Epigenetic Modifications in the Pathogenesis of Diabetic Nephropathy

Seminars in Nephrology

Volumn 33, Issue 4, 2013, Pages 341-353

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

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

Author keywords

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

Indexed keywords

DNA; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE METHYLTRANSFERASE; LYSINE;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; DIABETIC NEPHROPATHY; DISEASE ASSOCIATION; DNA METHYLATION; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENERAL ASPECTS OF DISEASE; GENETIC ASSOCIATION; GENOMICS; GLYCEMIC CONTROL; HIGH THROUGHPUT SEQUENCING; HISTONE ACETYLATION; HISTONE METHYLATION; HUMAN; HYPERGLYCEMIA; IN VITRO STUDY; INTRACELLULAR SIGNALING; METABOLIC MEMORY; MICROARRAY ANALYSIS; MOLECULAR PATHOLOGY; MONOCYTE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN PROCESSING;

CHROMATIN; DIABETIC NEPHROPATHY; EPIGENOMICS; HISTONE MODIFICATIONS; METABOLIC MEMORY;

ANIMALS; DIABETIC NEPHROPATHIES; DISEASE MODELS, ANIMAL; DNA METHYLATION; EPIGENESIS, GENETIC; EPIGENOMICS; GENE EXPRESSION REGULATION; HIGH-THROUGHPUT SCREENING ASSAYS; HISTONES; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84883524268     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2013.05.006     Document Type: Article

References (99)

