Epigenetic modifications and diabetic nephropathy

Kidney Research and Clinical Practice

Volumn 31, Issue 3, 2012, Pages 139-150

  Reddy, Marpadga A ^a   Park, Jung Tak ^a   Natarajan, Rama ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Chromatin; Diabetic nephropathy; DNA methylation; Epigenomics; Histone modifications; Metabolic memory

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ANTIDIABETIC AGENT; BIOLOGICAL MARKER; DNA; HISTONE; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H4; INSULIN; LYSINE; UNTRANSLATED RNA;

CHROMATIN STRUCTURE; DIABETIC NEPHROPATHY; DISEASE ASSOCIATION; DNA METHYLATION; DNA MODIFICATION; DNA SEQUENCE; EPIGENETICS; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENETIC SUSCEPTIBILITY; GLYCEMIC CONTROL; HIGH THROUGHPUT SEQUENCING; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; REVIEW;

EID: 84879193787     PISSN: 22119132     EISSN: 22119140     Source Type: Journal    
DOI: 10.1016/j.krcp.2012.07.004     Document Type: Review

References (149)

1. F.N. Ziyadeh Mediators of diabetic renal disease: the case for TGF-Beta as the major mediator J Am Soc Nephrol 15 Suppl 1 2004 S55 S57
2. A.E. Decleves, and K. Sharma New pharmacological treatments for improving renal outcomes in diabetes Nat Rev Nephrol 6 2010 371 380
3. R. Ramasamy, S.F. Yan, and A.M. Schmidt Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications Ann N Y Acad Sci 1243 2011 88 102
4. M. Brownlee The pathobiology of diabetic complications: a unifying mechanism Diabetes 54 2005 1615 1625
5. D.J. Leehey, A.K. Singh, N. Alavi, and R. Singh Role of angiotensin II in diabetic nephropathy Kidney Int Suppl 77 2000 S93 S98
6. F.C. Brosius 3rd New insights into the mechanisms of fibrosis and sclerosis in diabetic nephropathy Rev Endocr Metab Disord 9 2008 245 254
7. L.M. Villeneuve, and R. Natarajan The role of epigenetics in the pathology of diabetic complications Am J Physiol Renal Physiol 299 2010 F14 F25
8. L. Pirola, A. Balcerczyk, J. Okabe, and A. El-Osta Epigenetic phenomena linked to diabetic complications Nat Rev Endocrinol 6 2010 665 675
9. K. Susztak, and E.P. Böttinger Diabetic nephropathy: a frontier for personalized medicine J Am Soc Nephrol 17 2006 361 367
10. K.I. Woroniecka, A.S. Park, D. Mohtat, D.B. Thomas, J.M. Pullman, and K. Susztak Transcriptome analysis of human diabetic kidney disease Diabetes 60 2011 2354 2369
11. M.C. Thomas, P.H. Groop, and K. Tryggvason Towards understanding the inherited susceptibility for nephropathy in diabetes Curr Opin Nephrol Hypertens 21 2012 195 202
12. H. Rincon-Choles, F. Thameem, D.M. Lehman, R. Arya, N. Arar, R. Duggirala, M.P. Stern, and H.E. Abboud Genetic basis of diabetic nephropathy Am J Ther 12 2005 555 561
13. R.L. Jirtle, and M.K. Skinner Environmental epigenomics and disease susceptibility Nat Rev Genet 8 2007 253 262
14. C. Ling, and L. Groop Epigenetics: a molecular link between environmental factors and type 2 diabetes Diabetes 58 2009 2718 2725
15. A.D. Goldberg, C.D. Allis, and E. Bernstein Epigenetics: a landscape takes shape Cell 128 2007 635 638
16. R. Bonasio, S. Tu, and D. Reinberg Molecular signals of epigenetic states Science 330 2010 612 616
17. T. Kouzarides Chromatin modifications and their function Cell 128 2007 693 705
18. T.B. Miranda, and P.A. Jones DNA methylation: the nuts and bolts of repression J Cell Physiol 213 2007 384 390
19. G. Natoli Maintaining cell identity through global control of genomic organization Immunity 33 2010 12 24
