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 Radical Biology and Medicine

Volumn 75, Issue , 2014, Pages 129-139

  Mishra, Manish ^a   Zhong, Qing ^a   Kowluru, Renu A ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

Diabetic retinopathy; Epigenetic modifications; Free radicals; Glutamate cysteine ligase; GSH; Histone methylation; Nrf2

Indexed keywords

DMETHYLATION OF LYSINE 4 HISTONE 3; GLUCOSE; GLUTAMATE CYSTEINE LIGASE; GLYCOSYLATED HEMOGLOBIN; HISTONE DEMETHYLASE; HISTONE H3; HISTONE H4; LYSINE; METHYLATION OF LYSINE 4 HISTONE 3; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; GLUTATHIONE; HISTONE; LSD1 PROTEIN, RAT; NFE2L2 PROTEIN, HUMAN; PROTEIN BINDING;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; BINDING AFFINITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DIABETIC RETINOPATHY; DISEASE ASSOCIATION; DNA BINDING; DNA MODIFICATION; ENDOTHELIUM CELL; EPIGENETICS; GENE ACTIVATION; GENE EXPRESSION; GLYCEMIC CONTROL; HISTONE METHYLATION; HISTONE MODIFICATION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MALE; MEMORY; METABOLIC MEMORY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; RAT; REGULATORY MECHANISM; TRANSCRIPTION INITIATION; ANIMAL; BIOSYNTHESIS; BOVINE; CELL LINE; CYTOLOGY; DNA METHYLATION; EXPERIMENTAL DIABETES MELLITUS; GENETIC EPIGENESIS; GENETICS; HYPERGLYCEMIA; METABOLISM; MIDDLE AGED; OXIDATIVE STRESS; PATHOLOGY; RETINA; RNA INTERFERENCE; WISTAR RAT;

AGED; ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; CATTLE; CELL LINE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; DNA METHYLATION; EPIGENESIS, GENETIC; GLUCOSE; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; HISTONE DEMETHYLASES; HISTONES; HUMANS; HYPERGLYCEMIA; MALE; MIDDLE AGED; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROTEIN BINDING; RATS; RATS, WISTAR; RETINA; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84906331499     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.07.001     Document Type: Article

References (48)

