Mitochondrial Oxidative stress in the retinal pigment epithelium leads to localized retinal degeneration

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 7, 2014, Pages 4613-4627

  Mao, Haoyu ^a   Seo, Soo Jung ^a   Biswal, Manas R ^a   Li, Hong ^a   Conners, Mandy ^a   Nandyala, Arathi ^a   Jones, Kyle ^a   Le, Yun Zheng ^b   Lewin, Alfred S ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

Manganese superoxide dismutase; Mouse model; Reactive oxygen species; Retinal degeneration; Retinal pigment epithelium

Indexed keywords

EXTRACELLULAR SUPEROXIDE DISMUTASE; MANGANESE SUPEROXIDE DISMUTASE; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOFLUORESCENCE IMAGING; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRORETINOGRAPHY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ANGIOGRAPHY; GENE DELETION; GENE EXPRESSION; GENETIC ANALYSIS; GENOTYPE; HISTOLOGY; HISTOPATHOLOGY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MITOCHONDRIAL DYNAMICS; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PIGMENT EPITHELIUM; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RETINA IMAGE; RETINA PIGMENT DEGENERATION; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY;

MANGANESE SUPEROXIDE DISMUTASE; MOUSE MODEL; REACTIVE OXYGEN SPECIES; RETINAL DEGENERATION; RETINAL PIGMENT EPITHELIUM;

ANIMALS; DISEASE MODELS, ANIMAL; DOXYCYCLINE; ELECTRORETINOGRAPHY; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLUORESCEIN ANGIOGRAPHY; GENE DELETION; GENE EXPRESSION; GEOGRAPHIC ATROPHY; INTEGRASES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MITOCHONDRIA; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; RETINAL PIGMENT EPITHELIUM; ROD CELL OUTER SEGMENT; SUPEROXIDE DISMUTASE; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 84905041061     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.14-14633     Document Type: Article

References (77)

1. Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest. 2005;115:500-508.
2. Beal MF. Aging, energy, and oxidative stress in neurodegenerative diseases. Ann Neurol. 1995;38:357-366.
3. Uchino Y, Kawakita T, Miyazawa M, et al. Oxidative stress induced inflammation initiates functional decline of tear production. PLoS One. 2012;7:45805.
4. Brennan LA, Kantorow M. Mitochondrial function and redox control in the aging eye: role of MsrA and other repair systems in cataract and macular degenerations. Exp Eye Res. 2009;88: 195-203.
5. Tezel G, Yang X, Luo C, et al. Oxidative stress and the regulation of complement activation in human glaucoma. Invest Ophthalmol Vis Sci. 2010;51:5071-5082.
6. Sacca SC, Pascotto A, Camicione P, Capris P, Izzotti A. Oxidative DNA damage in the human trabecular meshwork: clinical correlation in patients with primary open-angle glaucoma. Arch Ophthalmol. 2005;123:458-463.
7. Dong A, Xie B, Shen J, et al. Oxidative stress promotes ocular neovascularization. J Cell Physiol. 2009;219:544-552.
8. Barnett BP, Handa JT. Retinal microenvironment imbalance in dry age-related macular degeneration: a mini-review. Gerontology. 2013;59:297-306.
9. Zarbin MA. Current concepts in the pathogenesis of agerelated macular degeneration. Arch Ophthalmol. 2004;122: 598-614.
10. Cano M, Thimmalappula R, Fujihara M, et al. Cigarette smoking, oxidative stress, the anti-oxidant response through Nrf2 signaling, and age-related macular degeneration. Vision Res. 2010;50:652-664.
11. Seddon JM, Reynolds R, Maller J, Fagerness JA, Daly MJ, Rosner B. Prediction model for prevalence and incidence of advanced age-related macular degeneration based on genetic, demographic, and environmental variables. Invest Ophthalmol Vis Sci. 2009;50:2044-2053.
12. Tan JS, Mitchell P, Kifley A, Flood V, Smith W, Wang JJ. Smoking and the long-term incidence of age-related macular degeneration: the Blue Mountains Eye Study. Arch Ophthalmol. 2007; 125:1089-1095.
13. Tomany SC, Wang JJ, van Leeuwen R, et al. Risk factors for incident age-related macular degeneration: pooled findings from 3 continents. Ophthalmology. 2004;111:1280-1287.
14. Age-Related Eye Disease Study Research Group. The relationship of dietary carotenoid and vitamin A, E, and C intake with age-related macular degeneration in a case-control study: AREDS report No. 22. Arch Ophthalmol. 2007;125:1225-1232.
15. Hollyfield JG, Bonilha VL, Rayborn ME, et al. Oxidative damage-induced inflammation initiates age-related macular degeneration. Nat Med. 2008;14:194-198.
16. Decanini A, Nordgaard CL, Feng X, Ferrington DA, Olsen TW. Changes in select redox proteins of the retinal pigment epithelium in age-related macular degeneration. Am J Ophthalmol. 2007;143:607-615.
17. Cai J, Nelson KC, Wu M, Sternberg P Jr, Jones DP. Oxidative damage and protection of the RPE. Prog Retin Eye Res. 2000; 19:205-221.
18. Hageman GS, Luthert PJ, Victor Chong NH, Johnson LV, Anderson DH, Mullins RF. An integrated hypothesis that considers drusen as biomarkers of immune-mediated processes at the RPE-Bruch's membrane interface in aging and agerelated macular degeneration. Prog Retin Eye Res. 2001;20: 705-732.
19. Liang FQ, Godley BF. 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.
20. Crabb JW, Miyagi M, Gu X, et al. From the cover: drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc Natl Acad Sci U S A. 2002;99: 14682-14687.
21. Wang L, Clark ME, Crossman DK, et al. Abundant lipid and protein components of drusen. PLoS One. [serial online]. 2010;5:e10329. Available at: http://www.ncbi.nlm.nih.gov/ pmc/articles/PMC2859054/. Accessed June 25, 2014.
22. Holz FG, Strauss EC, Schmitz-Valckenberg S, van Lookeren Campagne M. Geographic atrophy: clinical features and potential therapeutic approaches. Ophthalmology. 2014;121: 1079-1091.
23. Kaarniranta K, Sinha D, Blasiak J, et al. Autophagy and heterophagy dysregulation leads to retinal pigment epithelium dysfunction and development of age-related macular degeneration. Autophagy. 2013;9:973-984.
24. Bergmann M, Schutt F, Holz FG, Kopitz J. Inhibition of the ATPdriven proton pump in RPE lysosomes by the major lipofuscin fluorophore A2-E may contribute to the pathogenesis of agerelated macular degeneration. FASEB J. 2004;18:562-564.
25. Finnemann SC, Leung LW, Rodriguez-Boulan E. The lipofuscin component A2E selectively inhibits phagolysosomal degradation of photoreceptor phospholipid by the retinal pigment epithelium. Proc Natl Acad Sci U S A. 2002;99:3842-3847.
26. Jarrett SG, Boulton ME. Consequences of oxidative stress in age-related macular degeneration. Mol Aspects Med. 2012;33: 399-417.
27. Brand MD. The sites and topology of mitochondrial superoxide production. Exp Gerontol. 2010;45:466-472.