20. A. Portela, and M. Esteller Epigenetic modifications and human disease Nat Biotechnol 28 2010 1057 1068
21. R. Feil, and M.F. Fraga Epigenetics and the environment: emerging patterns and implications Nat Rev Genet 13 2011 97 109
22. R. Woroniecki, A.B. Gaikwad, and K. Susztak Fetal environment, epigenetics, and pediatric renal disease Pediatr Nephrol 26 2011 705 711
23. J. Fagerudd, C. Forsblom, K. Pettersson-Fernholm, M. Saraheimo, J. Wadén, M. Rönnback, M. Rosengård-Bärlund, C.G. Björkesten, L. Thorn, M. Wessman, and P.H. Groop Low birth weight does not increase the risk of nephropathy in Finnish type 1 diabetic patients Nephrol Dial Transplant 21 2006 2159 2165
24. K. Luger, A.W. Mader, R.K. Richmond, D.F. Sargent, and T.J. Richmond Crystal structure of the nucleosome core particle at 2.8 A resolution Nature 389 1997 251 260
25. V.W. Zhou, A. Goren, and B.E. Bernstein Charting histone modifications and the functional organization of mammalian genomes Nat Rev Genet 12 2011 7 18
26. B.E. Bernstein, A. Meissner, and E.S. Lander The mammalian epigenome Cell 128 2007 669 681
27. O.J. Sansom, K. Maddison, and A.R. Clarke Mechanisms of disease: methyl-binding domain proteins as potential therapeutic targets in cancer Nat Clin Pract Oncol 4 2007 305 315
28. S.C. Wu, and Y. Zhang Active DNA demethylation: many roads lead to Rome Nat Rev Mol Cell Biol 11 2010 607 620
29. Z.X. Chen, and A.D. Riggs DNA methylation and demethylation in mammals J Biol Chem 286 2011 18347 18353
30. T.R. Haines, D.I. Rodenhiser, and P.J. Ainsworth Allele-specific non-CpG methylation of the Nf1 gene during early mouse development Dev Biol 240 2001 585 598
31. B.H. Ramsahoye, D. Biniszkiewicz, F. Lyko, V. Clark, A.P. Bird, and R. Jaenisch Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a Proc Natl Acad Sci U S A 97 2000 5237 5242
32. J.A. Law, and S.E. Jacobsen Establishing, maintaining and modifying DNA methylation patterns in plants and animals Nat Rev Genet 11 2010 204 220
33. H. Han, C.C. Cortez, X. Yang, P.W. Nichols, P.A. Jones, and G. Liang DNA methylation directly silences genes with non-CpG island promoters and establishes a nucleosome occupied promoter Hum Mol Genet 20 2011 4299 4310
34. P.A. Jones, and S.B. Baylin The epigenomics of cancer Cell 128 2007 683 692
35. T.K. Kelly, D.D. De Carvalho, and P.A. Jones Epigenetic modifications as therapeutic targets Nat Biotechnol 28 2010 1069 1078
36. S.R. Bhaumik, E. Smith, and A. Shilatifard Covalent modifications of histones during development and disease pathogenesis Nat Struct Mol Biol 14 2007 1008 1016
37. C.D. Allis, S.L. Berger, J. Cote, S. Dent, T. Jenuwien, T. Kouzarides, L. Pillus, D. Reinberg, Y. Shi, R. Shiekhattar, A. Shilatifard, J. Workman, and Y. Zhang New nomenclature for chromatin-modifying enzymes Cell 131 2007 633 636
38. S.Y. Roth, J.M. Denu, and C.D. Allis Histone acetyltransferases Annu Rev Biochem 70 2001 81 120
39. Y.F. Ramos, M.S. Hestand, M. Verlaan, E. Krabbendam, Y. Ariyurek, M. van Galen, H. van Dam, G.J. van Ommen, J.T. den Dunnen, A. Zantema, and P.A. t Hoen Genome-wide assessment of differential roles for p300 and CBP in transcription regulation Nucleic Acids Res 38 2010 5396 5408
40. T.K. Kim, M. Hemberg, J.M. Gray, A.M. Costa, D.M. Bear, J. Wu, D.A. Harmin, M. Laptewicz, K. Barbara-Haley, S. Kuersten, E. Markenscoff- Papadimitriou, D. Kuhl, H. Bito, P.F. Worley, G. Kreiman, and M.E. Greenberg Widespread transcription at neuronal activity-regulated enhancers Nature 465 2010 182 187
