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Epigenetic Basis of Oxidative Stress in Diabetic Coronary Atherosclerosis: A Shift in Focus from Genetic Prerogative

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Modulation of Oxidative Stress in Heart Disease

Abstract

Hyperglycemia-induced excessive superoxide production is the single unifying link to development and progression of diabetes micro- and macrovascular complications. Oxidative stress and antioxidant defense systems, inter alia, are recognized as both antecedent and consequent factors in the development of major diabetic complications like diabetic coronary atherosclerosis. The attendant cellular sequelae of exacerbated oxidative stress in diabetic and coronary atherosclerotic milieu are entrenched in canonical epigenetic changes like DNA methylation and histone posttranslational modifications. They alter the chromatin accessibility to the transcriptional network and steer the transcriptional programs to invoke atherogenic and inflammatory phenotype in distinct cell types. They also act as portals for propagation of the effects of ‘hyperglycemic or metabolic memory’ or the ‘legacy effect’. This chapter presents an update on the contribution of hyperglycemia and oxidative stress both singly and in connivance to accelerated development of coronary atherosclerosis through epigenetic modalities. Such a conceptual understanding would enable the identification of plausible therapeutic strategies for alleviating the burden of diabetic coronary atherosclerosis that is compounded by a formidable challenge posed by metabolic memory.

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References

  1. Stumvoll M, Goldstein BJ, van Haeften TW (2005) Type 2 diabetes: principles of pathogenesis and therapy. Lancet 365(9467):1333–1346

    CAS  PubMed  Google Scholar 

  2. Krolewski AS, Warram JH, Freire MB (1996) Epidemiology of late diabetic complications. A basis for the development and evaluation of preventive programs. Endocrinol Metab Clin N Am 2:217–242

    Google Scholar 

  3. Kannel WB, McGee DL (1979) Diabetes and cardiovascular disease. JAMA 241:2035–2038

    CAS  PubMed  Google Scholar 

  4. Beckman JA, Creager MA, Libby P (2002) Diabetes and atherosclerosis. Epidemiology, pathophysiology and management. JAMA 287:2570–2581

    CAS  PubMed  Google Scholar 

  5. Low Wang CC, Hess CN, Goldfine AB (2016) Clinical update: cardiovascular disease in diabetes mellitus: atherosclerotic cardiovascular disease and heart failure in type 2 diabetes mellitus – mechanisms, management, and clinical considerations. Circulation 133:124

    Google Scholar 

  6. Bowden DW, Cox AJ (2013) Diabetes: unravelling the enigma of type 2 DM and cardiovascular disease. Nat Rev Endocrinol 9:632–633

    PubMed  Google Scholar 

  7. Hayden MR, Tyagi SC (2002) Intimal redox stress: accelerated atherosclerosis in metabolic syndrome and type 2 diabetes mellitus. Atheroscler Cardiovasc Diabetol 1:3

    Google Scholar 

  8. Grundy SM (2012) Pre-diabetes, metabolic syndrome, and cardiovascular risk. J Am Coll Cardiol 59:7

    Google Scholar 

  9. Hossain P, Kawar B, El Nahas M (2007) Obesity and diabetes in the developing world – a growing challenge. N Engl J Med 356:213–215

    CAS  PubMed  Google Scholar 

  10. Sowers JR, Epstein M, Frohlich ED (2001) Diabetes, hypertension, and cardiovascular disease: an update. Hypertension 37:1053–1059

    CAS  PubMed  Google Scholar 

  11. Wu L, Parhofer KG (2014) Diabetic dyslipidemia. Metabolism 63:1469–1479

    CAS  PubMed  Google Scholar 

  12. Carr ME (2001) Diabetes mellitus: a hypercoagulable state. J Diabetes Complicat 15:44–54

    CAS  Google Scholar 

  13. Ross R (1999) Atherosclerosis – an inflammatory disease. N Engl J Med 340:115–126

    CAS  PubMed  Google Scholar 

  14. Festa A, D’Agostino R, Howard G et al (2000) Chronic subclinical inflammation as part of the insulin resistance syndrome: the insulin resistance atherosclerosis study (IRAS). Circulation 102:42–47

    CAS  PubMed  Google Scholar 

  15. Almdal T, Scharling H, Jensen JS, Vestergaard H (2004) The independent effect of type 2 diabetes mellitus on ischemic heart disease, stroke, and death: a population-based study of 13,000 men and women with 20 years of follow-up. Arch Intern Med 164:1422–1426

    PubMed  Google Scholar 

  16. Buse JB, Ginsberg HN, Bakris GL et al (2007) Primary prevention of cardiovascular diseases in people with diabetes mellitus: a scientific statement from the American Heart Association and the American Diabetes Association. Diabetes Care 30:162–172

    CAS  PubMed  Google Scholar 

  17. Benjamin EJ, Blaha MJ, Chiuve SE et al (2017) Heart disease and stroke statistics-2017 update: a report from the American Heart Association. Circulation 135:e146–e603

    PubMed  PubMed Central  Google Scholar 

  18. Guariguata L, Whiting DR, Hambleton I et al (2014) Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 103:137–149

    CAS  PubMed  Google Scholar 

  19. American Diabetes Association (2017) Standards of medical care in diabetes-2017, classification and diagnosis of diabetes. Diabetes Care 40:S11–S24

    Google Scholar 

  20. Mohlke KL, Boehnke M, Abecasis GR (2008) Metabolic and cardiovascular traits: an abundance of recently identified common genetic variants. Hum Mol Genet 17(R2):R102–R108

    CAS  PubMed  PubMed Central  Google Scholar 

  21. O’Donnell CJ, Nabel EG (2011) Genomics of cardiovascular disease. N Engl J Med 365:2098–2109

    PubMed  Google Scholar 

  22. Pfister R, Barnes D, Luben RN et al (2011) Individual and cumulative effect of type 2 diabetes genetic susceptibility variants on risk of coronary heart disease. Diabetologia 54:2283–2287

    CAS  PubMed  Google Scholar 

  23. Kathiresan S, Srivastava D (2012) Genetics of human cardiovascular disease. Cell 148:1242–1257

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Qi Q, Meigs JB, Rexrode KM et al (2013) Diabetes genetic predisposition score and cardiovascular complications among patients with type 2 diabetes. Diabetes Care 36:737–739

    PubMed  PubMed Central  Google Scholar 

  25. Cox AJ, Hsu FC, Ng MC et al (2014) Genetic risk score associations with cardiovascular disease and mortality in the diabetes heart study. Diabetes Care 37:1157–1164

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Wang X, Strizivh G, Hu Y et al (2016) Genetic markers of type 2 diabetes: progress in genome-wide association studies and clinical application for risk prediction. J Diabetes 8:24–35

    PubMed  Google Scholar 

  27. De Rosa S, Arcidiacono B, Chiefari E et al (2018) Type 2 diabetes mellitus and cardiovascular disease: genetic and epigenetic links. Front Endocrinol (Lausanne) 9:2

    Google Scholar 

  28. Pfohl M, Koch M, Enderle MD et al (1999) Paraoxonase 192 Gln/Arg gene polymorphism, coronary artery disease, and myocardial infarction in type 2 diabetes. Diabetes 48:623–627

    CAS  PubMed  Google Scholar 

  29. Vendrell J, Fernandez-Real JM, Gutierrez C et al (2003) A polymorphism in the promoter of the tumor necrosis factor-alpha gene (-308) is associated with coronary heart diseases in type 2 diabetic patients. Atherosclerosis 167:257–264

    CAS  PubMed  Google Scholar 

  30. Bacci S, Menzaghi C, Ercolino T et al (2004) The +276 G/T single nucleotide polymorphism of the adiponectin gene is associated with coronary artery disease in type 2 diabetic patients. Diabetes Care 27:2015–2020

