Blood glutathione redox status and global methylation of peripheral blood mononuclear cell DNA in Bangladeshi adults

Epigenetics

Volumn 8, Issue 7, 2013, Pages 730-738

  Niedzwiecki, Megan M ^a   Hall, Megan N ^a   Liu, Xinhua ^a   Oka, Julie ^a   Harper, Kristin N ^a   Slavkovich, Vesna ^a   Ilievski, Vesna ^a   Levy, Diane ^a   van Geen, Alexander ^b   Mey, Jacob L ^b   Alam, Shafiul ^c   Siddique, Abu B ^c   Parvez, Faruque ^a   Graziano, Joseph H ^a   Gamble, Mary V ^a  

^a Columbia University ^*  (United States)

^b Department of Earth and Environmental Sciences   (United States)

^c Och Spine at New York Presbyterian Hospitals   (Bangladesh)

Author keywords

DNA methylation; Glutathione; Glutathione disulfide; Homocysteine; Oxidative stress; Peripheral blood mononuclear cells; Redox

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; CREATININE; DNA METHYLTRANSFERASE; FOLIC ACID; GLUTATHIONE; GLUTATHIONE DISULFIDE; HISTONE DEACETYLASE; HOMOCYSTEINE; S ADENOSYLHOMOCYSTEINE; S ADENOSYLMETHIONINE;

ADULT; AGED; ARTICLE; BANGLADESH; CONTROLLED STUDY; DNA METHYLATION; FEMALE; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MALE; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; SMOKING;

EID: 84879656751     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.25012     Document Type: Article

References (65)