41. A. Visel, M.J. Blow, Z. Li, T. Zhang, J.A. Akiyama, A. Holt, I. Plajzer-Frick, M. Shoukry, C. Wright, F. Chen, V. Afzal, B. Ren, E.M. Rubin, and L.A. Pennacchio ChIP-seq accurately predicts tissue-specific activity of enhancers Nature 457 2009 854 858
42. F. Jin, Y. Li, B. Ren, and R. Natarajan Enhancers: multi-dimensional signal integrators Transcription 2 2011 226 230
43. X.J. Yang, and E. Seto HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention Oncogene 26 2007 5310 5318
44. O.M. Dovey, C.T. Foster, and S.M. Cowley Histone deacetylase 1 (HDAC1), but not HDAC2, controls embryonic stem cell differentiation Proc Natl Acad Sci U S A 107 2010 8242 8247
45. A. Margariti, A. Zampetaki, Q. Xiao, B. Zhou, E. Karamariti, D. Martin, X. Yin, M. Mayr, H. Li, Z. Zhang, E. De Falco, Y. Hu, G. Cockerill, Q. Xu, and L. Zeng Histone deacetylase 7 controls endothelial cell growth through modulation of beta-catenin Circ Res 106 2010 1202 1211
46. C.M. Trivedi, Y. Luo, Z. Yin, M. Zhang, W. Zhu, T. Wang, T. Floss, M. Goettlicher, P.R. Noppinger, W. Wurst, V.A. Ferrari, C.S. Abrams, P.J. Gruber, and J.A. Epstein Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3 beta activity Nat Med 13 2007 324 331
47. B.R. Selvi, D.V. Mohankrishna, Y.B. Ostwal, and T.K. Kundu Small molecule modulators of histone acetylation and methylation: a disease perspective Biochim Biophys Acta 810-828 1799 2010
48. Y. Shi Histone lysine demethylases: emerging roles in development, physiology and disease Nat Rev Genet 8 2007 829 833
49. Y. Shi, and J.R. Whetstine Dynamic regulation of histone lysine methylation by demethylases Mol Cell 25 2007 1 14
50. G.C. Hon, R.D. Hawkins, and B. Ren Predictive chromatin signatures in the mammalian genome Hum Mol Genet 18 2009 R195 R201
51. A. Barski, S. Cuddapah, K. Cui, T.Y. Roh, D.E. Schones, Z. Wang, G. Wei, I. Chepelev, and K. Zhao High-resolution profiling of histone methylations in the human genome Cell 129 2007 823 837
52. F. Jin, Y. Li, B. Ren, and R. Natarajan PU.1 and C/EBP(alpha) synergistically program distinct response to NF-kappaB activation through establishing monocyte specific enhancers Proc Natl Acad Sci U S A 108 2011 5290 5295
53. P.C. Taberlay, T.K. Kelly, C.C. Liu, J.S. You, D.D. De Carvalho, T.B. Miranda, X.J. Zhou, G. Liang, and P.A. Jones Polycomb-repressed genes have permissive enhancers that initiate reprogramming Cell 147 2011 1283 1294
54. H.M. Herz, S. Nakanishi, and A. Shilatifard The curious case of bivalent marks Dev Cell 17 2009 301 303
55. H. Cedar, and Y. Bergman Linking DNA methylation and histone modification: patterns and paradigms Nat Rev Genet 10 2009 295 304
56. F. Giacco, and M. Brownlee Oxidative stress and diabetic complications Circ Res 107 2010 1058 1070
57. M.A. Reddy, and R. Natarajan Epigenetic mechanisms in diabetic vascular complications Cardiovasc Res 90 2011 421 429
58. F. Bantignies, and G. Cavalli Cellular memory and dynamic regulation of polycomb group proteins Curr Opin Cell Biol 18 2006 275 283
59. N.J. Francis, N.E. Follmer, M.D. Simon, G. Aghia, and J.D. Butler Polycomb proteins remain bound to chromatin and DNA during DNA replication in vitro Cell 137 2009 110 122
60. H.D. Morgan, H.G. Sutherland, D.I. Martin, and E. Whitelaw Epigenetic inheritance at the agouti locus in the mouse Nat Genet 23 1999 314 318
61. R.A. Waterland, M. Travisano, K.G. Tahiliani, M.T. Rached, and S. Mirza Methyl donor supplementation prevents transgenerational amplification of obesity Int J Obes (Lond) 32 2008 1373 1379
62. T. Pentinat, M. Ramon-Krauel, J. Cebria, R. Diaz, and J.C. Jimenez-Chillaron Transgenerational inheritance of glucose intolerance in a mouse model of neonatal overnutrition Endocrinology 151 2010 5617 5623
