- Department of Ophthalmology, The Eye-ENT Hospital of Fudan University, Shanghai 200031, China;
Epigenetic modifications such as DNA methylation, histone post-translational modifications, non-coding RNA are reversible, heritable alterations which are induced by environmental stimuli. Major risk factors of diabetes and diabetic complications including hyperglycemia, oxidative stress and advanced glycation end products, can lead to abnormal epigenetic modifications in retinal vascular endothelial cells and retinal pigment epithelium cells. Epigenetic mechanisms are involved in the pathogenesis of macular edema and neovascularization of diabetic retinopathy (DR), as well as diabetic metabolic memory. The heritable nature of epigenetic marks also playsakey role in familial diabetes mellitus. Further elucidation of epigenetic mechanisms in DR can open the way for the discovery of novel therapeutic targets to prevent DR progression.
Citation: ChenWenwen, ChangQing. Epigenetic modifications in diabetic retinopathy. Chinese Journal of Ocular Fundus Diseases, 2016, 32(2): 213-217. doi: 10.3760/cma.j.issn.1005-1015.2016.02.026 Copy
1. | Diabetes Control and Complications Trial (DCCT)/Epidemiology of Diabetes Interventions and Complications (EDIC) Study Research Group.Intensive diabetes treatment and cardiovascular outcomes in type 1 diabetes: the DCCT/EDIC Study 30-year follow-up[J/OL].Diabetes Care, 2016:E151990[2016-02-09].http://care.diabetesjournals.org/content/early/2016/01/29/dc15-1990.[published online ahead of print]. |
2. | Aiello LP,DCCT/EDIC Research Group. Diabetic retinopathy and other ocular findings in the diabetes control and complications trial/epidemiology of diabetes interventions and complications study[J]. Diabetes Care, 2014,37(1):17-23.DOI: 10.2337/dc13-2251. |
3. | Ranjit Unnikrishnan I, Anjana RM, Mohan V.Importance of controlling diabetes early--the concept of metabolic memory, legacy effect and the case for early insulinisation[J].JAssoc Physicians India, 2011,59 Suppl:S8-12. |
4. | 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[J]. JAMA, 2002,287(19):2563-2569. |
5. | Perrone L, Matrone C, Singh LP.Epigenetic modifications and potential new treatment targets in diabetic retinopathy[J/OL].J Ophthalmol,2014,2014:789120 [2014-07-24]. https://www. researchgate.net/publication/264166836_Erratum_to_Epigenetic_Modifications_and_Potential_New_Treatment_Targets_in_Diabetic_Retinopathy.DOI: 10.1155/2014/789120. |
6. | Reddy MA, Zhang E, Natarajan R. Epigenetic mechanisms in diabetic complications and metabolic memory[J]. Diabetologia, 2015,58(3):443-455. DOI: 10.1007/s00125-014-3462-y. |
7. | Egger G, Liang G, Aparicio A, et al. Epigenetics in human disease and prospects for epigenetic therapy[J]. Nature, 2004,429(6990):457-463. |
8. | Bird A. Perceptions of epigenetics[J]. Nature, 2007,447(7143):396-398. |
9. | Intine RV, Olsen AS, Sarras MJ.Azebrafish model of diabetes mellitus and metabolic memory[J/OL].JVis Exp, 2013(72):50232[2013-02-28].http://www.jove.com/video/50232/a-zebrafish-model-of-diabetes-mellitus-and-metaboliz-memory.DOI: 10.3791/50232. |
10. | Reddy MA, Natarajan R. Epigenetic mechanisms in diabetic vascular complications[J]. Cardiovasc Res, 2011,90(3):421-429.DOI:10.1093/cvr/cvr024. |
11. | Kowluru RA. Mitochondria damage in the pathogenesis of diabetic retinopathy and in the metabolic memory associated with its continued progression[J]. Curr Med Chem, 2013,20(26):3226-3233. |
12. | Kim DI, Park MJ, Lim SK,et al.High-glucose-induced CARM1 expression regulates apoptosis of human retinal pigment epithelial cells via histone 3 arginine 17 dimethylation: role in diabetic retinopathy[J].Arch Biochem Biophys,2014,560:36-43. DOI: 10.1016/j.abb.2014.07.021. |
13. | Kato M, Castro NE, Natarajan R. MicroRNAs: potential mediators and biomarkers of diabetic complications[J]. Free Radic Biol Med, 2013,64:85-94. DOI: 10.1016/j. freeradbiomed. 2013. 06. 009. |