1. Kanwar Y.S., Sun L., Xie P., et al. A glimpse of various pathogenetic mechanisms of diabetic nephropathy. Annu Rev Pathol 2011, 6:395-423.
2. Woroniecka K.I., Park A.S., Mohtat D., et al. Transcriptome analysis of human diabetic kidney disease. Diabetes 2011, 60:2354-2369.
3. Sanchez A.P., Sharma K. Transcription factors in the pathogenesis of diabetic nephropathy. Expert Rev Mol Med 2009, 11:e13.
4. Ling C., Groop L. Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes 2009, 58:2718-2725.
5. Reddy M.A., Natarajan R. Epigenetics in diabetic kidney disease. J Am Soc Nephrol 2011, 22:2182-2185.
6. Dunham I., Kundaje A., Aldred S.F., et al. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74.
7. Human Epigenome Task Force. Moving AHEAD with an international human epigenome project. Nature 2008, 454:711-715.
8. Wang Y., Harris D.C. Macrophages in renal disease. J Am Soc Nephrol 2011, 22:21-27.
9. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414:813-820.
10. Kato M., Natarajan R. MicroRNA circuits in transforming growth factor-beta actions and diabetic nephropathy. Semin Nephrol 2012, 32:253-260.
11. Villeneuve L.M., Natarajan R. The role of epigenetics in the pathology of diabetic complications. Am J Physiol Renal Physiol 2010, 299:F14-F25.
12. 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 2002, 287:2563-2569.
13. 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 2003, 290:2159-2167.
14. Nathan D.M., Cleary P.A., Backlund J.Y., et al. Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 2005, 353:2643-2653.
15. Colagiuri S., Cull C.A., Holman R.R. Are lower fasting plasma glucose levels at diagnosis of type 2 diabetes associated with improved outcomes?: U.K. prospective diabetes study 61. Diabetes Care 2002, 25:1410-1417.
16. Roy S., Sala R., Cagliero E., et al. Overexpression of fibronectin induced by diabetes or high glucose: phenomenon with a memory. Proc Natl Acad Sci U S A 1990, 87:404-408.
17. Li S.L., Reddy M.A., Cai Q., et al. Enhanced proatherogenic responses in macrophages and vascular smooth muscle cells derived from diabetic db/db mice. Diabetes 2006, 55:2611-2619.
18. El-Osta A., Brasacchio D., Yao D., et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 2008, 205:2409-2417.
19. Zhong Q., Kowluru R.A. Epigenetic changes in mitochondrial superoxide dismutase in the retina and the development of diabetic retinopathy. Diabetes 2011, 60:1304-1313.
20. Engerman R.L., Kern T.S. Progression of incipient diabetic retinopathy during good glycemic control. Diabetes 1987, 36:808-812.
21. Kowluru R.A., Abbas S.N., Odenbach S. 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 2004, 18:282-288.
22. Kowluru R.A. Effect of reinstitution of good glycemic control on retinal oxidative stress and nitrative stress in diabetic rats. Diabetes 2003, 52:818-823.
23. Waddington C.H. The epigenotype. 1942. Int J Epidemiol 2012, 41:10-13.
24. Goldberg A.D., Allis C.D., Bernstein E. Epigenetics: a landscape takes shape. Cell 2007, 128:635-638.
25. Bonasio R., Tu S., Reinberg D. Molecular signals of epigenetic states. Science 2010, 330:612-616.
26. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
27. Jones P.A. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012, 13:484-492.
28. Zhou V.W., Goren A., Bernstein B.E. Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 2011, 12:7-18.
29. Portela A., Esteller M. Epigenetic modifications and human disease. Nat Biotechnol. 2010, 28:1057-1068.
30. Baylin S.B., Jones P.A. A decade of exploring the cancer epigenome - biological and translational implications. Nat Rev Cancer 2011, 11:726-734.
31. Jirtle R.L., Skinner M.K. Environmental epigenomics and disease susceptibility. Nat Rev Genet 2007, 8:253-262.
32. Wang J., Wu Z., Li D., et al. Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal 2012, 17:282-301.
33. Chen Z.X., Riggs A.D. DNA methylation and demethylation in mammals. J Biol Chem 2011, 286:18347-18353.
34. Simmons R. Epigenetics and maternal nutrition: nature v. nurture. Proc Nutr Soc. 2011, 70:73-81.
35. Ling C., Del Guerra S., Lupi R., et al. Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion. Diabetologia 2008, 51:615-622.
36. Barres R., Osler M.E., Yan J., et al. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 2009, 10:189-198.
37. Nikoshkov A., Sunkari V., Savu O., et al. Epigenetic DNA methylation in the promoters of the Igf1 receptor and insulin receptor genes in db/db mice. Epigenetics 2011, 6:405-409.
38. Yang B.T., Dayeh T.A., Kirkpatrick C.L., et al. Insulin promoter DNA methylation correlates negatively with insulin gene expression and positively with HbA(1c) levels in human pancreatic islets. Diabetologia 2011, 54:360-367.