28. Quinlan CL, Goncalves RL, Hey-Mogensen M, Yadava N, Bunik VI, Brand MD. The 2-oxoacid dehydrogenase complexes in mitochondria can produce superoxide/hydrogen peroxide at much higher rates than complex I. J Biol Chem. 2014;289: 8312-8325.
29. He Y, Ge J, Burke JM, Myers RL, Dong ZZ, Tombran-Tink J. Mitochondria impairment correlates with increased sensitivity of aging RPE cells to oxidative stress. J Ocul Biol Dis Inf. 2010; 3:92-108.
30. Nordgaard CL, Karunadharma PP, Feng X, Olsen TW, Ferrington DA. Mitochondrial proteomics of the retinal pigment epithelium at progressive stages of age-related macular degeneration. Invest Ophthalmol Vis Sci. 2008;49: 2848-2855.
31. Karunadharma PP, Nordgaard CL, Olsen TW, Ferrington DA. Mitochondrial DNA damage as a potential mechanism for agerelated macular degeneration. Invest Ophthalmol Vis Sci. 2010;51:5470-5479.
32. Kenney MC, Hertzog D, Chak G, et al. Mitochondrial DNA haplogroups confer differences in risk for age-related macular degeneration: a case control study. BMC Med Genet. [serial online]. 2013;14:4. Available at: http://www.ncbi.nlm.nih. gov/pmc/articles/PMC3566905/. Accessed June 25, 2014.
33. Rakoczy PE, Yu MJ, Nusinowitz S, Chang B, Heckenlively JR. Mouse models of age-related macular degeneration. Exp Eye Res. 2006;82:741-752.
34. Pennesi ME, Neuringer M, Courtney RJ. Animal models of age related macular degeneration. Mol Aspects Med. 2012;33:487-509.
35. Hunter JJ, Morgan JI, Merigan WH, Sliney DH, Sparrow JR, Williams DR. The susceptibility of the retina to photochemical damage from visible light. Prog Retin Eye Res. 2012;31:28-42.
36. Garland DL, Fernandez-Godino R, Kaur I, et al. Mouse genetics and proteomic analyses demonstrate a critical role for complement in a model of DHRD/ML, an inherited macular degeneration. Hum Mol Genet. 2014;23:52-68.
37. Nozaki M, Raisler BJ, Sakurai E, et al. Drusen complement components C3a and C5a promote choroidal neovascularization. Proc Natl Acad Sci U S A. 2006;103:2328-2333.
38. Radu RA, Hu J, Yuan Q, et al. Complement system dysregulation and inflammation in the retinal pigment epithelium of a mouse model for Stargardt macular degeneration. J Biol Chem. 2011;286:18593-18601.
39. Rohrer B, Long Q, Coughlin B, et al. A targeted inhibitor of the alternative complement pathway reduces angiogenesis in a mouse model of age-related macular degeneration. Invest Ophthalmol Vis Sci. 2009;50:3056-3064.
40. Kaneko H, Dridi S, Tarallo V, et al. DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature. 2011;471:325-330.
41. Kleinman ME, Yamada K, Takeda A, et al. Sequence-and targetindependent angiogenesis suppression by siRNA via TLR3. Nature. 2008;452:591-597.
42. Ufret-Vincenty RL, Aredo B, Liu X, et al. Transgenic mice expressing variants of complement factor H develop AMD-like retinal findings. Invest Ophthalmol Vis Sci. 2010;51:5878-5887.
43. Hadziahmetovic M, Dentchev T, Song Y, et al. Ceruloplasmin/ hephaestin knockout mice model morphologic and molecular features of AMD. Invest Ophthalmol Vis Sci. 2008;49:2728-2736.
44. Malek G, Johnson LV, Mace BE, et al. Apolipoprotein E allele-dependent pathogenesis: a model for age-related retinal degeneration. Proc Natl Acad Sci U S A. 2005;102:11900-11905.
45. Zhao C, Yasumura D, Li X, et al. mTOR-mediated dedifferentiation of the retinal pigment epithelium initiates photoreceptor degeneration in mice. J Clin Invest. 2011;121:369-383.
46. Hu P, Herrmann R, Bednar A, et al. Aryl hydrocarbon receptor deficiency causes dysregulated cellular matrix metabolism and age-related macular degeneration-like pathology. Proc Natl Acad Sci U S A. 2013;110:E4069-E4078. Available at: http:// www.pnas.org/content/110/43/E4069.long. Accessed June 25, 2014.
47. Imamura Y, Noda S, Hashizume K, et al. Drusen, choroidal neovascularization, and retinal pigment epithelium dysfunction in SOD1-deficient mice: a model of age-related macular degeneration. Proc Natl Acad Sci U S A. 2006;103:11282-11287.
48. Zhao Z, Chen Y, Wang J, et al. Age-related retinopathy in NRF2-deficient mice. PLoS One. [serial online]. 2011;6:e19456. Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/ PMC3084871/. Accessed June 25, 2014.
49. Justilien V, Pang JJ, Renganathan K, et al. SOD2 knockdown mouse model of early AMD. Invest Ophthalmol Vis Sci. 2007; 48:4407-4420.
50. Seo SJ, Krebs MP, Mao H, Jones K, Conners M, Lewin AS. Pathological consequences of long-term mitochondrial oxidative stress in the mouse retinal pigment epithelium. Exp Eye Res. 2012;101:60-71.
51. Thampi P, Rao HV, Mitter SK, et al. The 5HT(1a) receptor agonist 8-Oh DPAT induces protection from lipofuscin accumulation and oxidative stress in the retinal pigment epithelium. PLoS One. [serial online]. 2012;7:e34468. Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/ PMC3317995/. Accessed June 25, 2014.
