Mitochondrial and nuclear DNA damage and repair in age-related macular degeneration

International Journal of Molecular Sciences

Volumn 14, Issue 2, 2013, Pages 2996-3010

  Blasiak, Janusz ^a   Glowacki, Sylwester ^a   Kauppinen, Anu ^b   Kaarniranta, Kai ^b,c  

^a UNIVERSITY OF LODZ   (Poland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

Age related macular degeneration; DNA damage; DNA repair; Mitochondrial DNA; Oxidative stress

Indexed keywords

8 HYDROXYGUANINE; CELL NUCLEUS DNA; DNA DIRECTED DNA POLYMERASE GAMMA; DNA GLYCOSYLASE MUTY; HYDROGEN PEROXIDE; MITOCHONDRIAL DNA; PROTEIN MSH2; RAD51 PROTEIN;

AGING; DNA DAMAGE; DNA DEGRADATION; DNA END JOINING REPAIR; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EXCISION REPAIR; GENE EXPRESSION; GENE MUTATION; HUMAN; IONIZING RADIATION; LIGHT EXPOSURE; MISMATCH REPAIR; MUTAGENESIS; OXIDATIVE STRESS; PATHOGENESIS; PIGMENT EPITHELIUM; RECOMBINATION REPAIR; RETINA MACULA AGE RELATED DEGENERATION; REVIEW; SINGLE STRANDED DNA BREAK; ULTRAVIOLET RADIATION;

EID: 84875094879     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14022996     Document Type: Review

References (80)