63. A. Groth, A. Corpet, A.J. Cook, D. Roche, J. Bartek, J. Lukas, and G. Almouzni Regulation of replication fork progression through histone supply and demand Science 318 2007 1928 1931
64. A. Ceriello Hypothesis: the metabolic memory, the new challenge of diabetes Diabetes Res Clin Pract 86 Suppl 1 2009 S2 S6
65. Writing Team for the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group Effect of intensive therapy on the microvascular complications of type 1 diabetes mellitus JAMA 287 2002 2563 2569
66. Writing Team for the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group 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 2003 2159 2167
67. R. Pop-Busui, P.A. Low, B.H. Waberski, C.L. Martin, J.W. Albers, E.L. Feldman, C. Sommer, P.A. Cleary, J.M. Lachin, and W.H. Herman Effects of prior intensive insulin therapy on cardiac autonomic nervous system function in type 1 diabetes mellitus: the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications study (DCCT/EDIC) Circulation 119 2009 2886 2893
68. I.H. de Boer, W. Sun, P.A. Cleary, J.M. Lachin, M.E. Molitch, M.W. Steffes, and B. Zinman Intensive diabetes therapy and glomerular filtration rate in type 1 diabetes N Engl J Med 365 2011 2366 2376
69. N.H. White, W. Sun, P.A. Cleary, R.P. Danis, M.D. Davis, D.P. Hainsworth, L.D. Hubbard, J.M. Lachin, and D.M. Nathan Prolonged effect of intensive therapy on the risk of retinopathy complications in patients with type 1 diabetes mellitus: 10 years after the Diabetes Control and Complications Trial Arch Ophthalmol 126 2008 1707 1715
70. I.H. de Boer, T.C. Rue, P.A. Cleary, J.M. Lachin, M.E. Molitch, M.W. Steffes, W. Sun, B. Zinman, J.D. Brunzell, N.H. White, R.P. Danis, M.D. Davis, D. Hainsworth, L.D. Hubbard, and D.M. Nathan Long-term renal outcomes of patients with type 1 diabetes mellitus and microalbuminuria: an analysis of the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications cohort Arch Intern Med 171 2011 412 420
71. S. Colagiuri, C.A. Cull, and R.R. Holman Are lower fasting plasma glucose levels at diagnosis of type 2 diabetes associated with improved outcomes? U.K. prospective diabetes study 61 Diabetes Care 25 2002 1410 1417
72. R.R. Holman, S.K. Paul, M.A. Bethel, D.R. Matthews, and H.A. Neil 10-year follow-up of intensive glucose control in type 2 diabetes N Engl J Med 359 2008 1577 1589
73. A. Patel, S. MacMahon, J. Chalmers, B. Neal, L. Billot, M. Woodward, M. Marre, M. Cooper, P. Glasziou, D. Grobbee, P. Hamet, S. Harrap, S. Heller, L. Liu, G. Mancia, C.E. Mogensen, C. Pan, N. Poulter, A. Rodgers, B. Williams, S. Bompoint, B.E. de Galan, R. Joshi, and F. Travert Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes N Engl J Med 358 2008 2560 2572
74. A. Ceriello, K. Esposito, L. Piconi, M.A. Ihnat, J.E. Thorpe, R. Testa, M. Boemi, and D. Giugliano Oscillating glucose is more deleterious to endothelial function and oxidative stress than mean glucose in normal and type 2 diabetic patients Diabetes 57 2008 1349 1354
75. S. Roy, R. Sala, E. Cagliero, and M. Lorenzi Overexpression of fibronectin induced by diabetes or high glucose: phenomenon with a memory Proc Natl Acad Sci U S A 87 1990 404 408
76. A. El-Osta, D. Brasacchio, D. Yao, A. Pocai, P.L. Jones, R.G. Roeder, M.E. Cooper, and M. Brownlee Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia J Exp Med 205 2008 2409 2417