    CAS  PubMed  Google Scholar 

  31. Soccio T, Zhang YY, Bacci S et al (2006) Common haplotypes at the adiponectin receptor 1 (ADIPOR1) locus are associated with increased risk of coronary artery disease in type 2 diabetes. Diabetes 55:2770

    Google Scholar 

  32. Muendlein A, Saely CH, Geller-Rhomberg S et al (2011) Single nucleotide polymorphisms of TCF7L2 are linked to diabetic coronary atherosclerosis. PLoS One 3:e17978

    Google Scholar 

  33. Chiefari E, Tanyolaç S, Paonessa F et al (2011) Functional variants of the HMGA1 gene and type 2 diabetes mellitus. JAMA 305:309

    Google Scholar 

  34. Narne P, Ponnaluri KC, Singh S et al (2012) Relationship between angiotensin-converting enzyme gene insertion/deletion polymorphism, angiographically defined coronary artery disease and myocardial infarction in patients with type 2 diabetes mellitus. J Renin-Angiotensin-Aldosterone Syst 13:478–486

    PubMed  Google Scholar 

  35. Qi L, Qi Q, Prudente S et al (2013) Association between a genetic variant related to glutamic acid metabolism and coronary heart disease in individuals with type 2 diabetes. JAMA 310:821–828

    CAS  PubMed  Google Scholar 

  36. Beaney KE, Cooper JA, McLachlan S et al (2016) Variant rs10911021 that associates with coronary heart disease in type 2 diabetes, is associated with lower concentrations of circulating HDL cholesterol and large HDL particle but not with amino acids. Cardiovasc Diabetol 15:115

    PubMed  PubMed Central  Google Scholar 

  37. Narne P, Ponnaluri KC, Singh S et al (2013) Arg399Gln polymorphism of X-ray repair cross-complementing group 1 gene is associated with angiographically documented coronary artery disease in South Indian type 2 diabetic patients. Genet Test Mol Biomarkers 17(3):236–241

    CAS  PubMed  Google Scholar 

  38. El-Lebedy D, Raslan HM, Mohammed AM (2016) Apolipoprotein E gene polymorphism and risk of type 2 diabetes and cardiovascular disease. Cardiovasc Diabetol 15:12

    PubMed  PubMed Central  Google Scholar 

  39. De Rosa S, Chiefari E, Salerno N et al (2017) HMGA1 is a novel candidate gene for myocardial infarction susceptibility. Int J Cardiol 227:331–334

    PubMed  Google Scholar 

  40. Scott LJ, Mohlke KL, Bonnycastle LL et al (2007) A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 316:1341–1345

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Zeggini E, Weedon MN, Lindgren CM et al (2007) Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes. Science 316:1336–1341

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Sladek R, Rocheleau G, Rung J et al (2007) A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445:881–885

    CAS  PubMed  Google Scholar 

  43. Jarinova O, Stewart AF, Roberts R et al (2009) Functional analysis of the chromosome 9p21.3 coronary artery diseases risk locus. Arterioscler Thromb Vasc Biol 29:1671–1677

    CAS  PubMed  Google Scholar 

  44. Cunnington MS, Santibanez Koref M, Mayosi BM et al (2010) Chromosome 9p21 SNPs associated with multiple disease phenotypes correlate with ANRIL expression. PLoS Genet 6:e1000899

    PubMed  PubMed Central  Google Scholar 

  45. Qi L, Parast L, Cai T et al (2011) Genetic susceptibility to coronary heart disease in type 2 diabetes: 3 independent studies. J Am Coll Cardiol 58:2675–2682

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Welter D, MacArthur J, Morales J, Burdett T, Hall P, Junkins H et al (2014) The NHGRI GWAS catalog, a curated resource of SNP-trait associations. Nucleic Acids Res 42(Database issue):D1001–D1006

    CAS  PubMed  Google Scholar 

  47. Xiao R, Boehnke M (2009) Quantifying and correcting for the winner’s curse in genetic association studies. Genet Epidemiol 33(5):453–462

    PubMed  PubMed Central  Google Scholar 

  48. Zhong H, Prentice RL (2010) Correcting “winner’s curse” in odds ratios from genomewide association findings for major complex human diseases. Genet Epidemiol 34(1):78–91

    PubMed  PubMed Central  Google Scholar 

  49. Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447(7143):407–412

    CAS  PubMed  Google Scholar 

  50. Badeaux AI, Shi Y (2013) Emerging roles for chromatin as a signal integration and storage platform. Nat Rev Mol Cell Biol 14:211–224

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Manolio TA, Collins FS, Cox NJ et al (2009) Finding the missing heritability of complex diseases. Nature 461:747–753

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Eichler EE, Flint J, Gibson G et al (2010) Missing heritability and strategies for finding the underlying causes of complex disease. Nat Rev Genet 11:446–450

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Zeggini E, Scott LJ, Saxena R et al (2008) Meta-analysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet 40:638–645

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Kato T, Iwamoto K, Kakiuchi C et al (2005) Genetic or epigenetic difference causing discordance between monozygotic twins as a clue to molecular basis of mental disorders. Mol Psychiatry 10:622–630

    CAS  PubMed  Google Scholar 

  55. Bird A (2007) Perceptions of epigenetics. Nature 447:396–398

    CAS  PubMed  Google Scholar 

  56. Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33:245–254

    CAS  PubMed  Google Scholar 

  57. Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84:131–176

    PubMed  Google Scholar 

  58. Bjornsson HT, Fallin MD, Feinberg AP (2004) An integrated epigenetic and genetic approach to common human disease. Trends Genet 20(8):350–358

    CAS  PubMed  Google Scholar 

  59. McRae AF, Powell JE, Henders AK et al (2014) Contribution of genetic variation to transgenerational inheritance of DNA methylation. Genome Biol 15(5):R73

    PubMed  PubMed Central  Google Scholar 

  60. Kouzarides T (2007) Chromatin modifications and their function. Cell 128(4):693–705

    CAS  PubMed  Google Scholar 

  61. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21

    CAS  PubMed  Google Scholar 

  62. Tessarz P, Kouzarides T (2014) Histone core modifications regulating nucleosome structure and dynamics. Nat Rev Mol Cell Biol 15(11):703–708

    CAS  PubMed  Google Scholar 

  63. Fenley AT, Anandakrishnan R, Kidane YH, Onufriev AV (2018) Modulation of nucleosomal DNA accessibility via charge-altering post-translational modifications in histone core. Epigenetics Chromatin 11(1):11

    PubMed  PubMed Central  Google Scholar 

  64. Dick KJ, Nelson CP, Tsaprouni L (2014) DNA methylation and body-mass index: a genome-wide analysis. Lancet 383(9933):1990–1998

    CAS  PubMed  Google Scholar 

  65. Pfeiffer L, Wahl S, Pilling LC et al (2005) DNA methylation of lipid-related genes affects blood lipid levels. Circ Cardiovasc Genet 8:334–342

    Google Scholar 

  66. Irvin MR, Zhi D, Joehanes R et al (2014) Epigenome-wide association study of fasting blood lipids in the Genetics of Lipid-lowering Drugs and Diet Network study. Circulation 130:565–572

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Arner P, Sahlqvist AS, Sinha I, Xu H, Yao X, Waterworth D et al (2016) The epigenetic signature of systemic insulin resistance in obese women. Diabetologia 59:2393–2405

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Lu C, Thompson CB (2012) Metabolic regulation of epigenetics. Cell Metab 16:9–17

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Gut P, Verdin E (2013) The nexus of chromatin regulation and intermediary metabolism. Nature 502:489–498. https://doi.org/10.1038/nature12752