14. | Zeng J, Chen B. Epigenetic mechanisms in the pathogenesis of diabetic retinopathy[J]. Ophthalmologica, 2014,232(1):1-9. DOI: 10.1159/000357824. |
15. | Maghbooli Z, Pasalar P, Keshtkar A,et al.Predictive factors of diabetic complications:apossible link between family history of diabetes and diabetic retinopathy[J].J Diabetes Metab Disord, 2014,13:55. DOI: 10.1186/2251-6581-13-55. |
16. | Tang ZH, Wang L, Zeng F,et al.Human genetics of diabetic retinopathy[J].J Endocrinol Invest,2014,37(12):1165-1174. DOI: 10.1007/s40618-014-0172-8. |
17. | ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome[J]. Nature, 2012,489(7414):57-74.DOI:10.1038/nature11247. |
18. | Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics[J]. Science, 2001,293(5532):1068-1070. |
19. | Franchini DM, Schmitz KM, Petersen-Mahrt SK. 5-methylcytosine DNA demethylation: more than losingamethyl group[J]. Annu Rev Genet, 2012,46:419-441.DOI: 10.1146/annurev-genet-110711-155451. |
20. | Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond[J]. Nat Rev Genet, 2012,13(7):484-492.DOI:10.1038/nrg3230. |
21. | Maghbooli Z, Hossein-nezhad A, Larijani B,et al.Global DNA methylation asapossible biomarker for diabetic retinopathy[J].Diabetes Metab Res Rev,2015, 31(2):183-189.DOI: 10.1002/dmrr.2584. |
22. | Agardh E, Lundstig A, Perfilyev A, et al. Genome-wide analysis of DNA methylation in subjects with type 1 diabetes identifies epigenetic modifications associated with proliferative diabetic retinopathy[J]. BMC Med, 2015,13:182. DOI: 10.1186/s12916-015-0421-5. |
23. | Tewari S, Zhong Q, Santos JM, et al. Mitochondria DNA replication and DNA methylation in the metabolic memory associated with continued progression of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2012,53(8):4881-4888.DOI: 10.1167/iovs.12-9732. |
24. | Suganuma T, Workman JL. Signals and combinatorial functions of histone modifications[J]. Annu Rev Biochem, 2011,80:473-499.DOI: 10.1146/annurev-biochem-061809-175347. |
25. | Mosammaparast N, Shi Y. Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases[J]. Annu Rev Biochem, 2010,79:155-179.DOI: 10.1146/annurev.biochem.78.070907.103946. |
26. | Greer EL, Shi Y. Histone methylation:adynamic mark in health, disease and inheritance[J]. Nat Rev Genet, 2012,13(5):343-357.DOI: 10.1038/nrg3173. |
27. | Zhou VW, Goren A, Bernstein BE. Charting histone modifications and the functional organization of mammalian genomes[J]. Nat Rev Genet, 2011,12(1):7-18.DOI: 10.1038/nrg2905. |
28. | Zhong Q, Kowluru RA. Epigenetic modification of Sod2 in the development of diabetic retinopathy and in the metabolic memory: role of histone methylation[J]. Invest Ophthalmol Vis Sci, 2013,54(1):244-250.DOI: 10.1167/iovs.12-10854. |
29. | Zhong Q, Kowluru RA. Epigenetic changes in mitochondrial superoxide dismutase in the retina and the development of diabetic retinopathy[J]. Diabetes, 2011,60(4):1304-1313.DOI: 10.2337/db10-0133. |
30. | Zhong Q, Kowluru RA. Regulation of matrix metalloproteinase-9 by epigenetic modifications and the development of diabetic retinopathy[J]. Diabetes, 2013,62(7):2559-2568.DOI: 10.2337/db12-1141. |
31. | Okabe J, Orlowski C, Balcerczyk A, et al. Distinguishing hyperglycemic changes by Set7 in vascular endothelial cells[J]. Circ Res, 2012,110(8):1067-1076.DOI:10.1161/CIRCRESAHA. 112.266171. |
32. | Mishra M, Zhong Q, Kowluru RA. Epigenetic modifications of Nrf2-mediated glutamate-cysteine ligase: implications for the development of diabetic retinopathy and the metabolic memory phenomenon associated with its continued progression[J]. Free Radic Biol Med, 2014,75:129-139.DOI: 10.1016/j.freeradbiomed.2014.07.001. |
33. | Mishra M, Zhong Q, Kowluru RA. Epigenetic modifications of keap1 regulate its interaction with the protective factor nrf2 in the development of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2014,55(11):7256-7265.DOI:10.1167/iovs.14-15193. |
