani, M., Koh, K.P., Shen, Y., Pastor, W.A., Bandukwala, H., Brudno, Y., Agarwal, S., Lyer, L.M., Liu, D.R., Aravind, L. et al. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science, 324, 930-935.
5. He, Y.F., Li, B.Z., Li, Z., Liu, P., Wang, Y., Tang, Q., Ding, J., Jia, Y., Chen, Z., Li, L. et al. (2011) Tet-mediated formation of 5-carboxycytosine and its excision by TDG in mammalian DNA. Science, 333, 1303-1307.
6. Ito, S., Shen, L., Dai, Q., Wu, S.C., Collins, L.B., Swenberg, J.A., He, C. and Zhang, Y. (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science, 333, 1300-1303.
7. Globisch, D., Münzel, M., Müller, M., Michalakis, S., Wagner, M., Koch, S., Brückl, T., Biel, M. and Carell, T. (2010) Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS One, 5, e15367.
8. Münzel, M., Globisch, D., Brückl, T., Wagner, M., Welzmiller, V., Michalakis, S., Müller, M., Biel, M. and Carell, T. (2010) Quantification of the sixth DNA base hydroxymethylcytosine in the brain. Angew. Chem. Int. Ed., 49, 5375-5377.
9. Pastor, W.A., Pape, U.J., Huang, Y., Henderson, H.R., Lister, R., Ko, M., McLoughlin, E.M., Brudno, Y., Mahapatra, S., Kapranov, P. et al. (2011) Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature, 473, 394-397.
10. Yu, M., Hon, G.C., Szulwach, K.E., Song, C.X., Zhang, L., Kim, A., Li, X., Dai, Q., Shen, Y., Park, B. et al. (2012) Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell, 149, 1368-1380.
11. Song, C.X., Szulwach, K.E., Fu, Y., Dai, Q., Yi, C., Li, X., Li, Y., Chen, C.H., Zhang, W., Jian, X. et al. (2011) Selective chemical labeling reveals genome-wide distribution of 5-hydroxymethylcytosine. Nat. Biotechnol., 29, 68-72.
12. Ko, M., Huang, Y., Jankowska, A.M., Pape, U.J., Tahiliani, M., Bandukwala, H.S., An, J., Lamperti, E.D., Koh, K.P., Ganetzky, R. et al. (2010) Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature, 468, 839-843.
13. Langemeijer, S.M., Kuiper, R.P., Berends, M., Knops, R., Aslanyan, M.G., Massop, M., Linders, E.S., Hoogen, P., Kessel, A.G., Raymakers, R.A.P. et al. (2009) Acquired mutations in TET2 are common in myelodysplastic syndromes. Nat. Genet., 41, 838-842.
14. Yin, R., Mao, S.Q., Zhao, B., Chong, Z., Yang, Y., Zhao, C., Zhang, D., Huang, H., Gao, J., Li, Z. et al. (2013) Ascorbic acid enhances Tet-mediated 5-methylcytosine oxidation and promotes DNA demethylation in mammals. J. Am. Chem. Soc., 135, 10396-10403.
15. Baccarelli, A. and Bollati, V. (2009) Epigenetics and environmental chemicals. Curr.Opin. Pediatr., 21, 243-251.
16. Skinner, M.K., Manikkam, M. and Guerrero-Bosagna, C. (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol. Metabol., 21, 214-222.
17. Ho, S.M., Tang, W.Y., de Frausto, J.B. and Prins, G.S. (2006) Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant. Cancer Res., 66, 5624-5632.
18. Li, S., Hansman, R., Newbold, R., Davis, B., McLachlan, J.A. and Barrett, J.C. (2003) Neonatal diethylstilbestrol exposure induces persistent elevation of c-fos expression and hypomethylation in its exon-4 in mouse uterus. Mol. Carcinog., 38, 78-84.
19. Huang, D., Zhang, Y., Qi, Y., Chen, C. and Ji, W. (2008) Global DNA hypomethylation, rather than reactive oxygen species (ROS), a potential facilitator of cadmium-stimulated K562 cell proliferation. Toxicol. Letters, 179, 43-47.
20. Lee, Y.W., Klein, C.B., Kargacin, B., Salnikow, K., Kitahara, J., Dowjat, K., Zhitkovich, A., Christie, N.T. and Costa, M. (1995) Carcinogenic nickel silences gene expression by chromatin condensation and DNA methylation: a new model for epigenetic carcinogens. Mol. Cell. Biol., 15, 2547-2557.