    Article  CAS  PubMed  Google Scholar 

  70. Kaelin WG Jr, McKnight SL (2013) Influence of metabolism on epigenetics and disease. Cell 153:56–69. https://doi.org/10.1016/j.cell.2013.03.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Fan J, Krautkramer KA, Feldman JL, Denu JM (2015) Metabolic regulation of histone post-translational modifications. ACS Chem Biol 10:95–108. https://doi.org/10.1021/cb500846u

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Giacco F, Brownlee M (2010) Oxidative stress and diabetic complications. Circ Res 107:1058–1070

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Otani H (2011) Oxidative stress as pathogenesis of cardiovascular risk associated with metabolic syndrome. Antioxid Redox Signal 15:1911–1926

    CAS  PubMed  Google Scholar 

  74. Hitchler MJ, Domann FE (2007) An epigenetic perspective on the free radical theory of development. Free Radic Biol Med 43(7):1023–1036

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Cyr AR, Domann FE (2011) The redox basis of epigenetic modifications: from mechanisms to functional consequences. Antioxid Redox Signal 15(2):551–589. https://doi.org/10.1089/ars.2010.3492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Nagayoshi Y, Kawano H, Hokamaki J et al (2009) Differences in oxidative stress markers based on the aetiology of heart failure: comparison of oxidative stress in patients with and without coronary artery disease. Free Radic Res 43:1159–1166

    CAS  PubMed  Google Scholar 

  77. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820

    CAS  PubMed  Google Scholar 

  78. Brownlee M (2005) The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54:1615–1625

    CAS  PubMed  Google Scholar 

  79. Nishikawa TD, Eldestein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycemic damage. Nature 404:787–790

    CAS  PubMed  Google Scholar 

  80. De Vriese AS, Verbeuren TJ, Van de Voorde J et al (2000) Endothelial dysfunction in diabetes. Br J Pharmacol 130:963–974

    PubMed  PubMed Central  Google Scholar 

  81. Davignon J, Ganz P (2004) Role of endothelial dysfunction in atherosclerosis. Circulation 109(23 Suppl 1):III27–III32

    PubMed  Google Scholar 

  82. Rocic P, Seshiah P, Griendling KK (2003) Reactive oxygen species sensitivity of angiotensin II-dependent translation initiation in vascular smooth muscle cells. J Biol Chem 278:36973–36979

    CAS  PubMed  Google Scholar 

  83. Peiro C, Lafuente N, Matesanz N et al (2001) High glucose induces cell death of cultured human aortic smooth muscle cells through the formation of hydrogen peroxide. Br J Pharmacol 133:967–974

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Ishikawa K (2003) Heme oxygenase-1 against vascular insufficiency: roles of atherosclerotic disorders. Curr Pharm Des 9:2489–2497

    CAS  PubMed  Google Scholar 

  85. Hauser ER, Pericak-Vance MA (2000) Genetic analysis for common complex disease. Am Heart J 140:36–44

    Google Scholar 

  86. Foti D, Chiefari E, Fedele M, Iuliano R, Brunetti L, Paonessa F et al (2005) Lack of the architectural factor HMGA1 causes insulin resistance and diabetes in human and mice. Nat Med 7:765–773

    Google Scholar 

  87. Grant SF, Thorleifsson G, Reynisdottir I, Benediktsson R, Manolescu A, Sainz J et al (2006) Variant of transcription factor 7-like 2 (TCF7L2) gene confers risk of type 2 diabetes. Nat Genet 38:320–323

    CAS  PubMed  Google Scholar 

  88. Narne P, Ponnaluri KC, Singh S et al (2012) Relationship between NADPH oxidase p22phox C242T, PARP-1 Val762Ala polymorphisms, angiographically verified coronary artery disease and myocardial infarction in South Indian patients with type 2 diabetes mellitus. Thromb Res 130:e259–e265

    CAS  PubMed  Google Scholar 

  89. Jones DA, Prior SL, Tang TS et al (2010) Association between the rs4880 superoxide dismutase 2(C>T) gene variant and coronary heart disease in diabetes mellitus. Diabetes Res Clin Pract 90:196–201

    CAS  PubMed  Google Scholar 

  90. Narne P, Ponnaluri KC, Singh S et al (2013) Association of the genetic variants of endothelial nitric oxide synthase gene with angiographically defined coronary artery disease and myocardial infarction in South Indian patients with type 2 diabetes mellitus. J Diabetes Complicat 27(3):255–261

    Google Scholar 

  91. Adams JN, Cox AJ, Freedman BI et al (2013) Genetic analysis of haptoglobin polymorphisms with cardiovascular disease and type 2 diabetes in the diabetes heart study. Cardiovasc Diabetol 12:31

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Ruiz J, Blanché H, James RW et al (1995) Gln-Arg192 polymorphism of paraoxonase and coronary heart disease in type 2 diabetes. Lancet 346:869–872

    CAS  PubMed  Google Scholar 

  93. Blatter Garin MC, James P, Blanché H, Passa P et al (1997) Paraoxonase polymorphism Met-Leu54 is associated with modified serum concentration of the enzyme. A possible link between the paraoxonase gene and increased risk of cardiovascular disease. J Clin Invest 99:62–66

    Google Scholar 

  94. Asleh R, Marsch S, Shilkrut M et al (2003) Genetically determined heterogeneity in hemoglobin scavenging and susceptibility to diabetic cardiovascular disease. Circ Res 92:1193–1200

    CAS  PubMed  Google Scholar 

  95. Wellcome Trust Case Control Consortium (2007) Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447:661–678

    Google Scholar 

  96. Helgadottir A, Thorleifsson G, Manolescu A et al (2007) A common variant on chromosome 9p21 affects the risk of myocardial infarction. Science 316:1491–1493

    CAS  PubMed  Google Scholar 

  97. Diabetes Genetics Initiative of Broad Institute of Harvard and MIT, Lund University, and Novartis Institutes of BioMedical Research, Saxena R, Voight BF, Lyssenko V et al (2007) Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 316:1331–1336

    Google Scholar 

  98. Salonen JT, Uimari P, Aalto JM et al (2007) Type 2 diabetes whole-genome association study in four populations: the DiaGen consortium. Am J Hum Genet 81:338–345

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Broadbent HM, Peden JF, Lorkowski S et al (2008) Susceptibility to coronary heart disease and diabetes is encoded by distinct, tightly linked SNPs in the ANRIL locus on chromosome 9p. Hum Mol Genet 17:806–814

    CAS  PubMed  Google Scholar 

  100. Visel A, Zhu Y, May D et al (2010) Targeted deletion of the 9p21 non-coding coronary artery disease risk interval in mice. Nature 464:409–412

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Harismendy O, Notani D, Song X et al (2011) 9p21 DNA variants associated with coronary artery disease impair interferon-γ signalling response. Nature 470:264–268

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Stern MP (1995) Diabetes and cardiovascular disease. The “common soil” hypothesis. Diabetes 44:369–374

    CAS  PubMed  Google Scholar 

  103. Palmer C, Pe’er I (2017) Statistical correction of the Winner’s curse explains replication variability in quantitative trait genome-wide association studies. PLoS Genet 13(7):e1006916

    PubMed  PubMed Central  Google Scholar 

  104. The Diabetes Control and Complications Trial Research Group (1999) The effect of intensive treatment of diabetes on the development, and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329:977–986

    Google Scholar 

  105. Cleary PA, Orchard TJ, Genuth S et al (2006) The effect of intensive glycemic treatment on coronary artery calcification in type 1 diabetic participants of the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC) study. Diabetes 55:3556–3565

    CAS  PubMed  Google Scholar 

  106. EDIC (2003) Study sustained effect of intensive treatment of type 1 diabetes mellitus on development, and progression of diabetic nephropathy: the Epidemiology of Diabetes Interventions and Complications (EDIC) study. JAMA 290:2159–2167