34. | Pirola L. The DCCT/EDIC study: epigenetic clues after three decades[J]. Diabetes, 2014,63(5):1460-1462.DOI: 10.2337/db14-0238. |
35. | Pirola L, Balcerczyk A, Tothill RW, et al. Genome-wide analysis distinguishes hyperglycemia regulated epigenetic signatures of primary vascular cells[J]. Genome Res, 2011,21(10): 1601- 1615.DOI: 10.1101/gr.116095.110. |
36. | Perrone L, Devi TS, Hosoya KI, et al. Inhibition of TXNIP expression in vivo blocks early pathologies of diabetic retinopathy[J]. Cell Death Dis, 2010,1:65.DOI: 10.1038/cddis.2010.42. |
37. | Kowluru RA, Santos JM, Zhong Q. Sirt1,anegative regulator of matrix metalloproteinase-9 in diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2014,55(9):5653-5660.DOI: 10.1167 /iovs. 14-14383. |
38. | Zhang Y, Liu J, Tian XY, et al. Inhibition of bone morphogenic protein 4 restores endothelial function in db/db diabetic mice[J]. Arterioscler Thromb Vasc Biol, 2014,34(1):152-159.DOI: 10.1161/ATVBAHA.113.302696. |
39. | Giacco F, Brownlee M. Oxidative stress and diabetic complications[J]. Circ Res, 2010,107(9):1058-1070.DOI: 10.1161/CIRCRESAHA.110.223545. |
40. | Guttman M, Amit I, Garber M, et al. Chromatin signature reveals overathousand highly conserved large non-coding RNAs in mammals[J]. Nature, 2009,458(7235):223-227.DOI: 10.1038/nature07672. |
41. | Shukla GC, Singh J, Barik S. MicroRNAs: processing, maturation, target recognition and regulatory functions[J]. Mol Cell Pharmacol, 2011,3(3):83-92. |
42. | Silva VA, Polesskaya A, Sousa TA, et al. Expression and cellular localization of microRNA-29b and RAX, an activator of the RNA-dependent protein kinase (PKR), in the retina of streptozotocin-induced diabetic rats[J]. Mol Vis, 2011,17:2228-2240. |
43. | McArthur K, Feng B, Wu Y, et al. MicroRNA-200b regulates vascular endothelial growth factor-mediated alterations in diabetic retinopathy[J]. Diabetes, 2011,60(4):1314-1323.DOI: 10.2337/db10-1557. |
44. | Kovacs B, Lumayag S, Cowan C, et al. MicroRNAs in early diabetic retinopathy in streptozotocin-induced diabetic rats[J]. Invest Ophthalmol Vis Sci, 2011,52(7):4402-4409.DOI: 10.1167/iovs.10-6879. |
45. | Feng B, Chen S, McArthur K, et al. miR-146a-Mediated extracellular matrix protein production in chronic diabetes complications[J]. Diabetes, 2011,60(11):2975-2984.DOI: 10.2337/db11-0478. |
46. | Guttman M, Rinn JL. Modular regulatory principles of large non-coding RNAs[J]. Nature, 2012,482(7385):339-346.DOI: 10.1038/nature10887. |
47. | Kameswaran V, Kaestner KH. The Missing lnc(RNA) between the pancreatic beta-cell and diabetes[J]. Front Genet, 2014,5:200.DOI: 10.3389/fgene.2014.00200. |
48. | Leung A, Trac C, Jin W, et al. Novel long noncoding RNAs are regulated by angiotensin II in vascular smooth muscle cells[J]. Circ Res, 2013,113(3):266-278.DOI:10.1161/CIRCRESAHA. 112.300849. |
49. | Alvarez ML, DiStefano JK. Functional characterization of the plasmacytoma variant translocation 1 gene (PVT1) in diabetic nephropathy[J/OL]. PLoS One, 2011,6(4): 18671 [2011- 04- 22].http://www.doc88.com/p-0189783280919.html.DOI: 10.1371/journal.pone.0018671. |
50. | Kowluru RA, Kowluru A, Mishra M, et al. Oxidative stress and epigenetic modifications in the pathogenesis of diabetic retinopathy[J]. Prog Retin Eye Res, 2015,48:40-61.DOI:10.1016/j. preteyeres.2015.05.001. |
51. | Moore TC, Moore JE, Kaji Y, et al. The role of advanced glycation end products in retinal microvascular leukostasis[J]. Invest Ophthalmol Vis Sci, 2003,44(10):4457-4464. |
52. | Genuth S, Sun W, Cleary P, et al. Skin advanced glycation end products glucosepane and methylglyoxal hydroimidazolone are independently associated with long-term microvascular complication progression of type 1 diabetes[J]. Diabetes, 2015,64(1):266-278.DOI: 10.2337/db14-0215. |