21. Kondo, K., Takahashi, Y., Hirose, Y., Nagao, T., Tsuyuguchi, M., Hashimoto, M., Ochiai, A., Monden, Y. and Tangoku, A. (2006) The reduced expression and aberrant methylation of p16INK4a in chromate workers with lung cancer. Lung Cancer, 53, 295-302.
22. Dolinoy, D.C., Huang, D. and Jirtle, R.L. (2007) Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl Acad. Sci. USA, 104, 13056-13061.
23. Rusiecki, J.A., Baccarelli, A., Bollati, V., Tarantini, L., Moore, L.E. and Bonefeld-Jorgensen, E.C. (2008) Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit. Environ. Health Perspect., 116, 1547.
24. Wu, Q., Ohsako, S., Ishimura, R., Suzuki, J.S. and Tohyama, C. (2004) Exposure of mouse preimplantation embryos to 2, 3, 7, 8-tetrachlorodibenzo-p- dioxin (TCDD) alters the methylation status of imprinted genes H19 and Igf2. Biol. Reprod., 70, 1790-1797.
25. Yang, X., Lay, F., Han, H. and Jones, P.A. (2010) Targeting DNA methylation for epigenetic therapy. Trends Pharmacol. Sci., 31, 536-546.
26. Deb, S., Johnson, E.E., Robalinho-Teixeira, R.L. and Wessling-Resnick, M. (2009) Modulation of intracellular iron levels by oxidative stress implicates a novel role for iron in signal transduction. Biometals, 22, 855-862.
27. Cairo, G., Tacchini, L., Pogliaghi, G., Anzon, E., Tomasi, A. and Bernelli-Zazzera, A. (1995) Induction of ferritin synthesis by oxidative stress transcriptional and post-transcriptional regulation by expansion of the free iron pool. J. Bio. Chem., 270, 700-703.
28. Breuer, W., Epsztejn, S. and Ioav Cabantchik, Z. (1996) Dynamics of the cytosolic chelatable iron pool of K562 cells. FEBS Lett., 382, 304-308.
29. Kakhlon, O. and Cabantchik, Z.I. (2002) The labile iron pool: characterization, measurement, and participation in cellular processes. Free Rad. Biol. Med., 33, 1037-1046.
30. Wise, D.R., Ward, P.S., Shay, J.E., Cross, J.R., Gruber, J.J., Sachdeva, U.M., Platt, J.M., DeMatteo, R.G., Simon, M.C. and Thompson, C.B. (2011) Hypoxia promotes isocitrate dehydrogenase-dependent carboxylation of a-ketoglutarate to citrate to support cell growth and viability. Proc. Natl Acad. Sci. USA, 108, 19611-19616.
31. Bolton, J.L., Trush, M.A., Penning, T.M., Dryhurst, G. and Monks, T.J. (2000) Role of quinones in toxicology. Chem. Res. Toxicol., 13, 135-160.
32. Ravanat, J.L., Douki, T., Duez, P., Gremaud, E., Herbert, K., Hofer, T., Lasserre, L., Saint-Pierre, C., Favier, A. and Cadet, J. (2002) Cellular background level of 8-oxo-7, 8-dihydro-20-deoxyguanosine: an isotope based method to evaluate artefactual oxidation of DNA during its extraction and subsequent work-up. Carcinogenesis, 23, 1911-1918.
33. Li, H. and Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.
34. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W. et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol., 9, R137.
35. Li, H. and Durbin, R. (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics, 26, 589-595.
36. Zhao, W., Liu, W., Tian, D., Tang, B., Wang, Y., Yu, C., Li, R., Ling, Y., Wu, J., Song, S. et al. (2011) wapRNA: a web-based application for the processing of RNA sequences. Bioinformatics, 27, 3076-3077.
37. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5, 621-628.
38. Wang, L., Feng, Z., Wang, X., Wang, X. and Zhang, X. (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics, 26, 136-138.
39. Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B, 57, 289-300.
40. Storey, J. and Tibshirani, R. (2003) Statistical significance for genomewide studies. Proc. Natl Acad. Sci. USA, 100, 9440-9445.
41. Zhu, B.Z., Kalyanaraman, B. and Jiang, G.B. (2007) Molecular mechanism for metal-independent production of hydroxyl radicals by hydrogen peroxide and halogenated quinones. Proc. Natl Acad. Sci. USA, 104, 17575-17578.
