Evaluating the role of epigenetic histone modifications in the metabolic memory of type 1 diabetes

Diabetes

Volumn 63, Issue 5, 2014, Pages 1748-1762

  Miao, Feng ^a   Chen, Zhuo ^a   Genuth, Saul ^b   Paterson, Andrew ^c   Zhang, Lingxiao ^a   Wu, Xiwei ^a   Li, Sierra Min ^a   Cleary, Patricia ^d   Riggs, Arthur ^a   Harlan, David M ^e   Lorenzi, Gayle ^f   Kolterman, Orville ^f   Sun, Wanjie ^d   Lachin, John M ^d   Natarajan, Rama ^a  

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

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d GEORGE WASHINGTON UNIVERSITY   (United States)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; DIABETIC RETINOPATHY; DISEASE PROGRESSION; EPIGENESIS, GENETIC; FEMALE; HISTONES; HUMANS; HYPOGLYCEMIC AGENTS; MALE; MIDDLE AGED;

EID: 84897489404     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-1251     Document Type: Article

References (51)

1. Pezzolesi MG, Katavetin P, Kure M, et al. Confirmation of genetic associations at ELMO1 in the GoKinD collection supports its role as a susceptibility gene in diabetic nephropathy. Diabetes 2009;58:2698-2702
2. Pezzolesi MG, Poznik GD, Mychaleckyj JC, et al.; DCCT/EDIC Research Group. Genome-wide association scan for diabetic nephropathy susceptibility genes in type 1 diabetes. Diabetes 2009;58:1403-1410
3. Sandholm N, Salem RM, McKnight AJ, et al.; DCCT/EDIC Research Group. New susceptibility loci associated with kidney disease in type 1 diabetes. PLoS Genet 2012;8:e1002921
4. Leung A, Schones DE, Natarajan R. Using epigenetic mechanisms to understand the impact of common disease causing alleles. Curr Opin Immunol 2012;24:558-563
5. Villeneuve LM, Reddy MA, Natarajan R. Epigenetics: deciphering its role in diabetes and its chronic complications. Clin Exp Pharmacol Physiol 2011;38: 451-459
6. Reddy MA, Natarajan R. Epigenetic mechanisms in diabetic vascular complications. Cardiovasc Res 2011;90:421-429
7. Cooper ME, El-Osta A. Epigenetics: mechanisms and implications for diabetic complications. Circ Res 2010;107:1403-1413
8. Diabetes Control and Complications Trial Research Group. 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 1993;329: 977-986
9. Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. Retinopathy and nephropathy in patients with type 1 diabetes four years after a trial of intensive therapy. N Engl J Med 2000;342:381-389
10. Genuth S. Insights from the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications study on the use of intensive glycemic treatment to reduce the risk of complications of type 1 diabetes. Endocr Pract 2006;12(Suppl. 1):34-41 (Pubitemid 44963609)
11. Cleary PA, Orchard TJ, Genuth S, et al.; DCCT/EDIC Research Group. 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 2006;55:3556-3565 (Pubitemid 44923617)
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 DM, Cleary PA, Backlund JY, et al.; Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC) Study Research Group. Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 2005;353: 2643-2653
15. Holman RR, Paul SK, Bethel MA, Matthews DR, Neil HA. 10-year follow-up of intensive glucose control in type 2 diabetes. N Engl J Med 2008;359:1577-1589
16. Chalmers J, Cooper ME. UKPDS and the legacy effect. N Engl J Med 2008; 359:1618-1620
17. Miao F, Smith DD, Zhang L, Min A, Feng W, Natarajan R. 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
18. Miao F, Wu X, Zhang L, Yuan YC, Riggs AD, Natarajan R. Genome-wide analysis of histone lysine methylation variations caused by diabetic conditions in human monocytes. J Biol Chem 2007;282:13854-13863 (Pubitemid 47100501)
19. Pirola L, Balcerczyk A, Tothill RW, et al. Genome-wide analysis distinguishes hyperglycemia regulated epigenetic signatures of primary vascular cells. Genome Res 2011;21:1601-1615
20. 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
21. 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
22. Sun G, Reddy MA, Yuan H, Lanting L, Kato M, Natarajan R. Epigenetic histone methylation modulates fibrotic gene expression. J Am Soc Nephrol 2010; 21:2069-2080
23. Zhong Q, Kowluru RA. Role of histone acetylation in the development of diabetic retinopathy and the metabolic memory phenomenon. J Cell Biochem 2010;110:1306-1313