53. | Rabbani N, Thornalley PJ. Hidden complexities in the measurement of fructosyl-lysine and advanced glycation end products for risk prediction of vascular complications of diabetes[J]. Diabetes, 2015,64(1):9-11.DOI:10.2337/db14-1516. |
54. | Zhang L, Chen B, Tang L. Metabolic memory: mechanisms and implications for diabetic retinopathy[J]. Diabetes Res Clin Pract, 2012,96(3):286-293.DOI: 10.1016/j.diabres.2011.12.006. |
55. | Zhong Q, Kowluru RA. Role of histone acetylation in the development of diabetic retinopathy and the metabolic memory phenomenon[J].JCell Biochem, 2010,110(6):1306-1313.DOI: 10.1002/jcb.22644. |
56. | White NH, Sun W, Cleary PA, et al. Effect of prior intensive therapy in type 1 diabetes on 10-year progression of retinopathy in the DCCT/EDIC: comparison of adults and adolescents[J]. Diabetes, 2010,59(5):1244-1253.DOI: 10.2337/db09-1216. |
57. | Manolopoulos VG, Ragia G, Tavridou A. Pharmacogenomics of oral antidiabetic medications: current data and pharmacoepigenomic perspective[J]. Pharmacogenomics, 2011,12(8):1161-1191. DOI:10.2217/pgs.11.65. |
58. | Sandholm N, Salem RM, McKnight AJ, et al. New susceptibility loci associated with kidney disease in type 1 diabetes[J/OL]. PLoS Genet, 2012,8(9):1002921[2012-09-20]. http://lup.lub.lu.se/luur/download?func=downloadFile&recordOId=3287820&fileOId=3460726. DOI: 10.1371/journal.pgen.1002921. |
59. | Xie M, Tian J, Luo Y, et al. Effects of 5-aza-2′-deoxycytidine and trichostatinAon high glucose- and interleukin-1beta-induced secretory mediators from human retinal endothelial cells and retinal pigment epithelial cells[J]. Mol Vis, 2014,20:1411-1421. |
60. | Zhang Z, Tong N, Gong Y, et al. Valproate protects the retina from endoplasmic reticulum stress-induced apoptosis after ischemia-reperfusion injury[J]. Neurosci Lett, 2011,504(2):88-92. DOI: 0.1016/j.neulet.2011.09.003. |
61. | 张笃贞, 张涤, 孙鹏, 等. 白藜芦醇对糖尿病大鼠视网膜中SIRT1基因表达的干预作用[J]. 眼科新进展, 2014,34(4):322-325.DOI:10.13389/j.cnki.rao.2014.0087.Zhang DZ,Zhang D,Sun P.Effects of resveratrol on SIRT1 gene expression in retina of diabetic rat[J].Rec Adv Ophthalmol,2014,34(2):322-325.DOI:10.13389/j.cnki.rao.2014.0087. |
62. | Nguyen QD, Schachar RA, Nduaka CI, et al. Phase 1 dose-escalation study ofasiRNA targeting the RTP801 gene in age-related macular degeneration patients[J]. Eye (Lond), 2012,26(8):1099-1105.DOI: 10.1038/eye.2012.106. |
63. | Sun AX, Crabtree GR, Yoo AS. MicroRNAs: regulators of neuronal fate[J]. Curr Opin Cell Biol, 2013,25(2):215-221. DOI: 10.1016/j.ceb.2012.12.007. |
64. | Rafehi H, El-Osta A, Karagiannis TC. Genetic and epigenetic events in diabetic wound healing[J]. Int Wound J, 2011,8(1):12-21.DOI: 10.1111/j.1742-481X.2010.00745.x. |
65. | Vecellio M, Spallotta F, Nanni S, et al. The histone acetylase activator pentadecylidenemalonate 1b rescues proliferation and differentiation in the human cardiac mesenchymal cells of type 2 diabetic patients[J]. Diabetes, 2014,63(6):2132-2147. DOI: 10.2337/db13-0731. |
66. | Kassan M, Choi SK, Galan M, et al. Enhanced p22phox expression impairs vascular function through p38 and ERK1/2 MAP kinase-dependent mechanisms in type 2 diabetic mice[J]. AmJPhysiol Heart Circ Physiol, 2014,306(7):972-980.DOI: 10.1152/ajpheart.00872.2013. |
67. | Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms[J]. Nat Rev Genet, 2009,10(5):295-304.DOI: 10.1038/nrg2540. |
68. | Ronn T, Ling C. Effect of exercise on DNA methylation and metabolism in human adipose tissue and skeletal muscle[J]. Epigenomics, 2013,5(6):603-605.DOI: 10.2217/epi.13.61. |
- 1. Diabetes Control and Complications Trial (DCCT)/Epidemiology of Diabetes Interventions and Complications (EDIC) Study Research Group.Intensive diabetes treatment and cardiovascular outcomes in type 1 diabetes: the DCCT/EDIC Study 30-year follow-up[J/OL].Diabetes Care, 2016:E151990[2016-02-09].http://care.diabetesjournals.org/content/early/2016/01/29/dc15-1990.[published online ahead of print].