1. Jones PA, Taylor SM. Cellular differentiation, cytidine analogs and DNA methylation. Cell 1980; 20:85-93; PMID:6156004; http://dx.doi.org/10.1016/0092-8674(80)90237-8
2. Razin A, Riggs AD. DNA methylation and gene function. Science 1980; 210:604-10; PMID:6254144; http://dx.doi.org/10.1126/science.6254144
3. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, et al. The accessible chromatin landscape of the human genome. Nature 2012; 489:75-82; PMID:22955617; http://dx.doi. org/10.1038/nature11232
4. Lengauer C, Kinzler KW, Vogelstein B. DNA methylation and genetic instability in colorectal cancer cells. Proc Natl Acad Sci U S A 1997; 94:2545-50; PMID:9122232; http://dx.doi.org/10.1073/pnas.94.6.2545
5. Das PM, Singal R. DNA methylation and cancer. J Clin Oncol 2004; 22:4632-42; PMID:15542813; http://dx.doi.org/10.1200/JCO.2004.07.151
6. Robertson KD, Jones PA. DNA methylation: past, present and future directions. Carcinogenesis 2000; 21:461-7; PMID:10688866; http://dx.doi. org/10.1093/carcin/21.3.461
7. Klaunig JE, Kamendulis LM. The role of oxidative stress in carcinogenesis. Annu Rev Pharmacol Toxicol 2004; 44:239-67; PMID:14744246; http://dx.doi. org/10.1146/annurev.pharmtox.44.101802.121851
8. Forman HJ, Zhang H, Rinna A. Glutathione: overview of its protective roles, measurement, and biosynthesis. Mol Aspects Med 2009; 30:1-12; PMID:18796312; http://dx.doi.org/10.1016/j.mam.2008.08.006
9. Jones DP. Radical-free biology of oxidative stress. Am J Physiol Cell Physiol 2008; 295:C849-68; PMID:18684987; http://dx.doi.org/10.1152/ajpcell. 00283. 2008
10. Schafer FQ, Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 2001; 30:1191-212; PMID:11368918; http://dx.doi. org/10.1016/S0891-5849(01)00480-4
11. Beatty PW, Reed DJ. Involvement of the cystathionine pathway in the biosynthesis of glutathione by isolated rat hepatocytes. Arch Biochem Biophys 1980; 204:80-7; PMID:7425648; http://dx.doi.org/10.1016/0003-9861(80)90009-0
12. Franco R, Schoneveld O, Georgakilas AG, Panayiotidis MI. Oxidative stress, DNA methylation and carcinogenesis. Cancer Lett 2008; 266:6-11; PMID:18372104; http://dx.doi.org/10.1016/j.canlet. 2008. 02.026
13. Fomenko DE, Xing W, Adair BM, Thomas DJ, Gladyshev VN. High-throughput identification of catalytic redox-active cysteine residues. Science 2007; 315:387-9; PMID:17234949; http://dx.doi. org/10.1126/science.1133114
14. Pajares MA, Durán C, Corrales F, Pliego MM, Mato JM. Modulation of rat liver S-adenosylmethionine synthetase activity by glutathione. J Biol Chem 1992; 267:17598-605; PMID:1517209
15. Hitchler MJ, Domann FE. An epigenetic perspective on the free radical theory of development. Free Radic Biol Med 2007; 43:1023-36; PMID:17761298; http://dx.doi.org/10.1016/j.freeradbiomed.2007.06.027
16. Mosharov E, Cranford MR, Banerjee R. The quantitatively important relationship between homocysteine metabolism and glutathione synthesis by the transsulfuration pathway and its regulation by redox changes. Biochemistry 2000; 39:13005-11; PMID:11041866; http://dx.doi.org/10.1021/bi001088w
17. Lertratanangkoon K, Wu CJ, Savaraj N, Thomas ML. Alterations of DNA methylation by glutathione depletion. Cancer Lett 1997; 120:149-56; PMID:9461031; http://dx.doi.org/10.1016/S0304-3835(97)00300-5
18. Lertratanangkoon K, Orkiszewski RS, Scimeca JM. Methyl-donor deficiency due to chemically induced glutathione depletion. Cancer Res 1996; 56:995-1005; PMID:8640792
19. Hall MN, Niedzwiecki M, Liu X, Harper KN, Alam S, Slavkovich V, et al. Chronic arsenic exposure and blood glutathione and glutathione disulfide concentrations in Bangladeshi adults. Environ Health Perspect 2013; In press.
