Contribution of epigenetics in diabetic retinopathy

Science China Life Sciences

Volumn 58, Issue 6, 2015, Pages 556-563

  Kowluru, Renu A ^a   Mishra, Manish ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

diabetic retinopathy; epigenetic modifications; histone acetylation; histone methylation; miRNA

Indexed keywords

CARRIER PROTEIN; GELATINASE B; HISTONE; MICRORNA; SUPEROXIDE DISMUTASE; TXNIP PROTEIN, HUMAN;

ACETYLATION; ANIMAL; CHEMISTRY; DIABETIC RETINOPATHY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; MOUSE; PATHOPHYSIOLOGY; RETINA; UPREGULATION;

ACETYLATION; ANIMALS; CARRIER PROTEINS; DIABETIC RETINOPATHY; DNA METHYLATION; DOWN-REGULATION; EPIGENESIS, GENETIC; EPIGENOMICS; GENE EXPRESSION REGULATION; HISTONES; HUMANS; MATRIX METALLOPROTEINASE 9; MICE; MICRORNAS; MITOCHONDRIA; RETINA; SUPEROXIDE DISMUTASE; UP-REGULATION;

EID: 84931567071     PISSN: 16747305     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11427-015-4853-0     Document Type: Review

References (93)

1. Zheng Y, He M, Congdon N. The worldwide epidemic of diabetic retinopathy. Indian J Ophthalmol, 2012, 60: 428–431
2. Frank RN. Diabetic retinopathy. N Engl J Med, 2004, 350: 48–58
3. Lim LS, Wong TY. Lipids and diabetic retinopathy. Expert Opin Biol Ther, 2012, 12: 93–105
4. Zhang W, Liu H, Rojas M, Caldwell RW, Caldwell RB. Antiinflammatory therapy for diabetic retinopathy. Immunotherapy, 2011, 3: 609–628
5. Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet, 2010, 376: 124–136
6. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature, 2001, 414: 813–820
7. Kowluru RA, Chan PS. Oxidative stress and diabetic retinopathy. Exp Diabetes Res, 2007, 2007: 43603
8. Kowluru RA, Santos JM, Mishra M. Epigenetic modifications and diabetic retinopathy. Biomed Res Int, 2013, 2013: 635284
9. Abhary S, Hewitt AW, Burdon KP, Craig JE. A systematic meta-analysis of genetic association studies for diabetic retinopathy. Diabetes, 2009, 58: 2137–2147
10. Ma J, Li Y, Zhou F, Xu X, Guo G, Qu Y. Meta-analysis of association between the Pro12Ala polymorphism of the peroxisome proliferator–activated receptor-?2 gene and diabetic retinopathy in Caucasians and Asians. Mol Vis, 2012, 18: 2352–2360
11. Bonnefond A, Saulnier PJ, Stathopoulou MG, Grarup N, Ndiaye NC, Roussel R, Nezhad MA, Dechaume A, Lantieri O, Hercberg S, Lauritzen T, Balkau B, El-Sayed Moustafa JS, Hansen T, Pedersen O, Froguel P, Charpentier G, Marre M, Hadjadj S, Visvikis-Siest S. What is the contribution of two genetic variants regulating VEGF levels to type 2 diabetes risk and to microvascular complications? PLoS One, 2013, 8: e55921
12. Regha K, Sloane MA, Huang R, Pauler FM, Warczok KE, Melikant B, Radolf M, Martens JH, Schotta G, Jenuwein T, Barlow DP. Active and repressive chromatin are interspersed without spreading in an imprinted gene cluster in the mammalian genome. Mol Cell, 2007, 27: 353–366
13. Gemenetzi M, Lotery AJ. The role of epigenetics in age-related macular degeneration. Eye (Lond), 2014, 28: 1407–1417
14. Uribe-Lewis S, Woodfine K, Stojic L, Murrell A. Molecular mechanisms of genomic imprinting and clinical implications for cancer. Expert Rev Mol Med, 2011, 13: e2