    Google Scholar 

  107. UK Prospective Diabetes Study (UKPDS) Group (1998) Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352:837–853

    Google Scholar 

  108. Holman RR, Paul SK, Bethel MA et al (2008) 10-year follow-up of intensive glucose control in type 2 diabetes. N Engl J Med 359:1577–1589

    CAS  PubMed  Google Scholar 

  109. Hayward RA, Reaven PD, Wiitala WL et al (2015) Investigators V follow-up of glycemic control and cardiovascular outcomes in type 2 diabetes. N Engl J Med 372:2197–2206

    CAS  PubMed  Google Scholar 

  110. Patel A, MacMahon S, Chalmers J et al (2008) Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med 358:2560–2572

    CAS  PubMed  Google Scholar 

  111. Gaede P, Lund-Andersen H, Parving HH, Pedersen O (2008) Effect of a multifactorial intervention on mortality in type 2 diabetes. N Engl J Med 358:580–591

    CAS  PubMed  Google Scholar 

  112. El-Osta A (2012) Glycemic memory. Curr Opin Lipidol 23:24–29

    CAS  PubMed  Google Scholar 

  113. Miao F, Chen Z, Genuth S et al (2014) Evaluating the role of epigenetic histone modifications in the metabolic memory of type 1 diabetes. Diabetes 63(5):1748–1762

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Roy S, Sala R, Cagliero E, Lorenzi M (1990) Overexpression of fibronectin induced by diabetes or high glucose: phenomenon with a memory. Proc Natl Acad Sci U S A 87:404–408

    CAS  PubMed  PubMed Central  Google Scholar 

  115. El-Osta A, Brasacchio D, Yao D et al (2008) Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 205:2409–2417

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Brasacchio D, Okabe J, Tikellis C et al (2009) Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic marks that coexist on the lysine tail. Diabetes 58:1229–1236

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Ihnat MA, Thorpe JE, Kamat CD et al (2007) Reactive oxygen species mediate a cellular ‘memory’ of high glucose stress signalling. Diabetologia 50:1523–1531

    CAS  PubMed  Google Scholar 

  118. Li SL, Reddy MA, Cai Q et al (2006) Enhanced proatherogenic responses in macrophages and vascular smooth muscle cells derived from diabetic db/db mice. Diabetes 55:2611–2619

    CAS  PubMed  Google Scholar 

  119. Yao D, Brownlee M (2010) Hyperglycemia-induced reactive oxygen species increase expression of the receptor for advanced glycation end products (RAGE) and RAGE ligands. Diabetes 59:249–255

    CAS  PubMed  Google Scholar 

  120. Meerwaldt R, Links T, Zeebregts C et al (2008) The clinical relevance of assessing advanced glycation endproducts accumulation in diabetes. Cardiovasc Diabetol 7:29

    PubMed  PubMed Central  Google Scholar 

  121. Calcutt NA, Cooper ME, Kern TS, Schmidt AM (2009) Therapies for hyperglycaemia-induced diabetic complications: from animal models to clinical trials. Nat Rev Drug Discov 8:417–429

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Holmström KM, Finkel T (2014) Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol 15:411–421

    PubMed  Google Scholar 

  123. Kim GH, Ryan JJ, Archer SL (1920–1936) The role of redox signaling in epigenetics and cardiovascular disease. Antioxid Redox Signal 18:2013

    Google Scholar 

  124. Kietzmann T, Petry A, Shvetsova A et al (2017) The epigenetic landscape related to reactive oxygen species formation in the cardiovascular system. Br J Pharmacol 174:1533–1554

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Cooper ME, El-Osta A (2010) Epigenetics: mechanisms and implications for diabetic complications. Circ Res 107:1403–1413

    CAS  PubMed  Google Scholar 

  126. Siebel AL, Fernandez AZ, El-Osta A (2010) Glycemic memory associated epigenetic changes. Biochem Pharmacol 80:1853–1859

    CAS  PubMed  Google Scholar 

  127. Okabe J, Orlowski C, Balcerczyk A et al (2012) Distinguishing hyperglycemic changes by Set7 in vascular endothelial cells. Circ Res 110:1067–1076

    CAS  PubMed  Google Scholar 

  128. Reddy MA, Zhang E, Natarajan R (2015) Epigenetic mechanisms in diabetic complications and metabolic memory. Diabetologia 58(3):443–455

    CAS  PubMed  Google Scholar 

  129. Li Y, Reddy MA, Miao F et al (2008) Role of the histone H3 lysine 4 methyltransferase, SET7/9, in the regulation of NF-kappaB-dependent inflammatory genes. Relevance to diabetes and inflammation. J Biol Chem 283:26771–26781

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Paneni F, Costantino S, Battista R et al (2015) Adverse epigenetic signatures by histone methyltransferase Set7 contribute to vascular dysfunction in patients with type 2 diabetes mellitus. Circ Cardiovasc Genet 8:150–158

    CAS  PubMed  Google Scholar 

  131. Keating ST, Plutzky J, El-Osta A (2016) Epigenetic changes in diabetes and cardiovascular risk. Circ Res 118:1706–1722

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Geraldes P, King GL (2010) Activation of protein kinase C isoforms and its impact on diabetic complications. Circ Res 106:1319–1331

    CAS  PubMed  PubMed Central  Google Scholar 

  133. Baubec T, Schübeler D (2014) Genomic patterns and context specific interpretation of DNA methylation. Curr Opin Genet Dev 25:85–92

    CAS  PubMed  Google Scholar 

  134. Klose RJ, Bird AP (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 31(2):89–97

    CAS  PubMed  Google Scholar 

  135. Clouaire T, Stancheva I (2008) Methyl-CpG binding proteins: specialized transcriptional repressors or structural components of chromatin? Cell Mol Life Sci 65(10):1509–1522

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13(7):484–492

    CAS  PubMed  Google Scholar 

  137. Branco MR, Ficz G, Reik W (2012) Uncovering the role of 5- hydroxymethylcytosine in the epigenome. Nat Rev Genet 13:7–13

    CAS  Google Scholar 

  138. Breiling A, Lyko F (2015) Epigenetic regulatory functions of DNA modifications: 5-methylcytosine and beyond. Epigenetics Chromatin 8:24

    PubMed  PubMed Central  Google Scholar 

  139. Di Minno A, Turnu L, Porro B et al (2016) 8-Hydroxy-2-deoxyguanosine levels and cardiovascular disease: a systematic review and meta-analysis of the literature. Antioxid Redox Signal 24:548–555

    PubMed  PubMed Central  Google Scholar 

  140. Madugundu GS, Cadet J, Wagner JR (2014) Hydroxyl-radical induced oxidation of 5-methylcytosine in isolated and cellular DNA. Nucleic Acids Res 42:7450–7460

    CAS  PubMed  PubMed Central  Google Scholar 

  141. Valinluck V, Tsai HH, Rogstad DK et al (2004) 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 32:4100–41008

    CAS  PubMed  PubMed Central  Google Scholar 

  142. Fleming AM, Burrows CJ (2017) 8-Oxo-7,8-dihydroguanine, friend and foe: epigenetic-like regulator versus initiator of mutagenesis. DNA Repair (Amst) 56:75–83

    CAS  Google Scholar 

  143. Zhou X, Zhuang Z, Wang W et al (2016) OGG1 is essential in oxidative stress induced DNA demethylation. Cell Signal 28:1163–1171

    CAS  PubMed  Google Scholar 

  144. Afanas’ev I (2014) New nucleophilic mechanisms of ros-dependent epigenetic modifications: comparison of aging and cancer. Aging Dis 5:52–62