77. S.L. Li, M.A. Reddy, Q. Cai, L. Meng, H. Yuan, L. Lanting, and R. Natarajan Enhanced proatherogenic responses in macrophages and vascular smooth muscle cells derived from diabetic db/db mice Diabetes 55 2006 2611 2619
78. L.M. Villeneuve, M.A. Reddy, L.L. Lanting, M. Wang, L. Meng, and R. Natarajan 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 2008 9047 9052
79. R.L. Engerman, and T.S. Kern Progression of incipient diabetic retinopathy during good glycemic control Diabetes 36 1987 808 812
80. P.S. Chan, M. Kanwar, and R.A. Kowluru Resistance of retinal inflammatory mediators to suppress after reinstitution of good glycemic control: novel mechanism for metabolic memory J Diabetes Complications 24 2010 55 63
81. R.A. Kowluru Effect of reinstitution of good glycemic control on retinal oxidative stress and nitrative stress in diabetic rats Diabetes 52 2003 818 823
82. R.A. Kowluru, S.N. Abbas, and S. Odenbach Reversal of hyperglycemia and diabetic nephropathy: effect of reinstitution of good metabolic control on oxidative stress in the kidney of diabetic rats J Diabetes Complications 18 2004 282 288
83. Q. Zhong, and R.A. Kowluru Epigenetic changes in mitochondrial superoxide dismutase in the retina and the development of diabetic retinopathy Diabetes 60 2011 1304 1313
84. S.F. Yan, R. Ramasamy, L.G. Bucciarelli, T. Wendt, L.K. Lee, B.I. Hudson, D.M. Stern, E. Lalla, D.U. Yan, S. Rong, L.L. Naka, and Y. Schmidt AM: RAGE and its ligands: a lasting memory in diabetic complications? Diab Vasc Dis Res 1 2004 10 20
85. S.F. Yan, R. Ramasamy, and A.M. Schmidt Mechanisms of disease: advanced glycation end-products and their receptor in inflammation and diabetes complications Nat Clin Pract Endocrinol Metab 4 2008 285 293
86. D.C. Dolinoy, and R.L. Jirtle Environmental epigenomics in human health and disease Environ Mol Mutagen 49 2008 4 8
87. C. Ling, S. Del Guerra, R. Lupi, T. Rönn, C. Granhall, H. Luthman, P. Masiello, P. Marchetti, L. Groop, and S. Del Prato Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion Diabetologia 51 2008 615 622
88. R. Barres, M.E. Osler, J. Yan, A. Rune, T. Fritz, K. Caidahl, A. Krook, and J.R. Zierath Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density Cell Metab 10 2009 189 198
89. A. Nikoshkov, V. Sunkari, O. Savu, E. Forsberg, S.B. Catrina, and K. Brismar Epigenetic DNA methylation in the promoters of the Igf1 receptor and insulin receptor genes in db/db mice Epigenetics 6 2011 405 409
90. B.T. Yang, T.A. Dayeh, C.L. Kirkpatrick, J. Taneera, R. Kumar, L. Groop, C.B. Wollheim, M.D. Nitert, and C. Ling Insulin promoter DNA methylation correlates negatively with insulin gene expression and positively with HbA(1c) levels in human pancreatic islets Diabetologia 54 2011 360 367
91. J. Zhao, J. Goldberg, J.D. Bremner, and V. Vaccarino Global DNA methylation is associated with insulin resistance: a monozygotic twin study Diabetes 61 2012 542 546
92. K.A. Fawcett, and I. Barroso The genetics of obesity: FTO leads the way Trends Genet 26 2010 266 274
93. G. Toperoff, D. Aran, J.D. Kark, M. Rosenberg, T. Dubnikov, B. Nissan, J. Wainstein, Y. Friedlander, E. Levy-Lahad, B. Glaser, and A. Hellman Genome-wide survey reveals predisposing diabetes type 2-related DNA methylation variations in human peripheral blood Hum Mol Genet 21 2012 371 383
94. E.P. Brennan, M. Ehrich, D.P. Brazil, J.K. Crean, M. Murphy, D.M. Sadlier, F. Martin, C. Godson, D. van den Boom, A.P. Maxwell, and D.A. Savage DNA methylation profiling in cell models of diabetic nephropathy Epigenetics 5 2010 396 401
95. K.T. Williams, T.A. Garrow, and K.L. Schalinske Type I diabetes leads to tissue-specific DNA hypomethylation in male rats J Nutr 138 2008 2064 2069