39. Yang B.T., Dayeh T.A., Volkov P.A., et al. Increased DNA methylation and decreased expression of PDX-1 in pancreatic islets from patients with type 2 diabetes. Mol Endocrinol 2012, 26:1203-1212.
40. Toperoff G., Aran D., Kark J.D., et al. Genome-wide survey reveals predisposing diabetes type 2-related DNA methylation variations in human peripheral blood. Hum Mol Genet 2012, 21:371-383.
41. Bell C.G., Finer S., Lindgren C.M., et al. Integrated genetic and epigenetic analysis identifies haplotype-specific methylation in the FTO type 2 diabetes and obesity susceptibility locus. PLoS One 2010, 5:e14040.
42. Leung A., Schones D.E., Natarajan R. Using epigenetic mechanisms to understand the impact of common disease causing alleles. Curr Opin Immunol 2012, 24:558-563.
43. Bell C.G., Teschendorff A.E., Rakyan V.K., et al. Genome-wide DNA methylation analysis for diabetic nephropathy in type 1 diabetes mellitus. BMC Med Genomics 2010, 3:33-42.
44. Sapienza C., Lee J., Powell J., et al. DNA methylation profiling identifies epigenetic differences between diabetes patients with ESRD and diabetes patients without nephropathy. Epigenetics 2011, 6:20-28.
45. Bechtel W., McGoohan S., Zeisberg E.M., et al. Methylation determines fibroblast activation and fibrogenesis in the kidney. Nat Med 2010, 16:544-550.
46. Pirola L., Balcerczyk A., Tothill R.W., et al. Genome-wide analysis distinguishes hyperglycemia regulated epigenetic signatures of primary vascular cells. Genome Res 2011, 21:1601-1615.
47. Jin F., Li Y., Ren B., et al. Enhancers: multi-dimensional signal integrators. Transcription 2011, 2:226-230.
48. Chen S., Ma J., Wu F., et al. The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation. Genes Dev 2012, 26:1364-1375.
49. Guttman M., Amit I., Garber M., et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009, 458:223-227.
50. Baur J.A., Ungvari Z., Minor R.K., et al. Are sirtuins viable targets for improving healthspan and lifespan?. Nat Rev Drug Discov 2012, 11:443-461.
51. Klose R.J., Zhang Y. Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 2007, 8:307-318.
52. Smith E., Shilatifard A. The chromatin signaling pathway: diverse mechanisms of recruitment of histone-modifying enzymes and varied biological outcomes. Mol Cell 2010, 40:689-701.
53. Guttman M., Rinn J.L. Modular regulatory principles of large non-coding RNAs. Nature 2012, 482:339-346.
54. Allis C.D., Berger S.L., Cote J., et al. New nomenclature for chromatin-modifying enzymes. Cell 2007, 131:633-636.
55. Sassone-Corsi P. Physiology. When metabolism and epigenetics converge. Science 2013, 339:148-150.
56. Groth A., Corpet A., Cook A.J., et al. Regulation of replication fork progression through histone supply and demand. Science 2007, 318:1928-1931.
57. Abmayr S.M., Workman J.L. Holding on through DNA replication: histone modification or modifier?. Cell 2012, 150:875-877.
58. Cedar H., Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 2009, 10:295-304.
59. Babu D.A., Deering T.G., Mirmira R.G. A feat of metabolic proportions: Pdx1 orchestrates islet development and function in the maintenance of glucose homeostasis. Mol Genet Metab 2007, 92:43-55.
60. Deering T.G., Ogihara T., Trace A.P., et al. Methyltransferase Set7/9 maintains transcription and euchromatin structure at islet-enriched genes. Diabetes 2009, 58:185-193.
61. Stitzel M.L., Sethupathy P., Pearson D.S., et al. Global epigenomic analysis of primary human pancreatic islets provides insights into type 2 diabetes susceptibility loci. Cell Metab 2010, 12:443-455.
62. Gaulton K.J., Nammo T., Pasquali L., et al. A map of open chromatin in human pancreatic islets. Nat Genet 2010, 42:255-259.
63. Musri M.M., Gomis R., Parrizas M. A chromatin perspective of adipogenesis. Organogenesis 2010, 6:15-23.
64. Lefterova M.I., Steger D.J., Zhuo D., et al. Cell-specific determinants of peroxisome proliferator-activated receptor gamma function in adipocytes and macrophages. Mol Cell Biol 2010, 30:2078-2089.
65. Fujiki K., Kano F., Shiota K., et al. Expression of the peroxisome proliferator activated receptor gamma gene is repressed by DNA methylation in visceral adipose tissue of mouse models of diabetes. BMC Biol 2009, 7:38.
66. Tateishi K., Okada Y., Kallin E.M., et al. Role of Jhdm2a in regulating metabolic gene expression and obesity resistance. Nature 2009, 458:757-761.
67. Dressler G.R. Epigenetics, development, and the kidney. J Am Soc Nephrol 2008, 19:2060-2067.
68. Ross S., Cheung E., Petrakis T.G., et al. Smads orchestrate specific histone modifications and chromatin remodeling to activate transcription. EMBO J 2006, 25:4490-4502.