15. Toiyama Y, Okugawa Y, Goel A. DNA methylation and microRNA biomarkers for noninvasive detection of gastric and colorectal cancer. Biochem Biophys Res Commun, 2014, 455: 43–57
16. Gravina S, Vijg J. Epigenetic factors in aging and longevity. Pflugers Arch, 2010, 459: 247–258
17. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science, 2001, 293: 1068–1070
18. Lim U, Song MA. Dietary and lifestyle factors of DNA methylation. Methods Mol Biol, 2012, 863: 359–376
19. Esteller M. Cancer epigenomics: DNA methylomes and histonemodification maps. Nat Rev Genet, 2007, 8: 286–298
20. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, Leonhardt H, Jaenisch R. Induction of tumors in mice by genomic hypomethylation. Science, 2003, 300: 489–492
21. Guibert S, Forne T, Weber M. Dynamic regulation of DNA methylation during mammalian development. Epigenomics, 2009, 1: 81–98
22. Majumdar S, Buckles E, Estrada J, Koochekpour S. Aberrant DNA methylation and prostate cancer. Curr Genomics, 2011, 12: 486–505
23. Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev, 2011, 2510: 1010–1022
24. Zhang P, Huang B, Xu X, Sessa WC. Ten-eleven translocation (Tet) and thymine DNA glycosylase (TDG), components of the demethylation pathway, are direct targets of miRNA-29a. Biochem Biophys Res Commun, 2013, 437: 368–373
25. Kohli RM, Zhang Y. TET enzymes, TDG and the dynamics of DNA demethylation. Nature, 2013, 502: 472–479
26. Zhu JK. Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet, 2009, 43: 143–166
27. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 1997, 389: 251–260
28. Gurard-Levin Z, Almouzni G. Histone modifications and a choice of variant: a language that helps the genome express itself. F1000Prime Rep, 2014, 6: 76
29. Ropero S, Esteller M. The role of histone deacetylases (HDACs) in human cancer. Mol Oncol, 2007, 1: 19–25
30. Sarkar S, Goldgar S, Byler S, Rosenthal S, Heerboth S. Demethylation and re-expression of epigenetically silenced tumor suppressor genes: sensitization of cancer cells by combination therapy. Epigenomics, 2013, 5: 87–94
31. Glozak MA, Seto E. Histone deacetylases and cancer. Oncogene, 2007, 26: 5420–5432
32. Kouzarides T. Histone methylation in transcriptional control. Curr Opin Genet Dev, 2002, 12: 198–209
33. Kubicek S, Jenuwein T. A crack in histone lysine methylation. Cell, 2004, 119: 903–906
34. Kubicek S, O’Sullivan RJ, August EM, Hickey ER, Zhang Q, Teodoro ML, Rea S, Mechtler K, Kowalski JA, Homon CA, Kelly TA, Jenuwein T. Reversal of H3K9me2 by a small-molecule inhibitor for the G9a histone methyltransferase. Mol Cell, 2007, 25: 473–481
35. Nightingale KP, O'Neill LP, Turner BM. Histone modifications: signalling receptors and potential elements of a heritable epigenetic code. Curr Opin Genet Dev, 2006, 16: 125–136
36. Forneris F, Binda C, Battaglioli E, Mattevi A. LSD1: oxidative chemistry for multifaceted functions in chromatin regulation. Trends Biochem Sci, 2008, 33: 181–189
37. Musri MM, Carmona MC, Hanzu FA, Kaliman P, Gomis R, Párrizas M. Histone demethylase LSD1 regulates adipogenesis. J Biol Chem, 2010, 285: 30034–30041
38. Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet, 2009, 10: 295–304
39. Fahrner JA, Eguchi S, Herman JG, Baylin SB. Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res, 2002, 62: 7213–7218
