Role of mitochondrial DNA damage in the development of diabetic retinopathy, and the metabolic memory phenomenon associated with its progression

Antioxidants and Redox Signaling

Volumn 13, Issue 6, 2010, Pages 797-805

  Madsen Bouterse, Sally A ^a   Mohammad, Ghulam ^a   Kanwar, Mamta ^a   Kowluru, Renu A ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA GLYCOSYLTRANSFERASE; MITOCHONDRIAL DNA; MULTIENZYME COMPLEX;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIABETIC RETINOPATHY; DNA DAMAGE; DNA DETERMINATION; GLYCEMIC CONTROL; HYPERGLYCEMIA; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; RESPIRATORY CHAIN; STREPTOZOCIN DIABETES; ANIMAL; DISEASE COURSE; GENETICS; METABOLISM; MITOCHONDRIAL GENOME; OXIDATION REDUCTION REACTION; PATHOLOGY; WISTAR RAT;

RATTUS;

ANIMALS; DIABETIC RETINOPATHY; DISEASE PROGRESSION; DNA DAMAGE; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; GENOME, MITOCHONDRIAL; HYPERGLYCEMIA; MALE; OXIDATION-REDUCTION; RATS; RATS, WISTAR;

EID: 77954909054     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2009.2932     Document Type: Article

References (48)