52. Li Y, Huang TT, Carlson EJ, et al. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet. 1995;11:376-381.
53. Le YZ, Zheng W, Rao PC, et al. Inducible expression of cre recombinase in the retinal pigmented epithelium. Invest Ophthalmol Vis Sci. 2008;49:1248-1253.
54. Strassburger M, Bloch W, Sulyok S, et al. Heterozygous deficiency of manganese superoxide dismutase results in severe lipid peroxidation and spontaneous apoptosis in murine myocardium in vivo. Free Radic Biol Med. 2005;38: 1458-1470.
55. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227:680-685.
56. Komeima K, Usui S, Shen J, Rogers BS, Campochiaro PA. Blockade of neuronal nitric oxide synthase reduces cone cell death in a model of retinitis pigmentosa. Free Radic Biol Med. 2008;45:905-912.
57. Ethen CM, Reilly C, Feng X, Olsen TW, Ferrington DA. Agerelated macular degeneration and retinal protein modification by 4-hydroxy-2-nonenal. Invest Ophthalmol Vis Sci. 2007;48: 3469-3479.
58. Lois N, Owens SL, Coco R, Hopkins J, Fitzke FW, Bird AC. Fundus autofluorescence in patients with age-related macular degeneration and high risk of visual loss. Am J Ophthalmol. 2002;133:341-349.
59. Bindewald A, Bird AC, Dandekar SS, et al. Classification of fundus autofluorescence patterns in early age-related macular disease. Invest Ophthalmol Vis Sci. 2005;46:3309-3314.
60. Zhou J, Kim SR, Westlund BS, Sparrow JR. Complement activation by bisretinoid constituents of RPE lipofuscin. Invest Ophthalmol Vis Sci. 2009;50:1392-1399.
61. Mullins RF, Aptsiauri N, Hageman GS. Structure and composition of drusen associated with glomerulonephritis: implications for the role of complement activation in drusen biogenesis. Eye. 2001;15:390-395.
62. Johnson LV, Leitner WP, Staples MK, Anderson DH. Complement activation and inflammatory processes in drusen formation and age related macular degeneration. Exp Eye Res. 2001;73:887-896.
63. Ebrahimi KB, Fijalkowski N, Cano M, Handa JT. Decreased membrane complement regulators in the retinal pigmented epithelium contributes to age-related macular degeneration. J Pathol. 2013;229:729-742.
64. Fruttiger M. Development of the retinal vasculature. Angiogenesis. 2007;10:77-88.
65. Curcio CA, Presley JB, Millican CL, Medeiros NE. Basal deposits and drusen in eyes with age-related maculopathy: evidence for solid lipid particles. Exp Eye Res. 2005;80:761-775.
66. Boulton M, Docchio F, Dayhaw-Barker P, Ramponi R, Cubeddu R. Age-related changes in the morphology, absorption and fluorescence of melanosomes and lipofuscin granules of the retinal pigment epithelium. Vision Res. 1990;30:1291-1303.
67. Lindquist NG, Larsson BS, Stjernschantz J, Sjöquist B. Agerelated melanogenesis in the eye of mice, studied by microautoradiography of 3H-methimazole, a specific marker of melanin synthesis. Exp Eye Res. 1998;67:259-264.
68. Miquel J, Economos AC, Fleming J, Johnson J. Mitochondrial role in cell aging. Exp Gerontol. 1980;15:575-591.
69. Bratic A, Larsson NG. The role of mitochondria in aging. J Clin Invest. 2013;123:951-957.
70. McLeod DS, Grebe R, Bhutto I, Merges C, Baba T, Lutty GA. Relationship between RPE and choriocapillaris in age-related macular degeneration. Invest Ophthalmol Vis Sci. 2009;50: 4982-4991.
71. Nakazawa T, Matsubara A, Noda K, et al. Characterization of cytokine responses to retinal detachment in rats. Mol Vis. 2006;12:867-878.
72. Kanda A, Abecasis G, Swaroop A. Inflammation in the pathogenesis of age-related macular degeneration. Br J Ophthalmol. 2008;92:448-450.
73. Kauppinen A, Niskanen H, Suuronen T, Kinnunen K, Salminen A, Kaarniranta K. Oxidative stress activates NLRP3 inflammasomes in ARPE-19 cells: implications for age-related macular degeneration (AMD). Immunol Lett. 2012;147:29-33.
74. Danciger M, Matthes MT, Yasamura D, et al. A QTL on distal chromosome 3 that influences the severity of light-induced damage to mouse photoreceptors. Mamm Genome. 2000;11: 422-427.
75. Grimm C, Wenzel A, Hafezi F, Yu S, Redmond TM, Reme CE. Protection of Rpe65-deficient mice identifies rhodopsin as a mediator of light-induced retinal degeneration. Nat Genet. 2000;25:63-66.
76. Ding JD, Johnson LV, Herrmann R, et al. Anti-amyloid therapy protects against retinal pigmented epithelium damage and vision loss in a model of age-related macular degeneration. Proc Natl Acad Sci U S A. 2011;108:E279-E287. Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3136266/. Accessed June 25, 2014.
77. Le Y, Gagneten S, Tombaccini D, Bethke B, Sauer B. Nuclear targeting determinants of the phage P1 cre DNA recombinase. Nucleic Acids Res. 1999;27:4703-4709.