- 2. Aiello LP,DCCT/EDIC Research Group. Diabetic retinopathy and other ocular findings in the diabetes control and complications trial/epidemiology of diabetes interventions and complications study[J]. Diabetes Care, 2014,37(1):17-23.DOI: 10.2337/dc13-2251.
- 3. Ranjit Unnikrishnan I, Anjana RM, Mohan V.Importance of controlling diabetes early--the concept of metabolic memory, legacy effect and the case for early insulinisation[J].JAssoc Physicians India, 2011,59 Suppl:S8-12.
- 4. 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[J]. JAMA, 2002,287(19):2563-2569.
- 5. Perrone L, Matrone C, Singh LP.Epigenetic modifications and potential new treatment targets in diabetic retinopathy[J/OL].J Ophthalmol,2014,2014:789120 [2014-07-24]. https://www. researchgate.net/publication/264166836_Erratum_to_Epigenetic_Modifications_and_Potential_New_Treatment_Targets_in_Diabetic_Retinopathy.DOI: 10.1155/2014/789120.
- 6. Reddy MA, Zhang E, Natarajan R. Epigenetic mechanisms in diabetic complications and metabolic memory[J]. Diabetologia, 2015,58(3):443-455. DOI: 10.1007/s00125-014-3462-y.
- 7. Egger G, Liang G, Aparicio A, et al. Epigenetics in human disease and prospects for epigenetic therapy[J]. Nature, 2004,429(6990):457-463.
- 8. Bird A. Perceptions of epigenetics[J]. Nature, 2007,447(7143):396-398.
- 9. Intine RV, Olsen AS, Sarras MJ.Azebrafish model of diabetes mellitus and metabolic memory[J/OL].JVis Exp, 2013(72):50232[2013-02-28].http://www.jove.com/video/50232/a-zebrafish-model-of-diabetes-mellitus-and-metaboliz-memory.DOI: 10.3791/50232.
- 10. Reddy MA, Natarajan R. Epigenetic mechanisms in diabetic vascular complications[J]. Cardiovasc Res, 2011,90(3):421-429.DOI:10.1093/cvr/cvr024.
- 11. Kowluru RA. Mitochondria damage in the pathogenesis of diabetic retinopathy and in the metabolic memory associated with its continued progression[J]. Curr Med Chem, 2013,20(26):3226-3233.
- 12. Kim DI, Park MJ, Lim SK,et al.High-glucose-induced CARM1 expression regulates apoptosis of human retinal pigment epithelial cells via histone 3 arginine 17 dimethylation: role in diabetic retinopathy[J].Arch Biochem Biophys,2014,560:36-43. DOI: 10.1016/j.abb.2014.07.021.
- 13. Kato M, Castro NE, Natarajan R. MicroRNAs: potential mediators and biomarkers of diabetic complications[J]. Free Radic Biol Med, 2013,64:85-94. DOI: 10.1016/j. freeradbiomed. 2013. 06. 009.
- 14. Zeng J, Chen B. Epigenetic mechanisms in the pathogenesis of diabetic retinopathy[J]. Ophthalmologica, 2014,232(1):1-9. DOI: 10.1159/000357824.
- 15. Maghbooli Z, Pasalar P, Keshtkar A,et al.Predictive factors of diabetic complications:apossible link between family history of diabetes and diabetic retinopathy[J].J Diabetes Metab Disord, 2014,13:55. DOI: 10.1186/2251-6581-13-55.