1. Ayala-Torres S, Chen Y, Svoboda T, Rosenblatt J, and Van Houten B. Analysis of gene-specific DNA damage and repair using quantitative polymerase chain reaction. Methods 22: 135-147, 2000
2. Bai Y and Attardi G. The mtDNA-encoded ND6 subunit of mitochondrial NADH dehydrogenase is essential for the assembly of the membrane arm and the respiratory function of the enzyme. EMBO J 17: 4848-4858, 1998
3. Ballinger SW, Bouder TG, Davis GS, Judice SA, Nicklas JA, and Albertini RJ. Mitochondrial genome damage associated with cigarette smoking. Cancer Res 56: 5692-5697, 1996
4. Ballinger SW, Van Houten B, Jin GF, Conklin CA, and Godley BF. Hydrogen peroxide causes significant mito-chondrial DNA damage in human RPE cells. Exp Eye Res 68: 765-772, 1999
5. Bourges I, Ramus C, Mousson de Camaret B, Beugnot R, Remacle C, Cardol P, Hofhaus G, and Issartel JP. Structural organization of mitochondrial human complex. I: Role of the ND4 and ND5 mitochondria-encoded subunits and interaction with prohibitin. Biochem J 383: 491-799, 2004
6. Brownlee M. The pathobiology of diabetic complications: A unifying mechanism. Diabetes 54: 1615-1625, 2005
7. Cardol P, Matagne RF, and Remacle C. Impact of mutations affecting ND mitochondria-encoded subunits on the activity and assembly of complex I in Chlamydomonas. Implication for the structural organization of the enzyme. J Mol Biol 19: 1211-1221, 2002
8. Chen XJ and Butow RA. The organization and inheritance of the mitochondrial genome. Nat Rev Genet 6: 815-825, 2008
9. Cortina MS, Gordon WC, Lukiw WJ, and Bazan NG. Oxi-dative stress-induced retinal damage up-regulates DNA polymerase gamma and 8-oxoguanine-DNA- glycosylase in photoreceptor synaptic mitochondria. Exp Eye Res 81: 742-750, 2005
10. Cortopassi G and Wang E. Modeling the effects of age-related mtDNA mutation accumulation; complex I deficiency, superoxide and cell death. Biochim Biophys Acta 1271: 171-176, 1995
11. De Souza-Pinto NC, Wilson DM 3rd, Stevnsner TV, and Bohr VA. Mitochondrial DNA, base excision repair and neurodegeneration. DNA Repair (Amst) 7:91098-91109, 2008
12. Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329: 977-986, 1993
13. 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: 381-389, 2000
14. Diabetes Control and Complications Trial=Epidemiology of Diabetes Interventions and Complications Research Group. Prolonged effect of intensive therapy on the risk of reti-nopathy complications in patients with type 1 diabetes mellitus: 10 years after the Diabetes Control and Complications Trial. Arch Ophthalmol 126: 1707-1715, 2008
15. Druzhyna NM, Wilson GL, and LeDoux SP. Mitochondrial DNA repair in aging and disease. Mech Ageing Dev 129: 383-390, 2008
16. Du Y, Miller CM, and Kern TS. Hyperglycemia increases mitochondrial superoxide in retina and retinal cells. Free Radic Biol Med 35: 1491-1499, 2003
17. Godley BF, Shamsi FA, Liang FQ, Jarrett SG, Davies S, and Boulton M. Blue light induces mitochondrial DNA damage and free radical production in epithelial cells. J Biol Chem 280: 21061-21066, 2005
18. Hegde ML, Hazra TK, and Mitra S. Early steps in the DNA base excision=single-strand interruption repair pathway in mammalian cells. Cell Res 18: 27-47, 2008
19. Herrmann JM and Neupert W. What fuels polypeptide translocation? An energetical view on mitochondrial protein sorting. Biochem Biophys Acta 1459: 331-338, 2000
20. Jarrett SG, Albon J, and Boulton M. The contribution of DNA repair and antioxidants in determining cell type-specific resistance to oxidative stress. Free Radic Res 40: 155-1165, 2006
21. Kanwar M, Chan PS, Kern TS, and Kowluru RA. Oxidative damage in the retinal mitochondria of diabetic mice: Possible protection by superoxide dismutase. Invest Ophthalmol Vis Sci 48: 3805-3811, 2007
22. Kanwar M and Kowluru RA. Diabetes regulates small molecular weight G-protein, H-Ras, in the microvasculature of the retina: Implication in the development of retinopathy. Microv Res 76: 189-193, 2008
23. Kanwar M and Kowluru RA. Role of glyceraldehyde 3-phosphate dehydrogenase in the development and progression of diabetic retinopathy. Diabetes 58: 227-234, 2009
24. Kern TS, Tang J, Mizutani M, Kowluru RA, Nagaraj RH, Romeo G, Podesta F, and Lorenzi M. Response of capillary cell death to aminoguanidine predicts the development of retinopathy: Comparison of diabetes and galactosemia. Invest Ophthalmol Vis Sci 41: 3972-3978, 2000
25. Kowluru RA, Tang J, and Kern TS. Abnormalities of retinal metabolism in diabetes and experimental galactosemia. VII. Effect of long-term administration of antioxidants on the development of retinopathy. Diabetes 50: 1938-1942, 2001
26. Kowluru RA. Effect of re-institution of good glycemic control on retinal oxidative stress and nitrative stress in diabetic rats. Diabetes 52: 818-823, 2003
27. Kowluru RA and Abbas SN. Diabetes-induced mitochon-drial dysfunction in the retina. Invest Ophthalmol Vis Sci 44: 5327-5334, 2003
28. Kowluru RA, Koppolu P, Chakrabarti S, and Chen S. Diabetes-induced activation of nuclear transcriptional factor in the retina, and its inhibition by antioxidants. Free Radic Res 37: 1169-1180, 2003
29. Kowluru RA, Chakrabarti S, and Chen S. Re-institution of good metabolic control in diabetic rats and activation of caspase-3 and nuclear transcriptional factor in the retina. Acta Diabetologica 44: 194-199, 2004
30. Kowluru RA, Atasi L, and Ho YS. Role of mitochondrial superoxide dismutase in the development of diabetic reti-nopathy. Invest Ophthalmol Vis Sci 47: 1594-1599, 2006
31. Kowluru RA, Kanwar M, and Kennedy A. Metabolic memory phenomenon and accumulation of peroxynitrite in retinal capillaries. Exp Diab Res 2007: 21976, 2007
32. Kowluru RA, Kanwar M, Chan PS, and Zhang JP. Inhibition of retinopathy and retinal metabolic abnormalities in diabetic rats with AREDS-based micronutrients. Arch Ophthal-mol 126: 1266-1272, 2008
33. Kowluru RA and Chan PS. Metabolic memory in diabetes-from in vitro oddity to in vivo problem: Role of Apoptosis. Brain Res Bull 87: 2297-302, 2010
34. Kucej M, Kucejova B, Subramanian R, Chen XJ, and Butow RA. Mitochondrial nucleoids undergo remodeling in response to metabolic cues. J Cell Sci 121: 1861-1868, 2008
35. Liang FQ and Godley BF. Oxidative stress-induced mito-chondrial DNA damage in human retinal pigment epithelial cells: A possible mechanism for RPE aging and age-related macular degeneration. Exp Eye Res 76: 397-403, 2003
36. Madsen-Bouterse SA, Zhong Q, Mohammad G, Ho YS, and Kowluru RA. Diabetic retinopathy: Protection of oxidative damage of mitochondrial DNA by manganese superoxide dismutase, Free Radic Res 44: 313-321, 2010
37. Mizutani M, Kern TS, and Lorenzi M. Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J Clin Invest 97: 2883-2890, 1996
38. Obrosova IG, Minchenko AG, Marinescu V, Fathallah L, Kennedy A, Stockert CM, Frank RN, and Stevens MJ. Ant-ioxidants attenuate early up regulation of retinal vascular endothelial growth factor in streptozotocin-diabetic rats. Diabetologia 44: 1102-1110, 2001
39. Rana M, de Coo I, Diaz F, Smeets H, and Moraes CT. An out-of-frame cytochrome b gene deletion from a patient with parkinsonism is associated with impaired complex III assembly and an increase in free radical production. Ann Neurol 48: 774-781, 2000
40. Roy S, Sala R, Cagliero E, and Lorenzi M. Overexpression of fibronectin induced by diabetes or high glucose: phenomenon with a memory. Proc Natl Acad Sci USA 87: 404-408, 1990
41. Schärer OD and Jiricny J. Recent progress in the biology, chemistry and structural biology of DNA glycosylases. Bioessays 23: 270-281, 2001
42. Stuart JA and Brown MF. Mitochondrial DNA maintenance and bioenergetics. Biochim Biophys Acta 1757: 79-89, 2006
43. Van Houten B, Woshner V, and Santos JH. Role of mito-chondrial DNA in toxic responses to oxidative stress. DNA Repair (Amst) 5: 145-152, 2005
44. Wang AL, Lukas TJ, Yuan M, and Neufeld AH. Increased mitochondrial DNA damage and down-regulation of DNA
45. repair enzymes in aged rodent retinal pigment epithelium and choroid. Mol Vis 14: 644-651, 2008
46. Wang AL, Lukas TJ, Yuan M, and Neufeld AH. Age-related increase in mitochondrial DNA damage and loss of DNA repair capacity in the neural retina. Neurobiol Aging, 2008 Dec 10. [Epub ahead of print]
47. Xie L, Zhu X, Hu Y, Li T, Gao Y, Shi Y, and Tang S. Mi-tochondrial DNA oxidative damage triggering mitochon-drial dysfunction and apoptosis in high glucose-induced HRECs. Invest Ophthalmol Vis Sci 49: 4203-4209, 2008
48. Yakes FM and Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci USA 94: 514-519, 1997.