96. K.T. Williams, and K.L. Schalinske Tissue-specific alterations of methyl group metabolism and DNA hypermethylation in the Zucker (type 2) diabetic fatty rat Diabetes Metab Res Rev 28 2011 123 131
97. C.G. Bell, A.E. Teschendorff, V.K. Rakyan, A.P. Maxwell, S. Beck, and D.A. Savage Genome-wide DNA methylation analysis for diabetic nephropathy in type 1 diabetes mellitus BMC Med Genomics 3 2010 33 42
98. C. Sapienza, J. Lee, J. Powell, O. Erinle, F. Yafai, J. Reichert, E.S. Siraj, and M. Madaio DNA methylation profiling identifies epigenetic differences between diabetes patients with ESRD and diabetes patients without nephropathy Epigenetics 6 2011 20 28
99. L. Pirola, A. Balcerczyk, R.W. Tothill, I. Haviv, A. Kaspi, S. Lunke, M. Ziemann, T. Karagiannis, S. Tonna, A. Kowalczyk, B. Beresford-Smith, G. Macintyre, M. Kelong, Z. Hongyu, J. Zhu, and A. El-Osta Genome-wide analysis distinguishes hyperglycemia regulated epigenetic signatures of primary vascular cells Genome Res 21 2011 1601 1615
100. S.K. Chakrabarti, J. Francis, S.M. Ziesmann, J.C. Garmey, and R.G. Mirmira Covalent histone modifications underlie the developmental regulation of insulin gene transcription in pancreatic beta cells J Biol Chem 278 2003 23617 23623
101. J. Francis, D.A. Babu, T.G. Deering, S.K. Chakrabarti, J.C. Garmey, C. Evans-Molina, D.G. Taylor, and R.G. Mirmira Role of chromatin accessibility in the occupancy and transcription of the insulin gene by the pancreatic and duodenal homeobox factor 1 Mol Endocrinol 20 2006 3133 3145
102. J. Francis, S.K. Chakrabarti, J.C. Garmey, and R.G. Mirmira Pdx-1 links histone H3-Lys-4 methylation to RNA polymerase II elongation during activation of insulin transcription J Biol Chem 280 2005 36244 36253
103. S.E. Pinney, L.J. Jaeckle Santos, Y. Han, D.A. Stoffers, and R.A. Simmons Exendin-4 increases histone acetylase activity and reverses epigenetic modifications that silence Pdx1 in the intrauterine growth retarded rat Diabetologia 54 2011 2606 2614
104. M.M. Musri, M.C. Carmona, F.A. Hanzu, P. Kaliman, R. Gomis, and M. Parrizas Histone demethylase LSD1 regulates adipogenesis J Biol Chem 285 2010 30034 30041
105. K. Tateishi, Y. Okada, E.M. Kallin, and Y. Zhang Role of Jhdm2a in regulating metabolic gene expression and obesity resistance Nature 458 2009 757 761
106. M.L. Stitzel, P. Sethupathy, D.S. Pearson, P.S. Chines, L. Song, M.R. Erdos, R. Welch, S.C. Parker, A.P. Boyle, L.J. Scott, E.H. Margulies, M. Boehnke, T.S. Furey, G.E. Crawford, and F.S. Collins Global epigenomic analysis of primary human pancreatic islets provides insights into type 2 diabetes susceptibility loci Cell Metab 12 2010 443 455
107. S.G. Gray, and P. De Meyts Role of histone and transcription factor acetylation in diabetes pathogenesis Diabetes Metab Res Rev 21 2005 416 433
108. M.C. Haigis, and D.A. Sinclair Mammalian sirtuins: biological insights and disease relevance Annu Rev Pathol 5 2010 253 295
109. T. Nakagawa, M. Segal, B. Croker, and R.J. Johnson A breakthrough in diabetic nephropathy: the role of endothelial dysfunction Nephrol Dial Transplant 22 2007 2775 2777
110. Y. Wang, and D.C. Harris Macrophages in renal disease J Am Soc Nephrol 22 2011 21 27
111. C.C. Matouk, and P.A. Marsden Epigenetic regulation of vascular endothelial gene expression Circ Res 102 2008 873 887
112. M.A. Reddy, and R. Natarajan Epigenetics in diabetic kidney disease J Am Soc Nephrol 22 2011 2182 2185