1. McCall, M.R.; Frei, B. Can antioxidant vitamins materially reduce oxidative damage in humans? Free Radic. Biol. Med. 1999, 26, 1034-1053.
2. Naviaux, R.K. Oxidative Shielding or Oxidative Stress? J. Pharmacol. Exp. Ther. 2012, 342, 608-618.
3. Ohia, S.E.; Opere, C.A.; Leday, A.M. Pharmacological consequences of oxidative stress in ocular tissues. Mutat. Res. 2005, 579, 22-36.
4. Vegh, M.J.; de Waard, M.C.; van der Pluijm, I.; Ridwan, Y.; Sassen, M.J.; van Nierop, P.; van der Schors, R.C.; Li, K.W.; Hoeijmakers, J.H.; Smit, A.B.; et al. Synaptic proteome changes in a DNA repair deficient ercc1 mouse model of accelerated aging. J. Proteome Res. 2012, 11, 1855-1867.
5. Cai, X.; McGinnis, J.F. Oxidative stress: The achilles' heel of neurodegenerative diseases of the retina. Front Biosci. 2012, 17, 1976-1995.
6. Jager, R.D.; Mieler, W.F.; Miller, J.W. Age-related macular degeneration. N. Engl. J. Med. 2008, 358, 2606-2617.
7. Durik, M.; Kavousi, M.; van der Pluijm, I.; Isaacs, A.; Cheng, C.; Verdonk, K.; Loot, A.E.; Oeseburg, H.; Bhaggoe, U.M.; Leijten, F.; et al. Nucleotide excision DNA repair is associated with age-related vascular dysfunction. Circulation 2012, 126, 468-478.
8. Khandhadia, S.; Lotery, A. Oxidation and age-related macular degeneration: Insights from molecular biology. Expert Rev. Mol. Med. 2010, 12, e34.
9. Shabalina, I.G.; Nedergaard, J. Mitochondrial ("mild") uncoupling and ROS production: Physiologically relevant or not? Biochem. Soc. Trans. 2011, 39, 1305-1309.
10. Harper, J.W.; Elledge, S.J. The DNA damage response: Ten years after. Mol. Cell. 2007, 28, 739-745.
11. Estaquier, J.; Vallette, F.; Vayssiere, J.L.; Mignotte, B. The mitochondrial pathways of apoptosis. Adv. Exp. Med. Biol. 2012, 942, 157-183.
12. Feher, J.; Kovacs, I.; Artico, M.; Cavallotti, C.; Papale, A.; Gabrieli, C. Mitochondrial alterations of retinal pigment epithelium in age-related macular degeneration. Neurobiol. Aging 2006, 27, 983-993.
13. Jarrett, S.G.; Lewin, A.S.; Boulton, M.E. The importance of mitochondria in age-related and inherited eye disorders. Ophthalmic Res. 2010, 44, 179-190.
14. Harman, D. Free radical theory of aging: An update: Increasing the functional life span. Ann. N. Y. Acad. Sci. 2006, 1067, 10-21.
15. Anderson, S.; Bankier, A.T.; Barrell, B.G.; de Bruijn, M.H.; Coulson, A.R.; Drouin, J.; Eperon, I.C.; Nierlich, D.P.; Roe, B.A.; Sanger, F.; et al. Sequence and organization of the human mitochondrial genome. Nature 1981, 290, 457-465.
16. Boesch, P.; Weber-Lotfi, F.; Ibrahim, N.; Tarasenko, V.; Cosset, A.; Paulus, F.; Lightowlers, R.N.; Dietrich, A. DNA repair in organelles: Pathways, organization, regulation, relevance in disease and aging. Biochim. Biophys. Acta 2011, 1813, 186-200.
17. Evans, M.D.; Dizdaroglu, M.; Cooke, M.S. Oxidative DNA damage and disease: Induction, repair and significance. Mutat. Res. 2004, 567, 1-61.
18. Nair, J.; Strand, S.; Frank, N.; Knauft, J.; Wesch, H.; Galle, P.R.; Bartsch, H. Apoptosis and age-dependant induction of nuclear and mitochondrial etheno-DNA adducts in Long-Evans Cinnamon (LEC) rats: Enhanced DNA damage by dietary curcumin upon copper accumulation. Carcinogenesis 2005, 26, 1307-1315.
19. Chalam, K.V.; Khetpal, V.; Rusovici, R.; Balaiya, S. A review: Role of ultraviolet radiation in age-related macular degeneration. Eye Contact Lens. 2011, 37, 225-232.
20. Zhang, H.; Maguire, D.J.; Zhang, M.; Zhang, L.; Okunieff, P. Elevated mitochondrial DNA copy number and POL-γ expression but decreased expression of TFAM in murine intestine following therapeutic dose irradiation. Adv. Exp. Med. Biol. 2011, 701, 201-206.
21. Bacman, S.R.; Williams, S.L.; Moraes, C.T. Intra-and inter-molecular recombination of mitochondrial DNA after in vivo induction of multiple double-strand breaks. Nucleic Acids Res. 2009, 37, 4218-4226.
22. Kazak, L.; Reyes, A.; Holt, I.J. Minimizing the damage: Repair pathways keep mitochondrial DNA intact. Nat. Rev. Mol. Cell Biol. 2012, 13, 659-671.