40. Lehnertz B, Ueda Y, Derijck AA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AH. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol, 2003, 13: 1192–1200
41. Fuks F, Hurd PJ, Deplus R, Kouzarides T. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res, 2003, 31: 2305–2312
42. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM, Bollen M, Esteller M, Di Croce L, de Launoit Y, Fuks F. The polycomb group protein EZH2 directly controls DNA methylation. Nature, 2006, 439: 871–874
43. Zhao Q, Rank G, Tan YT, Li H, Moritz RL, Simpson RJ, Cerruti L, Curtis DJ, Patel DJ, Allis CD, Cunningham JM, Jane SM. PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat Struct Mol Biol, 2009, 16: 304–311
44. Dykxhoorn DM, Novina CD, Sharp PA. Killing the messenger: short RNAs that silence gene expression. Nat Rev Mol Cell Biol, 2003, 4: 457–467
45. Garzon R, Calin GA, Croce CM. MicroRNAs in Cancer. Annu Rev Med, 2009, 60: 167–179
46. Baer C, Claus R, Plass C. Genome-wide epigenetic regulation of miRNAs in cancer. Cancer Res, 2013, 73: 473–477
47. Cabezas-Cruz A, Lancelot J, Caby S, Oliveira G, Pierce RJ. Epigenetic control of gene function in schistosomes: a source of therapeutic targets? Front Genet, 2014, 5: 317
48. Stankov K, Benc D, Draskovic D. Genetic and epigenetic factors in etiology of diabetes mellitus type 1. Pediatrics, 2013, 132: 1112–1122
49. Kato M, Natarajan R. Diabetic nephropathy—emerging epigenetic mechanisms. Nat Rev Nephrol, 2014, 10: 517–530
50. Poirier LA, Brown AT, Fink LM, Wise CK, Randolph CJ, Delongchamp RR, Fonseca VA. Blood S-adenosylmethionine concentrations and lymphocyte methylenetetrahydrofolate reductase activity in diabetes mellitus and diabetic nephropathy. Metabolism, 2001, 50: 1014–1018
51. Tewari S, Zhong Q, Santos JM, Kowluru RA. Mitochondria DNA replication and DNA methylation in the metabolic memory associated with continued progression of diabetic retinopathy. Inves Ophthalmol Vis Sci, 2012, 53: 4881–4888
52. Williams KT, Garrow TA, Schalinske KL. Type I diabetes leads to tissue-specific DNA hypomethylation in male rats. J Nutr, 2008, 138: 2064–2069
53. Williams KT, Schalinske KL. Tissue-specific alterations of methyl group metabolism with DNA hypermethylation in the Zucker (type 2) diabetic fatty rat. Diabetes Metab Res Rev, 2012, 28: 123–131
54. Akçay T, Dinçer Y, Celebi N, Ilkova H. O(6)-methylguanine DNA methyltransferase activity in diabetic patients. Diabetes Res Clin Pract, 2003, 61: 1–6
55. Olsen AS, Sarras MP, Leontovich A, Intine RV. Heritable transmission of diabetic metabolic memory in zebrafish correlates with DNA hypomethylation and aberrant gene expression. Diabetes, 2012, 61: 485–491
56. Miao F, Chen Z, Zhang L, Wang J, Gao H, Wu X, Natarajan R. RNA-sequencing analysis of high glucose-treated monocytes reveals novel transcriptome signatures and associated epigenetic profiles. Physiol Genomics, 2013, 45: 287–299
57. 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
58. Miao F, Chen Z, Genuth S, Paterson A, Zhang L, Wu X, Li SM, Cleary P, Riggs A, Harlan DM, Lorenzi G, Kolterman O, Sun W, Lachin JM, Natarajan R; DCCT/EDIC Research Group. Evaluating the role of epigenetic histone modifications in the metabolic memory of type 1 diabetes. Diabetes, 2014, 63: 1748–1762