20. Hultberg M, Hultberg B. Oxidative stress decreases extracellular homocysteine concentration in human hepatoma (HepG2) cell cultures. Chem Biol Interact 2007; 165:54-8; PMID:17141750; http://dx.doi. org/10.1016/j.cbi.2006.10.009
21. Rogers EJ, Chen S, Chan A. Folate deficiency and plasma homocysteine during increased oxidative stress. N Engl J Med 2007; 357:421-2; PMID:17652662; http://dx.doi.org/10.1056/NEJMc066569
22. Weitzman SA, Turk PW, Milkowski DH, Kozlowski K. Free radical adducts induce alterations in DNA cytosine methylation. Proc Natl Acad Sci U S A 1994; 91:1261-4; PMID:8108398; http://dx.doi. org/10.1073/pnas.91.4.1261
23. Valinluck V, Tsai HH, Rogstad DK, Burdzy A, Bird A, Sowers LC. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res 2004; 32:4100-8; PMID:15302911; http://dx.doi.org/10.1093/nar/gkh739
24. Tunc O, Tremellen K. Oxidative DNA damage impairs global sperm DNA methylation in infertile men. J Assist Reprod Genet 2009; 26:537-44; PMID:19876730; http://dx.doi.org/10.1007/s10815-009-9346-2
25. Patchsung M, Boonla C, Amnattrakul P, Dissayabutra T, Mutirangura A, Tosukhowong P. Long interspersed nuclear element-1 hypomethylation and oxidative stress: correlation and bladder cancer diagnostic potential. PLoS One 2012; 7:e37009; PMID:22615872; http://dx.doi.org/10.1371/journal.pone.0037009
26. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010; 466:1129-33; PMID:20639862; http://dx.doi.org/10.1038/nature09303
27. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009; 324:930-5; PMID:19372391; http://dx.doi.org/10.1126/science. 1170116
28. Guo JU, Su Y, Zhong C, Ming GL, Song H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 2011; 145:423-34; PMID:21496894; http://dx.doi. org/10.1016/j.cell.2011.03.022
29. Wu SC, Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 2010; 11:607-20; PMID:20683471; http://dx.doi. org/10.1038/nrm2950
30. Chen CC, Wang KY, Shen CK. The mammalian de novo DNA methyltransferases DNMT3A and DNMT3B are also DNA 5-hydroxymethylcytosine dehydroxymethylases. J Biol Chem 2012; 287:33116-21; PMID:22898819; http://dx.doi.org/10.1074/jbc. C112.406975
31. Selker EU. Trichostatin A causes selective loss of DNA methylation in Neurospora. Proc Natl Acad Sci U S A 1998; 95:9430-5; PMID:9689097; http://dx.doi. org/10.1073/pnas.95.16.9430
32. Cyr AR, Domann FE. The redox basis of epigenetic modifications: from mechanisms to functional consequences. Antioxid Redox Signal 2011; 15:551-89; PMID:20919933; http://dx.doi.org/10.1089/ars.2010.3492
33. Gu X, Sun J, Li S, Wu X, Li L. Oxidative stress induces DNA demethylation and histone acetylation in SH-SY5Y cells: potential epigenetic mechanisms in gene transcription in Aβ production. Neurobiol Aging 2013; 34:1069-79; PMID:23141413; http://dx.doi. org/10.1016/j.neurobiolaging.2012.10.013
34. Doyle K, Fitzpatrick FA. Redox signaling, alkylation (carbonylation) of conserved cysteines inactivates class I histone deacetylases 1, 2, and 3 and antagonizes their transcriptional repressor function. J Biol Chem 2010; 285:17417-24; PMID:20385560; http://dx.doi. org/10.1074/jbc.M109.089250
35. Ago T, Liu T, Zhai P, Chen W, Li H, Molkentin JD, et al. A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy. Cell 2008; 133:978-93; PMID:18555775; http://dx.doi.org/10.1016/j. cell.2008.04.041
36. Nijhout HF, Reed MC, Anderson DF, Mattingly JC, James SJ, Ulrich CM. Long-range allosteric interactions between the folate and methionine cycles stabilize DNA methylation reaction rate. Epigenetics 2006; 1:81-7; PMID:17998813; http://dx.doi.org/10.4161/epi.1.2.2677