23. Rasmussen, A.K.; Rasmussen, L.J. Targeting of O6-MeG DNA methyltransferase (MGMT) to mitochondria protects against alkylation induced cell death. Mitochondrion 2005, 5, 411-417.
24. Waters, R.; Moustacchi, E. Dose dependence of the excision of ultraviolet-induced pyrimidine dimers from nuclear deoxyribonucleic acids of haploid and diploid Saccharomyces cerevisiae. J. Bacteriol. 1975, 121, 901-906.
25. LeDoux, S.P.; Wilson, G.L. Base excision repair of mitochondrial DNA damage in mammalian cells. Prog. Nucleic Acid Res. Mol. Biol. 2001, 68, 273-284.
26. De Souza-Pinto, N.C.; Mason, P.A.; Hashiguchi, K.; Weissman, L.; Tian, J.; Guay, D.; Lebel, M.; Stevnsner, T.V.; Rasmussen, L.J.; Bohr, V.A. Novel DNA mismatch-repair activity involving YB-1 in human mitochondria. DNA Repair 2009, 8, 704-719.
27. Bharati, S.; Krokan, H.E.; Kristiansen, L.; Otterlei, M.; Slupphaug, G. Human mitochondrial uracil-DNA glycosylase preform (UNG1) is processed to two forms one of which is resistant to inhibition by AP sites. Nucleic Acids Res. 1998, 26, 4953-4959.
28. Ruchko, M.V.; Gorodnya, O.M.; Zuleta, A.; Pastukh, V.M.; Gillespie, M.N. The DNA glycosylase Ogg1 defends against oxidant-induced mtDNA damage and apoptosis in pulmonary artery endothelial cells. Free Radic. Biol. Med. 2011, 50, 1107-1113.
29. Hu, J.; de Souza-Pinto, N.C.; Haraguchi, K.; Hogue, B.A.; Jaruga, P.; Greenberg, M.M.; Dizdaroglu, M.; Bohr, V.A. Repair of formamidopyrimidines in DNA involves different glycosylases: Role of the OGG1, NTH1, and NEIL1 enzymes. J. Biol. Chem. 2005, 280, 40544-40551.
30. Stierum, R.H.; Dianov, G.L.; Bohr, V.A. Single-nucleotide patch base excision repair of uracil in DNA by mitochondrial protein extracts. Nucleic Acids Res. 1999, 27, 3712-3719.
31. Akbari, M.; Visnes, T.; Krokan, H.E.; Otterlei, M. Mitochondrial base excision repair of uracil and AP sites takes place by single-nucleotide insertion and long-patch DNA synthesis. DNA Repair 2008, 7, 605-616.
32. Liu, P.; Qian, L.; Sung, J.-S.; de Souza-Pinto, N.C.; Zheng, L.; Bogenhagen, D.F.; Bohr, V.A.; Wilson, D.M.; Shen, B.; Demple, B. Removal of oxidative DNA damage via FEN1-dependent long-patch base excision repair in human cell mitochondria. Mol. Cell. Biol. 2008, 28, 4975-4987.
33. Boesch, P.; Ibrahim, N.; Dietrich, A.; Lightowlers, R.N. Membrane association of mitochondrial DNA facilitates base excision repair in mammalian mitochondria. Nucleic Acids Res. 2010, 38, 1478-1488.
34. Kalifa, L.; Beutner, G.; Phadnis, N.; Sheu, S.-S.; Sia, E.A. Evidence for a role of FEN1 in maintaining mitochondrial DNA integrity. DNA Repair 2009, 8, 1242-1249.
35. Copeland, W.C.; Longley, M.J. DNA2 resolves expanding flap in mitochondrial base excision repair. Mol. Cell 2008, 32, 457-458.
36. Ralph, S.J.; Rodriguez-Enríquez, S.; Neuzil, J.; Saavedra, E.; Moreno-Sanchez, R. The causes of cancer revisited: "Mitochondrial malignancy" and ROS-induced oncogenic transformation-why mitochondria are targets for cancer therapy. Mol. Asp. Med. 2010, 31, 145-170.
37. Mason, P.A.; Matheson, E.C.; Hall, A.G.; Lightowlers, R.N. Mismatch repair activity in mammalian mitochondria. Nucleic Acids Res. 2003, 31, 1052-1058.
38. Kraytsberg, Y.; Schwartz, M.; Brown, T.A.; Ebralidse, K.; Kunz, W.S.; Clayton, D.A.; Vissing, J.; Khrapko, K. Recombination of human mitochondrial DNA. Science 2004, 304, 981
39. Sage, J.M.; Gildemeister, O.S.; Knight, K.L. Discovery of a novel function for human Rad51: Maintenance of the mitochondrial genome. J. Biol. Chem. 2010, 285, 18984-18990.
40. Lakshmipathy, U.; Campbell, C. Double strand break rejoining by mammalian mitochondrial extracts. Nucleic Acids Res. 1999, 27, 1198-1204.
41. Liu, P.; Demple, B. DNA repair in mammalian mitochondria: Much more than we thought? Environ. Mol. Mutagen. 2010, 51, 417-426.
42. Wallace, D.C. Mitochondrial diseases in man and mouse. Science 1999, 283, 1482-1488.
43. Cui, H.; Kong, Y.; Zhang, H. Oxidative stress, mitochondrial dysfunction, and aging. J. Signal Transduct. 2012, 2012, doi:10.1155/2012/646354.