113. J.E. Fish, C.C. Matouk, A. Rachlis, S. Lin, S.C. Tai, C. D'Abreo, and P.A. Marsden The expression of endothelial nitric-oxide synthase is controlled by a cell-specific histone code J Biol Chem 280 2005 24824 24838
114. W. Chen, M. Bacanamwo, and D.G. Harrison Activation of p300 histone acetyltransferase activity is an early endothelial response to laminar shear stress and is essential for stimulation of endothelial nitric-oxide synthase mRNA transcription J Biol Chem 283 2008 16293 16298
115. M. Nangaku Chronic hypoxia and tubulointerstitial injury: a final common pathway to end-stage renal failure J Am Soc Nephrol 17 2006 17 25
116. J.E. Fish, M.S. Yan, C.C. Matouk St, R. Bernard, J.J. Ho, A. Gavryushova, D. Srivastava, and P.A. Marsden Hypoxic repression of endothelial nitric-oxide synthase transcription is coupled with eviction of promoter histones J Biol Chem 285 2010 810 826
117. O. Takeuch, and S. Akira Epigenetic control of macrophage polarization Eur J Immunol 41 2011 2490 2493
118. F. De Santa, M.G. Totaro, E. Prosperini, S. Notarbartolo, G. Testa, and G. Natoli The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing Cell 130 2007 1083 1094
119. T. Satoh, O. Takeuchi, A. Vandenbon, K. Yasuda, Y. Tanaka, Y. Kumagai, T. Miyake, K. Matsushita, T. Okazaki, T. Saitoh, K. Honma, T. Matsuyama, K. Yui, T. Tsujimura, D.M. Standley, K. Nakanishi, K. Nakai, and S. Akira The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection Nat immunol 11 2010 936 944
120. A. Villagra, F. Cheng, H.W. Wang, I. Suarez, M. Glozak, M. Maurin, D. Nguyen, K.L. Wright, P.W. Atadja, K. Bhalla, J. Pinilla-Ibarz, E. Seto, and E.M. Sotomayor The histone deacetylase HDAC11 regulates the expression of interleukin 10 and immune tolerance Nat Immunol 10 2009 92 100
121. F. Miao, I.G. Gonzalo, L. Lanting, and R. Natarajan In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions J Biol Chem 279 2004 18091 18097
122. Y. Li, M.A. Reddy, F. Miao, N. Shanmugam, J.K. Yee, D. Hawkins, B. Ren, and R. Natarajan 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 2008 26771 26781
123. F. Miao, X. Wu, L. Zhang, Y.C. Yuan, A.D. Riggs, and R. Natarajan Genome-wide analysis of histone lysine methylation variations caused by diabetic conditions in human monocytes J Biol Chem 282 2007 13854 13863
124. F. Miao, D.D. Smith, L. Zhang, A. Min, W. Feng, and R. Natarajan Lymphocytes from patients with type 1 diabetes display a distinct profile of chromatin histone H3 lysine 9 dimethylation: an epigenetic study in diabetes Diabetes 57 2008 3189 3198
125. F. Miao, Z. Chen, L. Zhang, Z. Liu, X. Wu, Y.C. Yuan, and R. Natarajan Profiles of epigenetic histone post-translational modifications at type 1 diabetes susceptible genes J Biol Chem 287 2012:. [125 143]. 16335 16345
126. A.B. Gaikwad, J. Gupta, and K. Tikoo Epigenetic changes and alteration of Fbn1 and Col3A1 gene expression under hyperglycaemic and hyperinsulinaemic conditions Biochem J 432 2010 333 341
127. S.G. Sayyed, A.B. Gaikwad, J. Lichtnekert, O. Kulkarni, D. Eulberg, S. Klussmann, K. Tikoo, and H.J. Anders Progressive glomerulosclerosis in type 2 diabetes is associated with renal histone H3K9 and H3K23 acetylation, H3K4 dimethylation and phosphorylation at serine 10 Nephrol Dial Transplant 25 2010 1811 1817
128. H. Noh, E.Y. Oh, J.Y. Seo, M.R. Yu, Y.O. Kim, H. Ha, and H.B. Lee Histone deacetylase-2 is a key regulator of diabetes- and transforming growth factor-beta1-induced renal injury Am J Physiol Renal Physiol 297 2009 F729 F739