    PubMed  Google Scholar 

  145. Pastukh V, Roberts JT, Clark DW et al (2015) An oxidative DNA “damage” and repair mechanism localized in the VEGF promoter is important for hypoxia-induced VEGF mRNA expression. Am J Physiol Lung Cell Mol Physiol 309:L1367–L1375

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Pan L, Zhu B, Hao W et al (2016) Oxidized guanine base lesions function in 8-oxoguanine DNA glycosylase-1-mediated epigenetic regulation of nuclear factor kappaB-driven gene expression. J Biol Chem 291:25553–25566

    CAS  PubMed  PubMed Central  Google Scholar 

  147. Khan MA, Alam K, Dixit K, Rizvi MM (2016) Role of peroxynitrite induced structural changes on H2B histone by physicochemical method. Int J Biol Macromol 82:31–38

    CAS  PubMed  Google Scholar 

  148. Galligan JJ, Rose KL, Beavers WN et al (2014) Stable histone adduction by 4-oxo-2-nonenal: a potential link between oxidative stress and epigenetics. J Am Chem Soc 136:11864–11866

    CAS  PubMed  PubMed Central  Google Scholar 

  149. Garcia-Gimenez JL, Olaso G, Hake SB et al (2013) Histone h3 glutathionylation in proliferating mammalian cells destabilizes nucleosomal structure. Antioxid Redox Signal 19:1305–1320

    CAS  PubMed  PubMed Central  Google Scholar 

  150. Kloypan C, Srisa-art M, Mutirangura A, Boonla C (2015) LINE-1 hypomethylation induced by reactive oxygen species is mediated via depletion of S-adenosylmethionine. Cell Biochem Funct 33:375–385

    CAS  PubMed  Google Scholar 

  151. Baccarelli A, Wright R, Bollati V et al (2010) Ischemic heart disease and stroke in relation to blood DNA methylation. Epidemiology 21:819–828

    PubMed  PubMed Central  Google Scholar 

  152. Narne P, Pandey V, Phanithi PB (2017) Interplay between mitochondrial metabolism and oxidative stress in ischemic stroke: an epigenetic connection. Mol Cell Neurosci 82:176–194

    CAS  PubMed  Google Scholar 

  153. Watson CJ, Collier P, Tea I et al (2014) Hypoxia-induced epigenetic modifications are associated with cardiac tissue fibrosis and the development of a myofibroblast like phenotype. Hum Mol Genet 23:2176–2188

    CAS  PubMed  Google Scholar 

  154. Bishop T, Ratcliffe PJ (2015) HIF hydroxylase pathways in cardiovascular physiology and medicine. Circ Res 117:65–79

    CAS  PubMed  PubMed Central  Google Scholar 

  155. Xiong F, Xiao D, Zhang L (2012) Norepinephrine causes epigenetic repression of PKCepsilon gene in rodent hearts by activating Nox1- dependent reactive oxygen species production. FASEB J 26:2753–2763

    CAS  PubMed  PubMed Central  Google Scholar 

  156. Xiao D, Dasgupta C, Chen M et al (2014) Inhibition of DNA methylation reverses norepinephrine-induced cardiac hypertrophy in rats. Cardiovasc Res 101:373–382

    CAS  PubMed  Google Scholar 

  157. Dunn J, Simmons R, Thabet S, Jo H (2015) The role of epigenetics in the endothelial cell shear stress response and atherosclerosis. Int J Biochem Cell Biol 67:167–176

    CAS  PubMed  PubMed Central  Google Scholar 

  158. O’Hagan HM, Wang W, Sen S et al (2011) Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG Islands. Cancer Cell 20:606–619

    PubMed  PubMed Central  Google Scholar 

  159. Muka T, Nano J, Voortman T et al (2016) The role of global and regional DNA methylation and histone modifications in glycemic traits and type 2 diabetes: a systematic review. Nutr Metab Cardiovasc Dis 26(7):553–566

    CAS  PubMed  Google Scholar 

  160. Laukkanen MO, Mannermaa S, Hiltunen MO et al (1999) Local hypomethylation in atherosclerosis found in rabbit ec-sod gene. Arterioscler Thromb Vasc Biol 19:2171–2178

    CAS  PubMed  Google Scholar 

  161. Valencia-Morales Mdel P, Zaina S, Heyn H et al (2015) The DNA methylation drift of the atherosclerotic aorta increases with lesion progression. BMC Med Genet 8:7

    Google Scholar 

  162. Niu Y, Des Marais TL, Tong Z et al (2015) Oxidative stress alters global histone modification and DNA methylation. Free Radic Biol Med 82:22–28

    CAS  PubMed  PubMed Central  Google Scholar 

  163. Thienpont B, Steinbacher J, Zhao H et al (2016) Tumour hypoxia causes DNA hypermethylation by reducing TET activity. Nature 537:63–68

    CAS  PubMed  PubMed Central  Google Scholar 

  164. Kalani A, Kamat PK, Tyagi N (2015) Diabetic stroke severity: epigenetic remodeling and neuronal, glial, and vascular dysfunction. Diabetes 64:4260–4271

    CAS  PubMed  PubMed Central  Google Scholar 

  165. Salminen A, Kaarniranta K, Kauppinen A (2016) Hypoxia-inducible histone lysine demethylases: impact on the aging process and age related diseases. Aging Dis 7:180–200

    PubMed  PubMed Central  Google Scholar 

  166. Monfort A, Wutz A (2013) Breathing-in epigenetic change with vitamin C. EMBO Rep 14:337–346

    CAS  PubMed  PubMed Central  Google Scholar 

  167. Laukka T, Mariani CJ, Ihantola T, Cao JZ, Hokkanen J, Kaelin WG Jr et al (2016) Fumarate and succinate regulate expression of hypoxia-inducible genes via TET enzymes. J Biol Chem 291:4256–4265

    CAS  PubMed  Google Scholar 

  168. Zhang J, Wang YT, Miller JH et al (2018) Accumulation of succinate in cardiac ischemia primarily occurs via canonical Krebs cycle activity. Cell Rep 23:2617–2628

    CAS  PubMed  PubMed Central  Google Scholar 

  169. Liu R, Jin Y, Tang WH et al (2013) Ten-eleven translocation-2 (TET2) is a master regulator of smooth muscle cell plasticity. Circulation 128(18):2047–2057

    PubMed  PubMed Central  Google Scholar 

  170. Feil S, Fehrenbacher B, Lukowski R et al (2014) Transdifferentiation of vascular smooth muscle cells to macrophage-like cells during atherogenesis. Circ Res 115:662–667

    CAS  PubMed  Google Scholar 

  171. Hiltunen MO, Yla-Herttuala S (2003) DNA methylation, smooth muscle cells, and atherogenesis. Arterioscler Thromb Vasc Biol 23:1750–1753

    CAS  PubMed  Google Scholar 

  172. Lund G, Andersson L, Lauria M et al (2004) DNA methylation polymorphisms precede any histological sign of atherosclerosis in mice lacking apolipoprotein E. J Biol Chem 279(28):29147–29154

    CAS  PubMed  Google Scholar 

  173. Zaina S, Lindholm MW, Lund G (2005) Nutrition and aberrant DNA methylation patterns in atherosclerosis: more than just hyperhomocysteinemia? J Nutr 135:5–8

    CAS  PubMed  Google Scholar 

  174. Stenvinkel P, Karimi M, Johansson S et al (2007) Impact of inflammation on epigenetic DNA methylation—a novel risk factor for cardiovascular disease? J Intern Med 261:488–499

    CAS  PubMed  Google Scholar 

  175. Kuroda A, Rauch TA, Todorov I et al (2009) Insulin gene expression is regulated by DNA methylation. PLoS One 4(9):e6953