59. Wang Q, Wang Y, Minto A, Wang J, Shi Q, Li X, Quigg RJ. MicroRNA-377 is up-regulated and can lead to increased fibronectin production in diabetic nephropathy. FASEB J, 2008, 22: 4126–4135
60. Zhang Z, Peng H, Chen J, Chen X, Han F, Xu X, He X, Yan N. MicroRNA-21 protects from mesangial cell proliferation induced by diabetic nephropathy in db/db mice. FEBS Lett, 2009, 583: 2009–2014
61. Feng B, Chen S, McArthur K, Wu Y, Sen S, Ding Q, Feldman RD, Chakrabarti S. miR-146a-mediated extracellular matrix protein production in chronic diabetes complications. Diabetes, 2011, 60: 2975–2984
62. Syreeni A, El-Osta A, Forsblom C, Sandholm N, Parkkonen M, Tarnow L, Parving HH, McKnight AJ, Maxwell AP, Cooper ME, Groop PH; FinnDiane Study Group. Genetic examination of SETD7 and SUV39H1/H2 methyltransferases and the risk of diabetes complications in patients with type 1 diabetes. Diabetes, 2011, 60: 3073–3080
63. Maghbooli Z, Hossein-Nezhad A, Larijani B, Amini M, Keshtkar A. Global DNA methylation as a possible biomarker for diabetic retinopathy. Diabetes Metab Res Rev, 2015, 31: 183–189
64. Maghbooli Z, Larijani B, Emamgholipour S, Amini M, Keshtkar A, Pasalar P. Aberrant DNA methylation patterns in diabetic nephropathy. J Diabetes Metab Disord, 2014, 13: 69
65. 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
66. Kadiyala CS, Zheng L, Du Y, Yohannes E, Kao HY, Miyagi M, Kern TS. 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
67. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature, 2000, 404: 787–790
68. Kowluru RA. Mitochondria damage in the pathogenesis of diabetic retinopathy and in the metabolic memory associated with its continued progression. Curr Med Chem, 2013, 20: 3226–3233
69. Kanwar M, Chan PS, Kern TS, Kowluru RA. Oxidative damage in the retinal mitochondria of diabetic mice: possible protection by superoxide dismutase. Invest Ophthalmol Vis Sci, 2007, 48: 3805–3811
70. Zhong Q, Kowluru RA. Epigenetic changes in mitochondrial superoxide dismutase in the retina and the development of diabetic retinopathy. Diabetes, 2011, 60: 1304–1313
71. Zhong Q, Kowluru RA. Epigenetic modification of Sod2 in the development of diabetic retinopathy and in the metabolic memory: role of histone methylation. Invest Ophthalmol Vis Sci, 2013, 54: 244–250
72. Zhong Q, Mishra M, Kowluru RA. Transcription factor Nrf2-mediated antioxidant defense system in the development of diabetic retinopathy. Invest Ophthalmol Vis Sci, 2013, 54: 3941–3948
73. 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. Free Radic Biol Med, 2014, 75C: 129–139
74. Mishra M, Zhong Q, Kowluru RA. Epigenetic modifications of Keap1 regulate its interaction with the protective factor Nrf2 in the development of diabetic retinopa. Invest Ophthalmol Vis Sci, 2014, 55: 7256–7265
75. Kowluru RA. Role of matrix metalloproteinase-9 in the development of diabetic retinopathy and its regulation by H-Ras. Invest Ophthalmol Vis Sci, 2010, 51: 4320–4326
76. Kowluru RA, Zhong Q, Santos JM. Matrix metalloproteinases in diabetic retinopathy: potential role of MMP-9. Expert Opin Investig Drugs, 2012, 21: 797–805