- 16. Tang ZH, Wang L, Zeng F,et al.Human genetics of diabetic retinopathy[J].J Endocrinol Invest,2014,37(12):1165-1174. DOI: 10.1007/s40618-014-0172-8.
- 17. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome[J]. Nature, 2012,489(7414):57-74.DOI:10.1038/nature11247.
- 18. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics[J]. Science, 2001,293(5532):1068-1070.
- 19. Franchini DM, Schmitz KM, Petersen-Mahrt SK. 5-methylcytosine DNA demethylation: more than losingamethyl group[J]. Annu Rev Genet, 2012,46:419-441.DOI: 10.1146/annurev-genet-110711-155451.
- 20. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond[J]. Nat Rev Genet, 2012,13(7):484-492.DOI:10.1038/nrg3230.
- 21. Maghbooli Z, Hossein-nezhad A, Larijani B,et al.Global DNA methylation asapossible biomarker for diabetic retinopathy[J].Diabetes Metab Res Rev,2015, 31(2):183-189.DOI: 10.1002/dmrr.2584.
- 22. Agardh E, Lundstig A, Perfilyev A, et al. Genome-wide analysis of DNA methylation in subjects with type 1 diabetes identifies epigenetic modifications associated with proliferative diabetic retinopathy[J]. BMC Med, 2015,13:182. DOI: 10.1186/s12916-015-0421-5.
- 23. Tewari S, Zhong Q, Santos JM, et al. Mitochondria DNA replication and DNA methylation in the metabolic memory associated with continued progression of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2012,53(8):4881-4888.DOI: 10.1167/iovs.12-9732.
- 24. Suganuma T, Workman JL. Signals and combinatorial functions of histone modifications[J]. Annu Rev Biochem, 2011,80:473-499.DOI: 10.1146/annurev-biochem-061809-175347.
- 25. Mosammaparast N, Shi Y. Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases[J]. Annu Rev Biochem, 2010,79:155-179.DOI: 10.1146/annurev.biochem.78.070907.103946.
- 26. Greer EL, Shi Y. Histone methylation:adynamic mark in health, disease and inheritance[J]. Nat Rev Genet, 2012,13(5):343-357.DOI: 10.1038/nrg3173.
- 27. Zhou VW, Goren A, Bernstein BE. Charting histone modifications and the functional organization of mammalian genomes[J]. Nat Rev Genet, 2011,12(1):7-18.DOI: 10.1038/nrg2905.
- 28. Zhong Q, Kowluru RA. Epigenetic modification of Sod2 in the development of diabetic retinopathy and in the metabolic memory: role of histone methylation[J]. Invest Ophthalmol Vis Sci, 2013,54(1):244-250.DOI: 10.1167/iovs.12-10854.
- 29. Zhong Q, Kowluru RA. Epigenetic changes in mitochondrial superoxide dismutase in the retina and the development of diabetic retinopathy[J]. Diabetes, 2011,60(4):1304-1313.DOI: 10.2337/db10-0133.
- 30. Zhong Q, Kowluru RA. Regulation of matrix metalloproteinase-9 by epigenetic modifications and the development of diabetic retinopathy[J]. Diabetes, 2013,62(7):2559-2568.DOI: 10.2337/db12-1141.
- 31. Okabe J, Orlowski C, Balcerczyk A, et al. Distinguishing hyperglycemic changes by Set7 in vascular endothelial cells[J]. Circ Res, 2012,110(8):1067-1076.DOI:10.1161/CIRCRESAHA. 112.266171.
- 32. Mishra M, Zhong Q, Kowluru RA. Epigenetic modifications of Nrf2-mediated glutamate-cysteine ligase: implications for the development of diabetic retinopathy and the metabolic memory phenomenon associated with its continued progression[J]. Free Radic Biol Med, 2014,75:129-139.DOI: 10.1016/j.freeradbiomed.2014.07.001.
- 33. Mishra M, Zhong Q, Kowluru RA. Epigenetic modifications of keap1 regulate its interaction with the protective factor nrf2 in the development of diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2014,55(11):7256-7265.DOI:10.1167/iovs.14-15193.
- 34. Pirola L. The DCCT/EDIC study: epigenetic clues after three decades[J]. Diabetes, 2014,63(5):1460-1462.DOI: 10.2337/db14-0238.
- 35. Pirola L, Balcerczyk A, Tothill RW, et al. Genome-wide analysis distinguishes hyperglycemia regulated epigenetic signatures of primary vascular cells[J]. Genome Res, 2011,21(10): 1601- 1615.DOI: 10.1101/gr.116095.110.