    PubMed  PubMed Central  Google Scholar 

  176. Yang BT, Dayeh TA, Kirkpatrick CL et al (2011) Insulin promoter DNA methylation correlates negatively with insulin gene expression and positively with HbA(1c) levels in human pancreatic islets. Diabetologia 54:360–367

    CAS  PubMed  Google Scholar 

  177. Yang BT, Dayeh TA, Volkov PA et al (2012) Increased DNA methylation and decreased expression of PDX-1 in pancreatic islets from patients with type 2 diabetes. Mol Endocrinol 26(7):1203–1212

    CAS  PubMed  PubMed Central  Google Scholar 

  178. Ling C, Del Guerra S, Lupi R et al (2008) Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion. Diabetologia 51:615–622

    CAS  PubMed  PubMed Central  Google Scholar 

  179. Davegårdh C, García-Calzón S, Bacos K, Ling C (2018) DNA methylation in the pathogenesis of type 2 diabetes in humans. Mol Metab 14:12–25. Feb 7. pii: S2212-8778(17)31102-X

    PubMed  PubMed Central  Google Scholar 

  180. Volkov P, Bacos K, Ofori JK et al (2017) Whole-genome bisulfite sequencing of human pancreatic islets reveals novel differentially methylated regions in type 2 diabetes pathogenesis. Diabetes 66(4):1074–1085

    CAS  PubMed  Google Scholar 

  181. Volkmar M, Dedeurwaerder S, Cunha DA et al (2012) DNA methylation profiling identifies epigenetic dysregulation in pancreatic islets from type 2 diabetic patients. EMBO J 31(6):1405–1426

    CAS  PubMed  PubMed Central  Google Scholar 

  182. Chen R, Xia L, Tu K, Duan M et al (2018) Longitudinal personal DNA methylome dynamics in a human with a chronic condition. Nat Med 24:1930–1939

    CAS  PubMed  PubMed Central  Google Scholar 

  183. Hedman ÅK, Mendelson MM, Marioni RE et al (2017) Epigenetic patterns in blood associated with lipid traits predict incident coronary heart disease events and are enriched for results from genome-wide association studies. Circ Cardiovasc Genet 10(1):e001487

    CAS  PubMed  PubMed Central  Google Scholar 

  184. Roh TY, Cuddapah S, Zhao K (2005) Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev 19:542–552

    CAS  PubMed  PubMed Central  Google Scholar 

  185. Margueron R, Reinberg D (2010) Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet 11:285–296

    CAS  PubMed  PubMed Central  Google Scholar 

  186. Allis CD, Jenuwein T (2016) The molecular hallmarks of epigenetic control. Nat Rev Genet 17:487–500

    CAS  PubMed  Google Scholar 

  187. Khyzha N, Alizada A, Wilson MD, Fish JE (2017) Epigenetics of atherosclerosis: emerging mechanisms and methods. Trends Mol Med 23:332–347

    CAS  PubMed  Google Scholar 

  188. Matsushima S, Sadoshima J (2015) The role of sirtuins in cardiac disease. Am J Physiol Heart Circ Physiol 309:H1375–H1389

    CAS  PubMed  PubMed Central  Google Scholar 

  189. Santos L, Escande C, Denicola A (2016) Potential modulation of sirtuins by oxidative stress. Oxidative Med Cell Longev 2016:9831825

    Google Scholar 

  190. Bekkering S, Quintin J, Joosten LA et al (2014) Oxidized low-density lipoprotein induces long-term proinflammatory cytokine production and foam cell formation via epigenetic reprogramming of monocytes significance. Arterioscler Thromb Vasc Biol 34:1731–1738

    CAS  PubMed  Google Scholar 

  191. Dje N’Guessan P, Riediger F, Vardarova K et al (2009) Statins control oxidized LDL-mediated histone modifications and gene expression in cultured human endothelial cells. Arterioscler Thromb Vasc Biol 29(3):380–386

    PubMed  Google Scholar 

  192. Papait R, Cattaneo P, Kunderfranco P et al (2013) Genome-wide analysis of histone marks identifying an epigenetic signature of promoters and enhancers underlying cardiac hypertrophy. Proc Natl Acad Sci U S A 110(50):20164–20169

    CAS  PubMed  PubMed Central  Google Scholar 

  193. Greißel A, Culmes M, Burgkart R et al (2016) Histone acetylation and methylation significantly change with severity of atherosclerosis in human carotid plaques. Cardiovasc Pathol 25(2):79–86

    PubMed  Google Scholar 

  194. Tomita K, Barnes PJ, Adcock IM (2003) The effect of oxidative stress on histone acetylation and IL-8 release. Biochem Biophys Res Commun 301:572–577

    CAS  PubMed  Google Scholar 

  195. Bartling TR, Subbaram S, Clark RR et al (2014) Redox-sensitive gene-regulatory events controlling aberrant matrix metalloproteinase-1 expression. Free Radic Biol Med 74:99–107

    CAS  PubMed  PubMed Central  Google Scholar 

  196. Lehrke M, Greif M, Broedl UC et al (2009) MMP-1 serum levels predict coronary atherosclerosis in humans. Cardiovasc Diabetol 2009:8–50

    Google Scholar 

  197. Wang X, Vatamaniuk MZ, Roneker CA et al (2011a) Knockouts of SOD1 and GPX1 exert different impacts on murine islet function and pancreatic integrity. Antioxid Redox Signal 14:391–401

    PubMed  PubMed Central  Google Scholar 

  198. Gupta J, Tikoo K (2012) Involvement of insulin-induced reversible chromatin remodeling in altering the expression of oxidative stress-responsive genes under hyperglycemia in 3T3-L1 preadipocytes. Gene 504:181–191

    CAS  PubMed  Google Scholar 

  199. Kikuchi H, Kuribayashi F, Kiwaki N, Takami Y, Nakayama T (2011) GCN5 regulates the superoxide-generating system in leukocytes via controlling gp91-phox gene expression. J Immunol 186:3015–3022

    CAS  PubMed  Google Scholar 

  200. Miao F, Gonzalo IG, Lanting L, Natarajan R (2004) In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions. J Biol Chem 279:18091–18097

    CAS  PubMed  Google Scholar 

  201. Kaur H, Chen S, Xin X et al (2006) Diabetes-induced extracellular matrix protein expression is mediated by transcription coactivator p300. Diabetes 55:3104–3111

    CAS  PubMed  Google Scholar 

  202. Xu B, Chiu J, Feng B, Chen S, Chakrabarti S (2008) PARP activation and the alteration of vasoactive factors and extracellular matrix protein in retina and kidney in diabetes. Diabetes Metab Res Rev 24:404–412

    CAS  PubMed  Google Scholar 

  203. Pacher P, Szabó C (2007) Role of poly(ADP-ribose) polymerase 1 (PARP-1) in cardiovascular diseases: the therapeutic potential of PARP inhibitors. Cardiovasc Drug Rev 25(3):235–260

    CAS  PubMed  PubMed Central  Google Scholar 

  204. Pons D, de Vries FR, van den Elsen PJ et al (2009) Epigenetic histone acetylation modifiers in vascular remodelling: new targets for therapy in cardiovascular disease. Eur Heart J 30(3):266–277

    CAS  PubMed  Google Scholar 

  205. Osoata GO, Yamamura S, Ito M, Vuppusetty C, Adcock IM, Barnes PJ et al (2009) Nitration of distinct tyrosine residues causes inactivation of histone deacetylase 2. Biochem Biophys Res Commun 384:366–371

    CAS  PubMed  Google Scholar 

  206. Doyle K, Fitzpatrick FA (2010) 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 285:17417–17424

    CAS  PubMed  PubMed Central  Google Scholar 

  207. Adenuga D, Yao H, March TH et al (2009) Histone deacetylase 2 is phosphorylated, ubiquitinated, and degraded by cigarette smoke. Am J Respir Cell Mol Biol 40:464–473