44. Poe, B.G.; Navratil, M.; Arriaga, E.A. Absolute quantitation of a heteroplasmic mitochondrial DNA deletion using a multiplex three-primer real-time PCR assay. Anal. Biochem. 2007, 362, 193-200.
45. Tatuch, Y.; Christodoulou, J.; Feigenbaum, A.; Clarke, J.T.; Wherret, J.; Smith, C.; Rudd, N.; Petrova-Benedict, R.; Robinson, B.H. Heteroplasmic mtDNA mutation (T-G) at 8993 can cause Leigh disease when the percentage of abnormal mtDNA is high. Am. J. Hum. Genet. 1992, 50, 852-858.
46. Chinnery, P.F.; Zwijnenburg, P.J.; Walker, M.; Howell, N.; Taylor, R.W.; Lightowlers, R.N.; Bindoff, L.; Turnbull, D.M. Nonrandom tissue distribution of mutant mtDNA. Am. J. Med. Genet. 1999, 85, 498-501.
47. Jarrett, S.G.; Lin, H.; Godley, B.F.; Boulton, M.E. Mitochondrial DNA damage and its potential role in retinal degeneration. Prog. Retin. Eye Res. 2008, 27, 596-607.
48. Pitceathly, R.D.; Rahman, S.; Hanna, M.G. Single deletions in mitochondrial DNA-Molecular mechanisms and disease phenotypes in clinical practice. Neuromuscul. Disord. 2012, 22, 577-586.
49. Barreau, E.; Brossas, J.Y.; Courtois, Y.; Treton, J.A. Accumulation of mitochondrial DNA deletions in human retina during aging. Invest. Ophthalmol. Vis. Sci. 1996, 37, 384-391.
50. Wang, A.L.; Lukas, T.J.; Yuan, M.; Neufeld, A.H. Increased mitochondrial DNA damage and down-regulation of DNA repair enzymes in aged rodent retinal pigment epithelium and choroid. Mol. Vis. 2008, 14, 644-651.
51. Ballinger, S.W.; van Houten, B.; Jin, G.F.; Conklin, C.A.; Godley, B.F. Hydrogen peroxide causes significant mitochondrial DNA damage in human RPE cells. Exp. Eye Res. 1999, 68, 765-772.
52. Jarrett, S.G.; Boulton, M.E. Antioxidant up-regulation and increased nuclear DNA protection play key roles in adaptation to oxidative stress in epithelial cells. Free Radic. Biol. Med. 2005, 38, 1382-1391.
53. Jarrett, S.G.; Boulton, M.E. Poly(ADP-ribose) polymerase offers protection against oxidative and alkylation damage to the nuclear and mitochondrial genomes of the retinal pigment epithelium. Ophthalmic Res. 2007, 39, 213-223.
54. Godley, B.F.; Shamsi, F.A.; Liang, F.Q.; Jarrett, S.G.; Davies, S.; Boulton, M.J. Blue light induces mitochondrial DNA damage and free radical production in epithelial cells. Biol. Chem. 2005, 280, 21061-21066.
55. Liang, F.Q.; Godley, B.F. Oxidative stress-induced mitochondrial DNA damage in human retinal pigment epithelial cells: A possible mechanism for RPE aging and age-related macular degeneration. Exp. Eye Res. 2003, 76, 397-403.
56. Kenney, M.C.; Atilano, S.R.; Boyer, D.; Chwa, M.; Chak, G.; Chinichian, S.; Coskun, P.; Wallace, D.C.; Nesburn, A.B.; Udar, N.S. Characterization of retinal and blood mitochondrial DNA from age-related macular degeneration patients. Invest. Ophthalmol. Vis. Sci. 2010, 51, 4289-4297.
57. Udar, N.; Atilano, S.R.; Memarzadeh, M.; Boyer, D.S.; Chwa, M.; Lu, S.; Maguen, B.; Langberg, J.; Coskun, P.; Wallace, D.C.; et al. Mitochondrial DNA haplogroups associated with age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2009, 50, 2966-2974.
58. Karunadharma, P.P.; Nordgaard, C. L; Olsen, T.W.; Ferrington, D.A. Mitochondrial DNA damage as a potential mechanism for age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2010, 51, 5470-5479.
59. Lin, H.; Xu, H.; Liang, F.Q.; Liang, H.; Gupta, P.; Havey, A.N.; Boulton, M.E.; Godley, B.F. Mitochondrial DNA damage and repair in RPE associated with aging and age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2011, 52, 3521-3529.
60. Park, M.J.; Park, J.H.; Hahm, S.H.; Ko, S.I.; Lee, Y.R.; Chung, J.H.; Sohn, S.Y.; Cho, Y.; Kang, L.W.; Han, Y.S. Repair activities of human 8-oxoguanine DNA glycosylase are stimulated by the interaction with human checkpoint sensor Rad9-Rad1-Hus1 complex. DNA Repair 2009, 8, 1190-1200.
61. Garinis, G.A.; van der Horst, G.T.; Vijg, J.; Hoeijmakers, J.H. DNA damage and ageing: New-age ideas for an age-old problem. Nat. Cell Biol. 2008, 10, 1241-1247.
62. Dunn, K.C.; Aotaki-Keen, A.E.; Putkey, F.R.; Hjelmeland, L.M. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp. Eye Res. 1996, 62, 155-169.