1. J.W. Baynes Role of oxidative stress in development of complications in diabetes Diabetes 40 1991 405 412
2. R.A. Kowluru, T.S. Kern, and R.L. Engerman Abnormalities of retinal metabolism in diabetes or experimental galactosemia. IV. Antioxidant defense system Free Radic. Biol. Med. 22 1997 587 592 (Pubitemid 27043395)
3. M. Brownlee The pathobiology of diabetic complications: a unifying mechanism Diabetes 54 2005 1615 1625 (Pubitemid 40770750)
4. T.S. Kern, R. Kowluru, and R.L. Engerman Abnormalities of retinal metabolism in diabetes or galactosemia: ATPases and glutathione Invest. Ophthalmol. Visual Sci. 35 1994 2962 2967 (Pubitemid 24186397)
5. R.A. Kowluru, J. Tang, and T.S. Kern Abnormalities of retinal metabolism in diabetes and experimental galactosemia. VII. Effect of long-term administration of antioxidants on the development of retinopathy Diabetes 50 2001 1938 1942 (Pubitemid 33641616)
6. R.A. Kowluru Diabetic retinopathy, oxidative stress and antioxidants Curr. Top. Nutraceutical Res. 3 2005 209 218 (Pubitemid 43192182)
7. R.A. Kowluru Mitochondria damage in the pathogenesis of diabetic retinopathy and in the metabolic memory associated with its continued progression Curr. Med. Chem. 20 2013 3226 3233
8. R.A. Kowluru, and P.S. Chan Oxidative stress and diabetic retinopathy Exp. Diabetes Res. 2007 2007 43603
9. Q. Zhong, M. Mishra, and R.A. Kowluru Transcription factor Nrf2-mediated antioxidant defense system in the development of diabetic retinopathy Invest. Ophthalmol. Visual Sci. 54 2013 3941 3948
10. T.W. Kensler, N. Wakabayashi, and S. Biswal Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway Annu. Rev. Pharm. Toxicol. 47 2007 89 116
11. S.C. Lu Regulation of glutathione synthesis Mol. Aspects Med. 30 2009 42 59
12. A.M. Erickson, Z. Nevarea, J.J. Gipp, and R.T. Mulcahy Identification of a variant antioxidant response element in the promoter of the human glutamate-cysteine ligase modifier subunit gene: revision of the ARE consensus sequence J. Biol. Chem. 277 2002 30730 30737 (Pubitemid 34970769)
13. S.C. Lu Glutathione synthesis Biochim. Biophys. Acta 1830 2013 3143 3153
14. R.T. Mulcahy, M.A. Wartman, H.H. Bailey, and J.J. Gipp Constitutive and beta-naphthoflavone-induced expression of the human gamma-glutamylcysteine synthetase heavy subunit gene is regulated by a distal antioxidant response element/TRE sequence J. Biol. Chem. 272 1997 7445 7454 (Pubitemid 27166457)
15. R. Jaenisch, and A. Bird Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals Nat. Genet. 33 2003 245 254 (Pubitemid 36278835)
16. A. Bird DNA methylation patterns and epigenetic memory Genes Dev. 16 2002 6 21 (Pubitemid 34049633)
17. E.R. Gibney, and C.M. Nolan Epigenetics and gene expression Heredity (Edinburgh) 105 2010 4 13
18. H. Stower Epigenetics: dynamic DNA methylation Nat. Rev. Genet. 13 2011 75
19. R.J. Klose, and Y. Zhang Regulation of histone methylation by demethylimination and demethylation Nat. Rev. Mol. Cell Biol. 8 2007 307 318 (Pubitemid 46474659)
20. F. Lan, A.C. Nottke, and Y. Shi Mechanisms involved in the regulation of histone lysine demethylases Curr. Opin. Cell Biol. 20 2008 316 325
21. R.J. Sims, and D. Reinberg Histone H3 Lys 4 methylation: caught in a bind? Genes Dev. 20 2006 2779 2786 (Pubitemid 44771740)
22. A. Shilatifard Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation Curr. Opin. Cell Biol. 20 2008 341 348
23. W.G. Kaelin Jr., and S.L. McKnight Influence of metabolism on epigenetics and disease Cell 153 2013 56 69
24. Q. Zhong, and R.A. Kowluru Epigenetic modification of Sod2 in the development of diabetic retinopathy and in the metabolic memory: role of histone methylation Invest. Ophthalmol. Visual Sci. 54 2013 244 250
25. Q. Zhong, and R.A. Kowluru Regulation of matrix metalloproteinase-9 by epigenetic modifications and the development of diabetic retinopathy Diabetes 62 2013 2559 2568
26. A. Chicas, A. Kapoor, X. Wang, O. Aksoy, A.G. Evertts, and M.Q. Zhang et al. H3K4 demethylation by Jarid1a and Jarid1b contributes to retinoblastoma-mediated gene silencing during cellular senescence Proc. Natl. Acad. Sci. USA 109 2012 8971 8976
27. 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. 342 2000 381 389
28. R.L. Engerman, and T.S. Kern Progression of incipient diabetic retinopathy during good glycemic control Diabetes 36 1987 808 812 (Pubitemid 17145301)
29. R.A. Kowluru Effect of re-institution of good glycemic control on retinal oxidative stress and nitrative stress in diabetic rats Diabetes 52 2003 818 823 (Pubitemid 36323591)
30. 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. USA 105 2008 9047 9052
31. M. Szyf, and M.J. Meaney Epigenetics, behaviour, and health Allergy Asthma Clin. Immunol. 4 2008 37 49 (Pubitemid 351729465)
32. L.M. Villeneuve, M.A. Reddy, and R. Natarajan Epigenetics: deciphering its role in diabetes and its chronic complications Clin. Exp. Pharm. Physiol. 38 2011 401 409
33. Q. Zhong, and R.A. Kowluru Role of histone acetylation in the development of diabetic retinopathy and the metabolic memory phenomenon J. Cell. Biochem. 110 2010 1306 1313
34. 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
35. S. Tewari, Q. Zhong, J.M. Santos, and R.A. Kowluru Mitochondria DNA replication and DNA methylation in the metabolic memory associated with continued progression of diabetic retinopathy Invest. Ophthalmol. Visual Sci. 53 2012 4881 4888
36. S. Jayaraman Epigenetic mechanisms of metabolic memory in diabetes Circ. Res. 110 2012 1039 1041
37. S.T. Keating, and A. El-Osta Epigenetic changes in diabetes Clin. Genet. 84 2013 1 10
38. R.A. Kowluru, and P.S. Chan Metabolic memory in diabetes - from in vitro oddity to in vivo problem: role of apoptosis Brain Res. Bull. 87 2010 297 302
39. Q. Zhong, and R.A. Kowluru Diabetic retinopathy and damage to mitochondrial structure and transport machinery Invest. Ophthalmol. Visual Sci. 52 2011 8739 8746
40. R.A. Kowluru, and M. Kanwar Oxidative stress and the development of diabetic retinopathy: contributory role of matrix metalloproteinase-2 Free Radic. Biol. Med. 46 2009 1677 1685
41. S.K. Niture, R. Khatri, and A.K. Jaiswal Regulation of Nrf2 - an update Free Radic. Biol. Med. 66 2014 36 44
42. A.K. Jain, D. Bloom, and A.K. Jaiswal Nuclear import and export signals in control of Nrf2 J. Biol. Chem. 280 2005 29158 29168 (Pubitemid 41161367)
43. L.M. Aleksunes, and J.E. Manautou Emerging role of Nrf2 in protecting against hepatic and gastrointestinal disease Toxicol. Pathol. 35 2007 459 473 (Pubitemid 46911886)
44. A. Saha, J. Wittmeyer, and B.R. Cairns Chromatin remodelling: the industrial revolution of DNA around histones Nat. Rev. Mol. Cell. Biol. 7 2006 437 447 (Pubitemid 44050097)
45. B.D. Strahl, and C.D. Allis The language of covalent histone modifications Nature 403 2000 41 45 (Pubitemid 30038513)
46. 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. USA 87 1990 404 408
47. S.A. Madsen-Bouterse, G. Mohammad, M. Kanwar, and R.A. Kowluru Role of mitochondrial DNA damage in the development of diabetic retinopathy, and the metabolic memory phenomenon associated with its progression Antioxid. Redox Signaling 13 2010 797 805
48. R.A. Kowluru, M. Kanwar, and A. Kennedy Metabolic memory phenomenon and accumulation of peroxynitrite in retinal capillaries. Exp Diabetes Res. 2007 2007 2196