69. Yuan H., Reddy M.A., Sun G., et al. Involvement of p300/CBP and epigenetic histone acetylation in TGF-beta1 mediated gene transcription in mesangial cells. Am J Physiol Renal Physiol 2013, 304:F601-F613.
70. Sun G., Reddy M.A., Yuan H., et al. Epigenetic histone methylation modulates fibrotic gene expression. J Am Soc Nephrol 2010, 21:2069-2080.
71. Lee H.B., Noh H., Seo J.Y., et al. Histone deacetylase inhibitors: a novel class of therapeutic agents in diabetic nephropathy. Kidney Int Suppl 2007, 106:S61-S66.
72. Reddy MA, Putta S, Lanting LL, Yuan H, Wang M, Alpers CE, et al. Effect of losartan on epigenetic changes in the renal glomeruli of diabetic db/db mice. [abstract] J Am Soc Nephrol. 2012;23:TH-PO467.
73. Ruggenenti P., Cravedi P., Remuzzi G. The RAAS in the pathogenesis and treatment of diabetic nephropathy. Nat Rev Nephrol 2010, 6:319-330.
74. Reddy M.A., Natarajan R. Epigenetic mechanisms in diabetic vascular complications. Cardiovasc Res 2011, 90:421-429.
75. Giacco F., Brownlee M. Oxidative stress and diabetic complications. Circ Res. 2010, 107:1058-1070.
76. Guha M., Bai W., Nadler J.L., et al. Molecular mechanisms of tumor necrosis factor alpha gene expression in monocytic cells via hyperglycemia-induced oxidant stress-dependent and -independent pathways. J Biol Chem 2000, 275:17728-17739.
77. Shanmugam N., Reddy M.A., Guha M., et al. High glucose-induced expression of proinflammatory cytokine and chemokine genes in monocytic cells. Diabetes 2003, 52:1256-1264.
78. Miao F., Gonzalo I.G., Lanting L., et al. In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions. J Biol Chem 2004, 279:18091-18097.
79. Miao F., Wu X., Zhang L., et al. Genome-wide analysis of histone lysine methylation variations caused by diabetic conditions in human monocytes. J Biol Chem 2007, 282:13854-13863.
80. Miao F., Smith D.D., Zhang L., et al. Lymphocytes from patients with type 1 diabetes display a distinct profile of chromatin histone H3 lysine 9 dimethylation: an epigenetic study in diabetes. Diabetes 2008, 57:3189-3198.
81. Miao F., Chen Z., Zhang L., et al. Profiles of epigenetic histone post-translational modifications at type 1 diabetes susceptible genes. J Biol Chem 2012, 287:16335-16345.
82. Li Y., Reddy M.A., Miao F., et al. 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 2008, 283:26771-26781.
83. Yun J.M., Jialal I., Devaraj S. Epigenetic regulation of high glucose-induced proinflammatory cytokine production in monocytes by curcumin. J Nutr Biochem 2011, 22:450-458.
84. Okabe J., Orlowski C., Balcerczyk A., et al. Distinguishing hyperglycemic changes by set7 in vascular endothelial cells. Circ Res 2012, 110:1067-1076.
85. Villeneuve L.M., Reddy M.A., Lanting L.L., et al. 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 2008, 105:9047-9052.
86. Villeneuve L.M., Kato M., Reddy M.A., et al. 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 2010, 59:2904-2915.
87. Park P.J. ChIP-seq: advantages and challenges of a maturing technology. Nat Rev Genet 2009, 10:669-680.
88. Mortazavi A., Williams B.A., McCue K., et al. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5:621-628.
89. Laird P.W. Principles and challenges of genomewide DNA methylation analysis. Nat Rev Genet 2010, 11:191-203.
90. Huebert D.J., Kamal M., O'Donovan A., et al. Genome-wide analysis of histone modifications by ChIP-on-chip. Methods 2006, 40:365-369.
91. Simon J.M., Giresi P.G., Davis I.J., et al. Using formaldehyde-assisted isolation of regulatory elements (FAIRE) to isolate active regulatory DNA. Nat Protoc 2012, 7:256-267.
92. Hesselberth J.R., Chen X., Zhang Z., et al. Global mapping of protein-DNA interactions in vivo by digital genomic footprinting. Nat Methods 2009, 6:283-289.
93. Pepke S., Wold B., Mortazavi A. Computation for ChIP-seq and RNA-seq studies. Nat Methods 2009, 6:S22-S32.
94. Hawkins R.D., Hon G.C., Ren B. Next-generation genomics: an integrative approach. Nat Rev Genet 2010, 11:476-486.
95. Stamatoyannopoulos J.A., Snyder M., Hardison R., et al. An encyclopedia of mouse DNA elements (Mouse ENCODE). Genome Biol 2012, 13:418.
96. Rosenbloom K.R., Dreszer T.R., Long J.C., et al. ENCODE whole-genome data in the UCSC Genome Browser: update 2012. Nucleic Acids Res 2012, 40:D912-D917.
97. Mutskov V., Felsenfeld G. The human insulin gene is part of a large open chromatin domain specific for human islets. Proc Natl Acad Sci U S A 2009, 106:17419-17424.
98. Bhandare R., Schug J., Le Lay J., et al. Genome-wide analysis of histone modifications in human pancreatic islets. Genome Res 2010, 20:428-433.
99. Putta S., Lanting L., Sun G., et al. Inhibiting microRNA-192 ameliorates renal fibrosis in diabetic nephropathy. J Am Soc Nephrol 2012, 23:458-469.