    CAS  PubMed  Google Scholar 

  208. Rajendrasozhan S, Yang SR, Edirisinghe I et al (2008) Deacetylases and NF-kappaB in redox regulation of cigarette smoke-induced lung inflammation: epigenetics in pathogenesis of COPD. Antioxid Redox Signal 10:799–811

    CAS  PubMed  Google Scholar 

  209. Sathishkumar C, Prabu P, Balakumar M et al (2016) Augmentation of histone deacetylase 3 (HDAC3) epigenetic signature at the interface of proinflammation and insulin resistance in patients with type 2 diabetes. Clin Epigenetics 8:125

    PubMed  PubMed Central  Google Scholar 

  210. Zhu H, Shan L, Schiller PW et al (2010) Histone deacetylase-3 activation promotes tumor necrosis factor-alpha (TNF-alpha) expression in cardiomyocytes during lipopolysaccharide stimulation. J Biol Chem 285:9429–9436

    CAS  PubMed  PubMed Central  Google Scholar 

  211. Choi JH, Nam KH, Kim J et al (2005) Trichostatin A exacerbates atherosclerosis in low density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol 25:2404–2409

    CAS  PubMed  Google Scholar 

  212. Okamoto H, Fujioka Y, Takahashi A et al (2006) Trichostatin A, an inhibitor of histone deacetylase, inhibits smooth muscle cell proliferation via induction of p21 (WAF1). J Atheroscler Thromb 13:183–191

    CAS  PubMed  Google Scholar 

  213. Pandey D, Sikka G, Bergman Y et al (2014) Transcriptional regulation of endothelial arginase 2 by histone deacetylase 2. Arterioscler Thromb Vasc Biol 34:1556–1566

    CAS  PubMed  PubMed Central  Google Scholar 

  214. Ago T, Liu T, Zhai P, Chen W, Li H, Molkentin JD et al (2008) A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy. Cell 133:978–993

    CAS  PubMed  Google Scholar 

  215. Zhang M, Brewer AC, Schroder K et al (2010) NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc Natl Acad Sci U S A 107:18121–18126

    CAS  PubMed  PubMed Central  Google Scholar 

  216. Usui T, Okada M, Mizuno W et al (2012) HDAC4 mediates development of hypertension via vascular inflammation in spontaneous hypertensive rats. Am J Physiol Heart Circ Physiol 302:H1894–H1904

    CAS  PubMed  Google Scholar 

  217. Kim J, Hwangbo C, Hu X et al (2015) Restoration of impaired endothelial myocyte enhancer factor 2 function rescues pulmonary arterial hypertension. Circulation 131:190–199

    PubMed  Google Scholar 

  218. Rajendran R, Garva R, Krstic-Demonacos M, Demonacos C (2011) Sirtuins: molecular traffic lights in the crossroad of oxidative stress, chromatin remodeling, and transcription. J Biomed Biotechnol 2011:368276

    PubMed  PubMed Central  Google Scholar 

  219. Zarzuelo MJ, Lopez-Sepulveda R, Sanchez M et al (2013) SIRT1 inhibits NADPH oxidase activation and protects endothelial function in the rat aorta: implications for vascular aging. Biochem Pharmacol 85:1288–1296

    CAS  PubMed  Google Scholar 

  220. de Kreutzenberg SV, Ceolotto G, Papparella I et al (2010) Downregulation of the longevity-associated protein sirtuin 1 in insulin resistance and metabolic syndrome: potential biochemical mechanisms. Diabetes 59:1006–1015

    PubMed  PubMed Central  Google Scholar 

  221. Yamamoto T, Tamaki K, Shirakawa K et al (2016) Cardiac Sirt1 mediates the cardioprotective effect of caloric restriction by suppressing local complement system activation after ischemia-reperfusion. Am J Physiol Heart Circ Physiol 310:H1003–H1014

    PubMed  Google Scholar 

  222. Bonello S, Zahringer C, BelAiba RS, Djordjevic T, Hess J, Michiels C et al (2007) Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol 27:755–761

    CAS  PubMed  Google Scholar 

  223. Hwang JW, Yao H, Caito S, Sundar IK, Rahman I (2013) Redox regulation of SIRT1 in inflammation and cellular senescence. Free Radic Biol Med 61:95–110

    CAS  PubMed  Google Scholar 

  224. Canto C, Sauve AA, Bai P (2013) Crosstalk between poly(ADP-ribose) polymerase and sirtuin enzymes. Mol Asp Med 34:1168–1201

    CAS  Google Scholar 

  225. Puthanveetil P, Zhang D, Wang Y et al (2012) Diabetes triggers a PARP1 mediated death pathway in the heart through participation of FoxO1. J Mol Cell Cardiol 53(5):677–686

    CAS  PubMed  Google Scholar 

  226. Narne P, Pandey V, Phanithi PB (2018) Role of nitric oxide and hydrogen sulfide in ischemic stroke and the emergent epigenetic underpinnings. Mol Neurobiol. https://doi.org/10.1007/s12035-018-1141-6

    PubMed  Google Scholar 

  227. Narne P, Pandey V, Simhadri PK, Phanithi PB (2017) Poly(ADP-ribose)polymerase-1 hyperactivation in neurodegenerative diseases: the death knell tolls for neurons. Semin Cell Dev Biol 63:154–166

    CAS  PubMed  Google Scholar 

  228. Bannister AJ, Kouzarides T (2005) Reversing histone methylation. Nature 436:1103–1106

    CAS  PubMed  Google Scholar 

  229. Chervona Y, Costa M (2012) The control of histone methylation and gene expression by oxidative stress, hypoxia, and metals. Free Radic Biol Med 53:1041–1047

    CAS  PubMed  PubMed Central  Google Scholar 

  230. Mentch SJ, Mehrmohamadi M, Huang L et al (2015) Histone methylation dynamics and gene regulation occur through the sensing of one-carbon metabolism. Cell Metab 22:861–873

    CAS  PubMed  PubMed Central  Google Scholar 

  231. Liu T, Wu C, Jain MR et al (1854) Master redox regulator Trx1 upregulates SMYD1 & modulates lysine methylation. Biochim Biophys Acta 2015:1816–1822

    Google Scholar 

  232. Franklin S, Kimball T, Rasmussen TL et al (2016) The chromatin-binding protein Smyd1 restricts adult mammalian heart growth. Am J Physiol Heart Circ Physiol 311:H1234–H1247

    PubMed  PubMed Central  Google Scholar 

  233. Zhang QJ, Liu ZP (2015) Histone methylations in heart development, congenital and adult heart diseases. Epigenomics 7:321–330

    CAS  PubMed  Google Scholar 

  234. Rajasekar P, O’Neill CL, Eeles L et al (2015) Epigenetic changes in endothelial progenitors as a possible cellular basis for glycemic memory in diabetic vascular complications. J Diabetes Res 2015:436879

    PubMed  PubMed Central  Google Scholar 

  235. Al-Sawaf O, Clarner T, Fragoulis A et al (2015) Nrf2 in health and disease: current and future clinical implications. Clin Sci 129:989–999

    CAS  Google Scholar 

  236. Friso S, Carvajal CA, Fardella CE, Olivieri O (2015) Epigenetics and arterial hypertension: the challenge of emerging evidence. Transl Res 165:154–165

    CAS  PubMed  Google Scholar 

  237. Li J, Braganza A, Sobol RW (2013) Base excision repair facilitates a functional relationship between guanine oxidation and histone demethylation. Antioxid Redox Signal 18:2429–2443