37. Prudova A, Bauman Z, Braun A, Vitvitsky V, Lu SC, Banerjee R. S-adenosylmethionine stabilizes cystathionine beta-synthase and modulates redox capacity. Proc Natl Acad Sci U S A 2006; 103:6489-94; PMID:16614071; http://dx.doi.org/10.1073/pnas.0509531103
38. Van Phi L, Söling HD. Methyl group transfer from exogenous S-adenosylmethionine on to plasmamembrane phospholipids without cellular uptake in isolated hepatocytes. Biochem J 1982; 206:481-7; PMID:6184050
39. McMillan JM, Walle UK, Walle T. S-adenosyl-Lmethionine: transcellular transport and uptake by Caco-2 cells and hepatocytes. J Pharm Pharmacol 2005; 57:599-605; PMID:15901349; http://dx.doi. org/10.1211/0022357056082
40. Melnyk S, Pogribna M, Pogribny IP, Yi P, James SJ. Measurement of plasma and intracellular S-adenosylmethionine and S-adenosylhomocysteine utilizing coulometric electrochemical detection: alterations with plasma homocysteine and pyridoxal 5'-phosphate concentrations. Clin Chem 2000; 46:265-72; PMID:10657384
41. Siems W, Mueller M, Garbe S, Gerber G. Damage of erythrocytes by activated oxygen generated in hypoxic rat liver. Free Radic Res Commun 1987; 4:31-9; PMID:3506895; http://dx.doi. org/10.3109/10715768709088086
42. Garg S, Vitvitsky V, Gendelman HE, Banerjee R. Monocyte differentiation, activation, and mycobacterial killing are linked to transsulfuration-dependent redox metabolism. J Biol Chem 2006; 281:38712-20; PMID:17046819; http://dx.doi.org/10.1074/jbc. M606235200
43. Garg SK, Yan Z, Vitvitsky V, Banerjee R. Differential dependence on cysteine from transsulfuration versus transport during T cell activation. Antioxid Redox Signal 2011; 15:39-47; PMID:20673163; http://dx.doi.org/10.1089/ars.2010.3496
44. Mannery YO, Ziegler TR, Park Y, Jones DP. Oxidation of plasma cysteine/cystine and GSH/GSSG redox potentials by acetaminophen and sulfur amino acid insufficiency in humans. J Pharmacol Exp Ther 2010; 333:939-47; PMID:20207721; http://dx.doi. org/10.1124/jpet.110.166421
45. Ashfaq S, Abramson JL, Jones DP, Rhodes SD, Weintraub WS, Hooper WC, et al. The relationship between plasma levels of oxidized and reduced thiols and early atherosclerosis in healthy adults. J Am Coll Cardiol 2006; 47:1005-11; PMID:16516085; http://dx.doi.org/10.1016/j.jacc.2005.09.063
46. Jones DP. Redox potential of GSH/GSSG couple: assay and biological significance. Methods Enzymol 2002; 348:93-112; PMID:11885298; http://dx.doi. org/10.1016/S0076-6879(02)48630-2
47. Calabrese V, Cornelius C, Leso V, Trovato-Salinaro A, Ventimiglia B, Cavallaro M, et al. Oxidative stress, glutathione status, sirtuin and cellular stress response in type 2 diabetes. Biochim Biophys Acta 2012; 1822:729-36; PMID:22186191; http://dx.doi. org/10.1016/j.bbadis.2011.12.003
48. Samiec PS, Drews-Botsch C, Flagg EW, Kurtz JC, Sternberg P Jr., Reed RL, et al. Glutathione in human plasma: decline in association with aging, age-related macular degeneration, and diabetes. Free Radic Biol Med 1998; 24:699-704; PMID:9586798; http://dx.doi.org/10.1016/S0891-5849(97)00286-4
49. João Cabrera E, Valezi AC, Delfino VD, Lavado EL, Barbosa DS. Reduction in plasma levels of inflammatory and oxidative stress indicators after Roux-en-Y gastric bypass. Obes Surg 2010; 20:42-9; PMID:19826889; http://dx.doi.org/10.1007/s11695-009-9988-2
50. Fitzpatrick AM, Stephenson ST, Hadley GR, Burwell L, Penugonda M, Simon DM, et al. Thiol redox disturbances in children with severe asthma are associated with posttranslational modification of the transcription factor nuclear factor (erythroid-derived 2)-like 2. J Allergy Clin Immunol 2011; 127:1604-11; PMID:21514635; http://dx.doi.org/10.1016/j. jaci.2011.03.031