24. Villeneuve LM, Reddy MA, Lanting LL, Wang M, Meng L, Natarajan R. Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes. Proc Natl Acad Sci USA 2008;105:9047-9052
25. Chan PS, Kanwar M, Kowluru RA. Resistance of retinal inflammatory mediators to suppress after reinstitution of good glycemic control: novel mechanism for metabolic memory. J Diabetes Complications 2010;24:55-63
26. Bird A. Perceptions of epigenetics. Nature 2007;447:396-398 (Pubitemid 46816744)
27. Bonasio R, Tu S, Reinberg D. Molecular signals of epigenetic states. Science 2010;330:612-616
28. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet 2007;8:253-262 (Pubitemid 46439287)
29. Jenuwein T, Allis CD. Translating the histone code. Science 2001;293: 1074-1080 (Pubitemid 32758077)
30. Kouzarides T. Chromatin modifications and their function. Cell 2007;128: 693-705 (Pubitemid 46273577)
31. Razin A, Riggs AD. DNA methylation and gene function. Science 1980;210:604-610
32. Martin C, Zhang Y. The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 2005;6:838-849 (Pubitemid 41568733)
33. Li Y, Reddy MA, 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
34. Miao F, Gonzalo IG, Lanting L, Natarajan R. In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions. J Biol Chem 2004;279:18091-18097 (Pubitemid 38560579)
35. Brasacchio D, Okabe J, Tikellis C, et al. Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic marks that coexist on the lysine tail. Diabetes 2009;58:1229-1236
36. Yuan H, Reddy MA, Sun G, et al. Involvement of p300/CBP and epigenetic histone acetylation in TGF-b1-mediated gene transcription in mesangial cells.Am J Physiol Renal Physiol 2013;304:F601-F613
37. Kadiyala CS, Zheng L, Du Y, et al. Acetylation of retinal histones in diabetes increases inflammatory proteins: effects of minocycline and manipulation of histone acetyltransferase (HAT) and histone deacetylase (HDAC). J Biol Chem 2012;287:25869-25880
38. Pirola L, Balcerczyk A, Okabe J, El-Osta A. Epigenetic phenomena linked to diabetic complications. Nat Rev Endocrinol 2010;6:665-675
39. Zhong Q, Kowluru RA. Epigenetic changes in mitochondrial superoxide dismutase in the retina and the development of diabetic retinopathy. Diabetes 2011;60:1304-1313
40. Caramori ML, Kim Y, Moore JH, et al. Gene expression differences in skin fibroblasts in identical twins discordant for type 1 diabetes. Diabetes 2012;61: 739-744
41. Ko YA, Mohtat D, Suzuki M, et al. Cytosine methylation changes in enhancer regions of core pro-fibrotic genes characterize kidney fibrosis development. Genome Biol 2013;14:R108
42. Bieda M, Xu X, Singer MA, Green R, Farnham PJ. Unbiased location analysis of E2F1-binding sites suggests a widespread role for E2F1 in the human genome. Genome Res 2006;16:595-605
43. Thomas-Chollier M, Hufton A, Heinig M, et al. Transcription factor binding predictions using TRAP for the analysis of ChIP-seq data and regulatory SNPs. Nat Protoc 2011;6:1860-1869
44. Yun JM, Jialal I, Devaraj S. Epigenetic regulation of high glucose-induced proinflammatory cytokine production in monocytes by curcumin. J Nutr Biochem 2011;22:450-458
45. Miao F, Chen Z, Zhang L, et al. RNA-sequencing analysis of high glucose-treated monocytes reveals novel transcriptome signatures and associated epigenetic profiles. Physiol Genomics 2013;45:287-299
46. Gohda T, Niewczas MA, Ficociello LH, et al. Circulating TNF receptors 1 and 2 predict stage 3 CKD in type 1 diabetes. J Am Soc Nephrol 2012;23:516-524
47. Lopes-Virella MF, Baker NL, Hunt KJ, Cleary PA, Klein R, Virella G; DCCT/EDIC Research Group. Baseline markers of inflammation are associated with progression to macroalbuminuria in type 1 diabetic subjects. Diabetes Care 2013; 36:2317-2323
48. DCCT Research Group. The absence of a glycemic threshold for the development of long-term complications: the perspective of the Diabetes Control and Complications Trial. Diabetes 1996;45:1289-1298
49. 1c) to the risk of development and progression of retinopathy in the Diabetes Control and Complications Trial. Diabetes 1995;44:968-983
50. Petruk S, Sedkov Y, Johnston DM, et al. TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell 2012; 150:922-933
51. DCCT Research Group. The effect of intensive diabetes therapy on the development and progression of neuropathy. Ann Intern Med 1995;122:561-568