63. Kalariya, N.M.; Ramana, K.V.; Srivastava, S.K.; van Kuijk, F.J. Genotoxic effects of carotenoid breakdown products in human retinal pigment epithelial cells. Curr. Eye Res. 2009, 3, 737-747.
64. Delaney, S.; Jarem, D.A.; Volle, C.B.; Yennie, C.J. Chemical and biological consequences of oxidatively damaged guanine in DNA. Free Radic. Res. 2012, 46, 420-441.
65. Beard, W.A.; Batra, V.K.; Wilson, S.H. DNA polymerase structure-based insight on the mutagenic properties of 8-oxoguanine. Mutat. Res. 2010, 703, 18-23.
66. Synowiec, E.; Blasiak, J.; Zaras, M.; Szaflik, J.; Szaflik, J.P. Association between polymorphisms of the DNA base excision repair genes MUTYH and hOGG1 and age-related macular degeneration. Exp. Eye Res. 2012, 98, 58-66.
67. Totan, Y.; Yagci, R.; Bardak, Y.; Ozyurt, H.; Kendir, F.; Yilmaz, G.; Sahin, S.; Sahin, T.U. Oxidative macromolecular damage in age-related macular degeneration. Curr. Eye Res. 2009, 34, 1089-1093.
68. Strunnikova, N.; Hilmer, S.; Flippin, J.; Robinson, M.; Hoffman, E.; Csaky, K.G. Differences in gene expression profiles in dermal fibroblasts from control and patients with age-related macular degeneration elicited by oxidative injury. Free Radic. Biol. Med. 2005, 39, 781-796.
69. Kaarniranta, K.; Salminen, A.; Haapasalo, A.; Soininen, H.; Hiltunen, M. Age-related macular degeneration (AMD): Alzheimer's disease in the eye? J. Alzheimers Dis. 2011, 24, 615-631.
70. Khan, J.C.; Thurlby, D.A.; Shahid, H.; Clayton, D.G.; Yates, J.R.; Bradley, M.; Moore, A.T.; Bird, A.C. Genetic Factors in AMD Study. Smoking and age related macular degeneration: The number of pack years of cigarette smoking is a major determinant of risk for both geographic atrophy and choroidal neovascularisation. Br. J. Ophthalmol. 2006, 90, 75-80.
71. Hecht, S.S. Progress and challenges in selected areas of tobacco carcinogenesis. Chem. Res. Toxicol. 2008, 21, 160-171.
72. Valavanidis, A.; Vlachogianni, T.; Fiotakis, K. Tobacco smoke: Involvement of reactive oxygen species and stable free radicals in mechanisms of oxidative damage, carcinogenesis and synergistic effects with other respirable particles. Int. J. Environ. Res. Public Health 2009, 6, 445-462.
73. Yang, Z.; Harrison, C.M.; Chuang, G.C.; Ballinger, S.W. The role of tobacco smoke induced mitochondrial damage in vascular dysfunction and atherosclerosis. Mutat. Res. 2007, 621, 61-74.
74. Fischer, F.; Hamann, A.; Osiewacz, H.D. Mitochondrial quality control: An integrated network of pathways. Trends Biochem. Sci. 2012, 37, 284-292.
75. Ballinger, S.W.; Patterson, C.; Yan, C.N.; Doan, R.; Burow, D.L.; Young, C.G.; Yakes, F.M.; van Houten, B.; Ballinger, C.A.; Freeman, B.A.; et al. Hydrogen peroxide-and peroxynitrite-induced mitochondrial DNA damage and dysfunction in vascular endothelial and smooth muscle cells. Circ. Res. 2000, 86, 960-966.
76. Knight-Lozano, C.A.; Young, C.G.; Burow, D.L.; Hu, Z.Y.; Uyeminami, D.; Pinkerton, K.E.; Ischiropoulos, H.; Ballinger, S.W. Cigarette smoke exposure and hypercholesterolemia increase mitochondrial damage in cardiovascular tissues. Circulation 2002, 105, 849-854.
77. Ballinger, S.W.; Patterson, C.; Knight-Lozano, C.A.; Burow, D.L.; Conklin, C.A.; Hu, Z.; Reuf, J.; Horaist, C.; Lebovitz, R.; Hunter, G.C.; et al. Mitochondrial integrity and function in atherogenesis. Circulation 2002, 106, 544-549.
78. Yang, Z.; Knight, C.A.; Mamerow, M.M.; Vickers, K.; Penn, A.; Postlethwait, E.M.; Ballinger, S.W. Prenatal environmental tobacco smoke exposure promotes adult atherogenesis and mitochondrial damage in apolipoprotein E-/-mice fed a chow diet. Circulation 2004, 110, 3715-3720.
79. Alexandrov, K.; Rojas, M.; Satarug, S. The critical DNA damage by benzo(a)pyrene in lung tissues of smokers and approaches to preventing its formation. Toxicol. Lett. 2010, 198, 63-68.
80. Blasiak, J.; Synowiec, E.; Salminen, A.; Kaarniranta, K. Genetic variability in dna repair proteins in age-related macular degeneration. Int. J. Mol. Sci. 2012, 13, 13378-13397.