- 36. Perrone L, Devi TS, Hosoya KI, et al. Inhibition of TXNIP expression in vivo blocks early pathologies of diabetic retinopathy[J]. Cell Death Dis, 2010,1:65.DOI: 10.1038/cddis.2010.42.
- 37. Kowluru RA, Santos JM, Zhong Q. Sirt1,anegative regulator of matrix metalloproteinase-9 in diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 2014,55(9):5653-5660.DOI: 10.1167 /iovs. 14-14383.
- 38. Zhang Y, Liu J, Tian XY, et al. Inhibition of bone morphogenic protein 4 restores endothelial function in db/db diabetic mice[J]. Arterioscler Thromb Vasc Biol, 2014,34(1):152-159.DOI: 10.1161/ATVBAHA.113.302696.
- 39. Giacco F, Brownlee M. Oxidative stress and diabetic complications[J]. Circ Res, 2010,107(9):1058-1070.DOI: 10.1161/CIRCRESAHA.110.223545.
- 40. Guttman M, Amit I, Garber M, et al. Chromatin signature reveals overathousand highly conserved large non-coding RNAs in mammals[J]. Nature, 2009,458(7235):223-227.DOI: 10.1038/nature07672.
- 41. Shukla GC, Singh J, Barik S. MicroRNAs: processing, maturation, target recognition and regulatory functions[J]. Mol Cell Pharmacol, 2011,3(3):83-92.
- 42. Silva VA, Polesskaya A, Sousa TA, et al. Expression and cellular localization of microRNA-29b and RAX, an activator of the RNA-dependent protein kinase (PKR), in the retina of streptozotocin-induced diabetic rats[J]. Mol Vis, 2011,17:2228-2240.
- 43. McArthur K, Feng B, Wu Y, et al. MicroRNA-200b regulates vascular endothelial growth factor-mediated alterations in diabetic retinopathy[J]. Diabetes, 2011,60(4):1314-1323.DOI: 10.2337/db10-1557.
- 44. Kovacs B, Lumayag S, Cowan C, et al. MicroRNAs in early diabetic retinopathy in streptozotocin-induced diabetic rats[J]. Invest Ophthalmol Vis Sci, 2011,52(7):4402-4409.DOI: 10.1167/iovs.10-6879.
- 45. Feng B, Chen S, McArthur K, et al. miR-146a-Mediated extracellular matrix protein production in chronic diabetes complications[J]. Diabetes, 2011,60(11):2975-2984.DOI: 10.2337/db11-0478.
- 46. Guttman M, Rinn JL. Modular regulatory principles of large non-coding RNAs[J]. Nature, 2012,482(7385):339-346.DOI: 10.1038/nature10887.
- 47. Kameswaran V, Kaestner KH. The Missing lnc(RNA) between the pancreatic beta-cell and diabetes[J]. Front Genet, 2014,5:200.DOI: 10.3389/fgene.2014.00200.
- 48. Leung A, Trac C, Jin W, et al. Novel long noncoding RNAs are regulated by angiotensin II in vascular smooth muscle cells[J]. Circ Res, 2013,113(3):266-278.DOI:10.1161/CIRCRESAHA. 112.300849.
- 49. Alvarez ML, DiStefano JK. Functional characterization of the plasmacytoma variant translocation 1 gene (PVT1) in diabetic nephropathy[J/OL]. PLoS One, 2011,6(4): 18671 [2011- 04- 22].http://www.doc88.com/p-0189783280919.html.DOI: 10.1371/journal.pone.0018671.
- 50. Kowluru RA, Kowluru A, Mishra M, et al. Oxidative stress and epigenetic modifications in the pathogenesis of diabetic retinopathy[J]. Prog Retin Eye Res, 2015,48:40-61.DOI:10.1016/j. preteyeres.2015.05.001.
- 51. Moore TC, Moore JE, Kaji Y, et al. The role of advanced glycation end products in retinal microvascular leukostasis[J]. Invest Ophthalmol Vis Sci, 2003,44(10):4457-4464.
- 52. Genuth S, Sun W, Cleary P, et al. Skin advanced glycation end products glucosepane and methylglyoxal hydroimidazolone are independently associated with long-term microvascular complication progression of type 1 diabetes[J]. Diabetes, 2015,64(1):266-278.DOI: 10.2337/db14-0215.
- 53. Rabbani N, Thornalley PJ. Hidden complexities in the measurement of fructosyl-lysine and advanced glycation end products for risk prediction of vascular complications of diabetes[J]. Diabetes, 2015,64(1):9-11.DOI:10.2337/db14-1516.