51. Huang YS, Zhi YF, Kong SY, Wang QL, Xu BS, Wang SR. Plasma glutathione of patients with coronary heart disease measured by fluorospectrophotometer. Guang Pu Xue Yu Guang Pu Fen Xi 2006; 26:936-40; PMID:16883873
52. Iwata S, Hori T, Sato N, Ueda-Taniguchi Y, Yamabe T, Nakamura H, et al. Thiol-mediated redox regulation of lymphocyte proliferation. Possible involvement of adult T cell leukemia-derived factor and glutathione in transferrin receptor expression. J Immunol 1994; 152:5633-42; PMID:8207197
53. Talens RP, Boomsma DI, Tobi EW, Kremer D, Jukema JW, Willemsen G, et al. Variation, patterns, and temporal stability of DNA methylation: considerations for epigenetic epidemiology. FASEB J 2010; 24:3135-44; PMID:20385621; http://dx.doi.org/10.1096/fj.09-150490
54. Wu HC, Delgado-Cruzata L, Flom JD, Kappil M, Ferris JS, Liao Y, et al. Global methylation profiles in DNA from different blood cell types. Epigenetics 2011; 6:76-85; PMID:20890131; http://dx.doi. org/10.4161/epi.6.1.13391
55. Shimazu T, Hirschey MD, Newman J, He W, Shirakawa K, Le Moan N, et al. Suppression of oxidative stress by β-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 2013; 339:211-4; PMID:23223453; http://dx.doi.org/10.1126/science. 1227166
56. Jones DP, Carlson JL, Samiec PS, Sternberg P Jr., Mody VC Jr., Reed RL, et al. Glutathione measurement in human plasma. Evaluation of sample collection, storage and derivatization conditions for analysis of dansyl derivatives by HPLC. Clin Chim Acta 1998; 275:175-84; PMID:9721075; http://dx.doi. org/10.1016/S0009-8981(98)00089-8
57. Pfeiffer CM, Huff DL, Gunter EW. Rapid and accurate HPLC assay for plasma total homocysteine and cysteine in a clinical laboratory setting. Clin Chem 1999; 45:290-2; PMID:9931056
58. Gamble MV, Ahsan H, Liu X, Factor-Litvak P, Ilievski V, Slavkovich V, et al. Folate and cobalamin deficiencies and hyperhomocysteinemia in Bangladesh. Am J Clin Nutr 2005; 81:1372-7; PMID:15941889
59. Poirier LA, Wise CK, Delongchamp RR, Sinha R. Blood determinations of S-adenosylmethionine, S-adenosylhomocysteine, and homocysteine: correlations with diet. Cancer Epidemiol Biomarkers Prev 2001; 10:649-55; PMID:11401915
60. Balaghi M, Wagner C. DNA methylation in folate deficiency: use of CpG methylase. Biochem Biophys Res Commun 1993; 193:1184-90; PMID:8323540; http://dx.doi.org/10.1006/bbrc.1993.1750
61. Pilsner JR, Liu X, Ahsan H, Ilievski V, Slavkovich V, Levy D, et al. Genomic methylation of peripheral blood leukocyte DNA: influences of arsenic and folate in Bangladeshi adults. Am J Clin Nutr 2007; 86:1179-86; PMID:17921400
62. Slot C. Plasma creatinine determination. A new and specific Jaffe reaction method. Scand J Clin Lab Invest 1965; 17:381-7; PMID:5838275; http://dx.doi. org/10.3109/00365516509077065
63. Cheng Z, Zheng Y, Mortlock R, Van Geen A. Rapid multi-element analysis of groundwater by high-resolution inductively coupled plasma mass spectrometry. Anal Bioanal Chem 2004; 379:512-8; PMID:15098084; http://dx.doi.org/10.1007/s00216-004-2618-x
64. Van Geen A, Cheng Z, Seddique AA, Hoque MA, Gelman A, Graziano JH, et al. Reliability of a commercial kit to test groundwater for arsenic in Bangladesh. Environ Sci Technol 2005; 39:299-303; PMID:15667109; http://dx.doi.org/10.1021/es0491073
65. van Geen A, Cheng Z, Jia Q, Seddique AA, Rahman MW, Rahman MM, et al. Monitoring 51 community wells in Araihazar, Bangladesh, for up to 5 years: implications for arsenic mitigation. J Environ Sci Health A Tox Hazard Subst Environ Eng 2007; 42:1729-40; PMID:17952774; http://dx.doi. org/10.1080/10934520701564236