42. Zhu, B.Z. and Shan, G.Q. (2009) Potential mechanism for pentachlorophenol-inducedcarcinogenicity: A novel mechanism for metal-independent production of hydroxyl radicals. Chem. Res. Toxicol., 22, 969-977.
43. IARC Working Group. (1998) Re-evaluation of some organic chemicals, hydrazine and hydrogen peroxide. In: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Int. Agency Res. Cancer, 71, 61-63.
44. Qin, F., Zhao, Y.Y., Zhao, Y., Boyd, J.M., Zhou, W. and Li, X.F. (2010) A toxic disinfection by-product, 2, 6-dichloro-1, 4-benzoquinone, identified in drinking water. Agnew. Chem. Int. Ed., 49, 790-792.
45. Rao, K.R. (ed.)), (1987) Pentachlorophenol: Chemistry, Pharmacology, and Environmental Toxicology. Plenum Press, New York, New York.
46. Reigner, B.G., Rigod, J.F. and Tozer, T.N. (1992) Disposition, bioavailability, and serum protein binding of pentachlorophenol in the B6C3F1 mouse. Pharmacol. Res., 9, 1053-1057.
47. Bass, D.A., Parce, J.W., Dechatelet, L.R., Szejda, P., Seeds, M.C. and Thomas, M. (1983) Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. J. Immunol., 130, 1910-1917.
48. Bienvenu, C., Wagner, J.R. and Cadet, J. (1996) Photosensitized oxidation of 5-methyl-20-deoxycytidine by 2-methyl-1, 4-naphthoquinone: characterization of 5-(Hydroperoxymethyl)-20-deoxycytidine and Stable Methyl Group Oxidation Products. J. Am. Chem. Soc., 118, 11406-11411.
49. Cao, H. and Wang, Y. (2007) Quantification of oxidative single-base and intrastrand cross-link lesions in unmethylated and CpG-methylated DNA induced by Fenton-type reagents. Nucleic Acids Res., 35, 4833-4844.
50. Jaakkola, P., Mole, D.R., Tian, Y.M., Wilson, M.I., Gielbert, J., Gaskell, S.J., Kriegsheim, A., Hebestreit, H.F., Mukherji, M., Schofield, C.J. et al. (2001) Targeting of HIF-A to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science, 292, 468-472.
51. Walden, W.E., Selezneva, A.I., Dupuy, J., Volbeda, A., Fontecilla-Camps, J.C., Theil, E.C. and Volz, K. (2006) Structure of dual function iron regulatory protein 1 complexed with ferritin IRERNA. Science, 314, 1903-1908.
52. Mackenzie, E.L., Iwasaki, K. and Tsuji, Y. (2008) Intracellular iron transport and storage: from molecular mechanisms to health implications. Antioxid. Redox Signal., 10, 997-1030.
53. Nemeth, E., Tuttle, M.S., Powelson, J., Vaughn, M.B., Donovan, A., Ward, D.M., Ganz, T. and Kaplan, J. (2004) Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science, 306, 2090-2093.
54. Imlay, J.A., Chin, S.M. and Linn, S. (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science, 240, 640-642.
55. Branco, M.R., Ficz, G. and Reik, W. (2011) Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat. Rev. Genet., 13, 7-13.
56. Wu, H. and Zhang, Y. (2011) Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev., 25, 2463-2452.
57. Bhutani, N., Burns, D.M. and Blau, H.M. (2011) DNA demethylation dynamics. Cell, 146, 866-872.
58. Feinberg, A.P. and Vogelstein, B. (1983) Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature, 301, 89-92.
59. Zhou, H., Chen, W.D., Qin, X., Lee, K., Liu, L., Markowitz, S.D. and Gerson, S.L. (2001) MMTV promoter hypomethylation is linked to spontaneous and MNU associated c-neu expression and mammary carcinogenesis in MMTV c-neu transgenic mice. Oncogene, 20, 6009-6017.
60. Almeida, A., Kokalj-Vokac, N., Lefrancois, D., Viegas-Pequignot, E., Jeanpierre, M., Dutrillaux, B. and Malfoy, B. (1993) Hypomethylation of classical satellite DNA and chromosome instability in lymphoblastoid cell lines. Hum. Genet., 91, 538-546.
61. Yin, R., Zhang, D., Song, Y., Zhu, B.Z. and Wang, H. (2013) Potent DNA damage by polyhalogenated quinones and H2O2 via a metal-independent and intercalation-enhanced oxidation mechanism. Scientific Rep., 3, 1269.