- 54. Zhang L, Chen B, Tang L. Metabolic memory: mechanisms and implications for diabetic retinopathy[J]. Diabetes Res Clin Pract, 2012,96(3):286-293.DOI: 10.1016/j.diabres.2011.12.006.
- 55. Zhong Q, Kowluru RA. Role of histone acetylation in the development of diabetic retinopathy and the metabolic memory phenomenon[J].JCell Biochem, 2010,110(6):1306-1313.DOI: 10.1002/jcb.22644.
- 56. White NH, Sun W, Cleary PA, et al. Effect of prior intensive therapy in type 1 diabetes on 10-year progression of retinopathy in the DCCT/EDIC: comparison of adults and adolescents[J]. Diabetes, 2010,59(5):1244-1253.DOI: 10.2337/db09-1216.
- 57. Manolopoulos VG, Ragia G, Tavridou A. Pharmacogenomics of oral antidiabetic medications: current data and pharmacoepigenomic perspective[J]. Pharmacogenomics, 2011,12(8):1161-1191. DOI:10.2217/pgs.11.65.
- 58. Sandholm N, Salem RM, McKnight AJ, et al. New susceptibility loci associated with kidney disease in type 1 diabetes[J/OL]. PLoS Genet, 2012,8(9):1002921[2012-09-20]. http://lup.lub.lu.se/luur/download?func=downloadFile&recordOId=3287820&fileOId=3460726. DOI: 10.1371/journal.pgen.1002921.
- 59. Xie M, Tian J, Luo Y, et al. Effects of 5-aza-2′-deoxycytidine and trichostatinAon high glucose- and interleukin-1beta-induced secretory mediators from human retinal endothelial cells and retinal pigment epithelial cells[J]. Mol Vis, 2014,20:1411-1421.
- 60. Zhang Z, Tong N, Gong Y, et al. Valproate protects the retina from endoplasmic reticulum stress-induced apoptosis after ischemia-reperfusion injury[J]. Neurosci Lett, 2011,504(2):88-92. DOI: 0.1016/j.neulet.2011.09.003.
- 61. 张笃贞, 张涤, 孙鹏, 等. 白藜芦醇对糖尿病大鼠视网膜中SIRT1基因表达的干预作用[J]. 眼科新进展, 2014,34(4):322-325.DOI:10.13389/j.cnki.rao.2014.0087.Zhang DZ,Zhang D,Sun P.Effects of resveratrol on SIRT1 gene expression in retina of diabetic rat[J].Rec Adv Ophthalmol,2014,34(2):322-325.DOI:10.13389/j.cnki.rao.2014.0087.
- 62. Nguyen QD, Schachar RA, Nduaka CI, et al. Phase 1 dose-escalation study ofasiRNA targeting the RTP801 gene in age-related macular degeneration patients[J]. Eye (Lond), 2012,26(8):1099-1105.DOI: 10.1038/eye.2012.106.
- 63. Sun AX, Crabtree GR, Yoo AS. MicroRNAs: regulators of neuronal fate[J]. Curr Opin Cell Biol, 2013,25(2):215-221. DOI: 10.1016/j.ceb.2012.12.007.
- 64. Rafehi H, El-Osta A, Karagiannis TC. Genetic and epigenetic events in diabetic wound healing[J]. Int Wound J, 2011,8(1):12-21.DOI: 10.1111/j.1742-481X.2010.00745.x.
- 65. Vecellio M, Spallotta F, Nanni S, et al. The histone acetylase activator pentadecylidenemalonate 1b rescues proliferation and differentiation in the human cardiac mesenchymal cells of type 2 diabetic patients[J]. Diabetes, 2014,63(6):2132-2147. DOI: 10.2337/db13-0731.
- 66. Kassan M, Choi SK, Galan M, et al. Enhanced p22phox expression impairs vascular function through p38 and ERK1/2 MAP kinase-dependent mechanisms in type 2 diabetic mice[J]. AmJPhysiol Heart Circ Physiol, 2014,306(7):972-980.DOI: 10.1152/ajpheart.00872.2013.
- 67. Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms[J]. Nat Rev Genet, 2009,10(5):295-304.DOI: 10.1038/nrg2540.
- 68. Ronn T, Ling C. Effect of exercise on DNA methylation and metabolism in human adipose tissue and skeletal muscle[J]. Epigenomics, 2013,5(6):603-605.DOI: 10.2217/epi.13.61.
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