129. G. Sun, M.A. Reddy, H. Yuan, L. Lanting, M. Kato, and R. Natarajan Epigenetic histone methylation modulates fibrotic gene expression J Am Soc Nephrol 21 2010 2069 2080
130. W. Zhang, X. Xia, M.R. Reisenauer, C.S. Hemenway, and B.C. Kone Dot1a-AF9 complex mediates histone H3 Lys-79 hypermethylation and repression of ENaCalpha in an aldosterone-sensitive manner J Biol Chem 281 2006 18059 18068
131. W. Zhang, X. Xia, M.R. Reisenauer, T. Rieg, F. Lang, D. Kuhl, V. Vallon, and B.C. Kone Aldosterone-induced Sgk1 relieves Dot1a-Af9-mediated transcriptional repression of epithelial Na channel alpha J Clin Invest 117 2007 773 783
132. M. Naito, R.A. Zager, and K. Bomsztyk BRG1 increases transcription of proinflammatory genes in renal ischemia J Am Soc Nephrol 20 2009 1787 1796
133. C.K. Abrass, K. Hansen, V. Popov, and O. Denisenko Alterations in chromatin are associated with increases in collagen III expression in aging nephropathy Am J Physiol Renal Physiol 300 2011 F531 F539
134. G.M. Lefevre, S.R. Patel, D. Kim, L. Tessarollo, and G.R. Dressler Altering a histone H3K4 methylation pathway in glomerular podocytes promotes a chronic disease phenotype PLoS Genet 6 2010 e1001142
135. G.R. Dressler Epigenetics, development, and the kidney J Am Soc Nephrol 19 2008 2060 2067
136. L.M. Villeneuve, M. Kato, M.A. Reddy, M. Wang, L. Lanting, and R. Natarajan 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 2010 2904 2915
137. D. Brasacchio, J. Okabe, C. Tikellis, A. Balcerczyk, P. George, E.K. Baker, A.C. Calkin, M. Brownlee, M.E. Cooper, and A. El-Osta 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 2009 1229 1236
138. A.W. Cowley Jr, J.H. Nadeau, A. Baccarelli, K. Berecek, M. Fornage, G.H. Gibbons, D.G. Harrison, M. Liang, P.W. Nathanielsz, D.T. O'Connor, J. Ordovas, W. Peng, M.B. Soares, M. Szyf, H.E. Tolunay, K.C. Wood, K. Zhao, and Z.S. Galis Report of the national heart, lung, and blood institute working group on epigenetics and hypertension Hypertension 59 2012 899 905
139. D.E. Schones, and K. Zhao Genome-wide approaches to studying chromatin modifications Nat Rev Genet 9 2008 179 191
140. A.K. Maunakea, I. Chepelev, and K. Zhao Epigenome mapping in normal and disease States Circ Res 107 2010 327 339
141. M.L. Metzker Sequencing technologies - the next generation Nat Rev Genet 11 2010 31 46
142. F. Mohn, M. Weber, D. Schübeler, and T.C. Roloff Methylated DNA immunoprecipitation (MeDIP) Methods Mol Biol 507 2009 55 64
143. T.A. Rauch, and G.P. Pfeifer DNA methylation profiling using the methylated-CpG island recovery assay (MIRA) Methods 52 2010 213 217
144. P.W. Laird Principles and challenges of genomewide DNA methylation analysis Nat Rev Genet 11 2010 191 203
145. R.D. Hawkins, G.C. Hon, and B. Ren Next-generation genomics: an integrative approach Nat Rev Genet 11 2010 476 486
146. D. Pons, F.R. de Vries, P.J. van den Elsen, B.T. Heijmans, P.H. Quax, and J.W. Jukema Epigenetic histone acetylation modifiers in vascular remodelling: new targets for therapy in cardiovascular disease Eur Heart J 30 2009 266 277
147. R. Natarajan Drugs targeting epigenetic histone acetylation in vascular smooth muscle cells for restenosis and atherosclerosis Arterioscler Thromb Vasc Biol 31 2011 725 727
148. J.M. Yun, I. Jialal, and S. Devaraj Epigenetic regulation of high glucose-induced proinflammatory cytokine production in monocytes by curcumin J Nutr Biochem 22 2011:. [148]. 450 458
149. J. Chiu, Z.A. Khan, H. Farhangkhoee, and S. Chakrabarti Curcumin prevents diabetes-associated abnormalities in the kidneys by inhibiting p300 and nuclear factor-kappaB Nutrition 25 2009 964 972