    CAS  PubMed  PubMed Central  Google Scholar 

  238. Hickok JR, Vasudevan D, Antholine WE, Thomas DD (2013) Nitric oxide modifies global histone methylation by inhibiting Jumonji C domain-containing demethylases. J Biol Chem 288:16004–16015

    CAS  PubMed  PubMed Central  Google Scholar 

  239. He C, Larson-Casey JL, Gu L, Ryan AJ, Murthy S, Carter AB (2016) Cu,Zn-SOD-mediated redox regulation of Jmjd3 modulates macrophage polarization and pulmonary fibrosis. Am J Respir Cell Mol Biol 55:58–71

    CAS  PubMed  PubMed Central  Google Scholar 

  240. Tausendschon M, Dehne N, Brune B (2011) Hypoxia causes epigenetic gene regulation in macrophages by attenuating Jumonji histone demethylase activity. Cytokine 53:256–262

    PubMed  Google Scholar 

  241. Zhang QJ, Chen HZ, Wang L, Liu DP, Hill JA, Liu ZP (2011) The histone trimethyllysine demethylase JMJD2A promotes cardiac hypertrophy in response to hypertrophic stimuli in mice. J Clin Invest 121:2447–2456

    CAS  PubMed  PubMed Central  Google Scholar 

  242. Matouk CC, Marsden PA (2008) Epigenetic regulation of vascular endothelial gene expression. Circ Res 102:873–887

    CAS  PubMed  Google Scholar 

  243. Gan Y, Shen YH, Wang J et al (2005) Role of histone deacetylation in cell-specific expression of endothelial nitric-oxide synthase. J Biol Chem 280:16467–16475

    CAS  PubMed  Google Scholar 

  244. Fish JE, Matouk CC, Rachlis A et al (2005) The expression of endothelial nitric-oxide synthase is controlled by a cell-specific histone code. J Biol Chem 280:24824–24838

    CAS  PubMed  Google Scholar 

  245. Wilcox JN, Subramanian RR, Sundell CL et al (1997) Expression of multiple isoforms of nitric oxide synthase in normal and atherosclerotic vessels. Arterioscler Thromb Vasc Biol 17:2479–2488

    CAS  PubMed  Google Scholar 

  246. Chan GC, Fish JE, Mawji IA et al (2005) Epigenetic basis for the transcriptional hyporesponsiveness of the human inducible nitric oxide synthase gene in vascular endothelial cells. J Immunol 175:3846–3861

    CAS  PubMed  Google Scholar 

  247. Chartrain NA, Geller DA, Koty PP et al (1994) Molecular cloning, structure, and chromosomal localization of the human inducible nitric oxide synthase gene. J Biol Chem 269:6765–6772

    CAS  PubMed  Google Scholar 

  248. Pirola L, Balcerczyk A, Tothill RW et al (2011) Genome-wide analysis distinguishes hyperglycemia regulated epigenetic signatures of primary vascular cells. Genome Res 21:1601–1615

    CAS  PubMed  PubMed Central  Google Scholar 

  249. Estève PO, Chin HG, Benner J et al (2009) Regulation of DNMT1 stability through SET7-mediated lysine methylation in mammalian cells. Proc Natl Acad Sci U S A 106:5076–5081

    PubMed  PubMed Central  Google Scholar 

  250. Deering TG, Ogihara T, Trace AP et al (2009) Methyltransferase Set7/9 maintains transcription and euchromatin structure at islet-enriched genes. Diabetes 58:185–193

    CAS  PubMed  PubMed Central  Google Scholar 

  251. Maganti AV, Maier B, Tersey SA et al (2015) Transcriptional activity of the islet β cell factor Pdx1 is augmented by lysine methylation catalyzed by the methyltransferase Set7/9. J Biol Chem 290:9812–9822

    CAS  PubMed  PubMed Central  Google Scholar 

  252. Chakrabarti SK, Francis J, Ziesmann SM et al (2003) Covalent histone modifications underlie the developmental regulation of insulin gene transcription in pancreatic beta cells. J Biol Chem 278(26):23617–23623

    CAS  PubMed  Google Scholar 

  253. Villeneuve LM, Reddy MA, Lanting LL et al (2008) Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes. Proc Natl Acad Sci U S A 105(26):9047–9052

    CAS  PubMed  PubMed Central  Google Scholar 

  254. Villeneuve LM, Kato M, Reddy MA et al (2010) Enhanced levels of microRNA-125b in vascular smooth muscle cells of diabetic db/db mice lead to increased inflammatory gene expression by targeting the histone methyltransferase Suv39h1. Diabetes 59(11):2904–2915

    CAS  PubMed  PubMed Central  Google Scholar 

  255. Leung A, Trac C, Jin W, Lanting L et al (2013) Novel long noncoding RNAs are regulated by angiotensin II in vascular smooth muscle cells. Circ Res 113(3):266–278

    CAS  PubMed  PubMed Central  Google Scholar 

  256. Chen J, Zhang J, Yang J et al (2017) Histone demethylase KDM3a, a novel regulator of vascular smooth muscle cells, controls vascular neointimal hyperplasia in diabetic rats. Atherosclerosis 257:152–163

    CAS  PubMed  Google Scholar 

  257. Chen Z, Miao F, Paterson AD et al (2016) Epigenomic profiling reveals an association between persistence of DNA methylation and metabolic memory in the DCCT/EDIC type 1 diabetes cohort. Proc Natl Acad Sci U S A 113(21):E3002–E3011

    CAS  PubMed  PubMed Central  Google Scholar 

  258. Paneni F, Mocharla P, Akhmedov A et al (2012) Gene silencing of the mitochondrial adaptor p66(Shc) suppresses vascular hyperglycemic memory in diabetes. Circ Res 111(3):278–289

    CAS  PubMed  Google Scholar 

  259. Paneni F, Volpe M, Lüscher TF, Cosentino F (2013) SIRT1, p66(Shc), and Set7/9 in vascular hyperglycemic memory: bringing all the strands together. Diabetes 62(6):1800–1807

    CAS  PubMed  PubMed Central  Google Scholar 

  260. Keating ST, Ziemann M, Okabe J et al (2014) Deep sequencing reveals novel Set7 networks. Cell Mol Life Sci 71(22):4471–4486

    CAS  PubMed  Google Scholar 

  261. Francia P, Cosentino F, Schiavoni M et al (2009) p66(Shc) protein, oxidative stress, and cardiovascular complications of diabetes: the missing link. J Mol Med (Berl) 87(9):885–891

    CAS  Google Scholar 

  262. Costantino S, Paneni F, Mitchell K et al (2018) Hyperglycaemia-induced epigenetic changes drive persistent cardiac dysfunction via the adaptor p66Shc. Int J Cardiol 268:179–186

    PubMed  Google Scholar 

  263. Costantino S, Paneni F, Battista R et al (2017) Impact of glycemic variability on chromatin remodeling, oxidative stress, and endothelial dysfunction in patients with type 2 diabetes and with target HbA1c levels. Diabetes 66(9):2472–2482

    CAS  PubMed  Google Scholar 

  264. Zhou S, Chen HZ, Wan YZ et al (2011) Repression of P66Shc expression by SIRT1 contributes to the prevention of hyperglycemia-induced endothelial dysfunction. Circ Res 109(6):639–648

    CAS  PubMed  Google Scholar 

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Narne, P. (2019). Epigenetic Basis of Oxidative Stress in Diabetic Coronary Atherosclerosis: A Shift in Focus from Genetic Prerogative. In: Chakraborti, S., Dhalla, N., Dikshit, M., Ganguly, N. (eds) Modulation of Oxidative Stress in Heart Disease. Springer, Singapore. https://doi.org/10.1007/978-981-13-8946-7_18

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