77. Kowluru RA, Santos JM, Zhong Q. Sirt1, a negative regulator of matrix metalloproteinase-9 in diabetic retinopathy. Invest Ophthalmol Vis Sci, 2014, 55: 5653–5660
78. Zhong Q, Kowluru RA. Regulation of matrix metalloproteinase-9 by epigenetic modifications and the development of diabetic retinopathy. Diabetes, 2013, 62: 2559–2568
79. Perrone L, Devi TS, Hosoya K, Terasaki T, Singh LP. Thioredoxin interacting protein (TXNIP) induces inflammation through chromatin modification in retinal capillary endothelial cells under diabetic conditions. J Cell Physiol, 2009, 221: 262–272
80. Perrone L, Matrone C, Singh LP. Epigenetic modifications and potential new treatment targets in diabetic retinopathy. J Ophthalmol, 2014, 2014: 789120
81. Thomson DW, Bracken CP, Goodall GJ. Experimental strategies for microRNA target identification. Nucleic Acids Res, 2011, 39: 6845–6853
82. Caroli A, Cardillo MT, Galea R, Biasucci LM. Potential therapeutic role of microRNAs in ischemic heart disease. J Cardiol, 2013, 61: 315–320
83. Silva VA, Polesskaya A, Sousa TA, Corrêa VM, André ND, Reis RI, Kettelhut IC, Harel-Bellan A, De Lucca FL. Expression and cellular localization of microRNA-29b and RAX, an activator of the RNAdependent protein kinase (PKR), in the retina of streptozotocininduced diabetic rats. Mol Vis, 2011, 17: 2228–2240
84. Mastropasqua R, Toto L, Cipollone F, Santovito D, Carpineto P, Mastropasqua L. Role of microRNAs in the modulation of diabetic retinopathy. Prog Retin Eye Res, 2014, 43C: 92–107
85. Choi KC, Jung MG, Lee YH, Yoon JC, Kwon SH, Kang HB, Kim MJ, Cha JH, Kim YJ, Jun WJ, Lee JM, Yoon HG. Epigallocatechin-3-gallate, a histone acetyltransferase inhibitor, inhibits EBV-induced B lymphocyte transformation via suppression of RelA acetylation. Cancer Res, 2009, 69: 583–592
86. Wood JG, Rogina B, Lavu S, Howitz K, Helfand SL, Tatar M, Sinclair D. Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature, 2004, 430: 686–689
87. Morimoto T, Sunagawa Y, Kawamura T, Takaya T, Wada H, Nagasawa A, Komeda M, Fujita M, Shimatsu A, Kita T, Hasegawa K. The dietary compound curcumin inhibits p300 histone acetyltransferase activity and prevents heart failure in rats. J Clin Invest, 2008, 118: 868–878
88. Majid S, Dar AA, Ahmad AE, Hirata H, Kawakami K, Shahryari V, Saini S, Tanaka Y, Dahiya AV, Khatri G, Dahiya R. BTG3 tumor suppressor gene promoter demethylation, histone modification and cell cycle arrest by genistein in renal cancer. Carcinogenesis, 2009, 30: 662–670
89. Bassett SA, Barnett MP. The role of dietary histone deacetylases (HDACs) inhibitors in health and disease. Nutrients, 2014, 6: 4273–4301
90. Marsh DJ, Shah JS, Cole AJ. Histones and their modifications in ovarian cancer—drivers of disease and therapeutic targets. Front Oncol, 2014, 4: 144
91. Itamochi H. Targeted therapies in epithelial ovarian cancer: molecular mechanisms of action. World J Biol Chem, 2010, 1: 209–220
92. Song SH, Han SW, Bang YJ. Epigenetic-based therapies in cancer: progress to date. Drugs, 2011, 71: 2391–2403
93. Kim J, Hwang J, Jeong H, Song HJ, Shin J, Hur G, Park YW, Lee SH, Kim J. Promoter methylation status of VEGF receptor genes: a possible epigenetic biomarker to anticipate the efficacy of intracellular-acting VEGF-targeted drugs in cancer cells. Epigenetics, 2012, 7: 191–200