Enhancing the efficacy of AREDS antioxidants in light-induced retinal degeneration

Molecular Vision

Volumn 23, Issue , 2017, Pages 718-739

  Wong, Paul ^a   Markey, M ^b   Rapp, C M ^c   Darrow, R M ^c   Ziesel, A ^a   Organisciak, D T ^c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WRIGHT STATE UNIVERSITY   (United States)

^c WRIGHT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; ASCORBIC ACID; BETA CAROTENE; CARNOSIC ACID; CUPRIC OXIDE; CYTOKINE; DNA; OPSIN; RETINA S ANTIGEN; RETINOL; RHODOPSIN; ROSMARINUS OFFICINALIS EXTRACT; URSOLIC ACID; ZINC; ZINC OXIDE; EYE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIETARY SUPPLEMENT; DNA DETERMINATION; DRUG EFFICACY; DRUG POTENTIATION; FEMALE; GENE EXPRESSION; GENE REPRESSION; GENETIC ANALYSIS; INFLAMMATION; INNATE IMMUNITY; LIGHT EXPOSURE; LIGHT INTENSITY; MALE; NONHUMAN; PHOTOOXIDATION; PRIORITY JOURNAL; RAT; RETINA CONE; RETINA DEGENERATION; RETINA ROD; SPRAGUE DAWLEY RAT; WESTERN BLOTTING; WHITE LIGHT; ANIMAL; CELL SURVIVAL; EXPERIMENTAL RADIATION INJURY; LIGHT; METABOLISM; PATHOLOGY; PHYSIOLOGY; PRECLINICAL STUDY; RADIATION RESPONSE; RETINA;

ANIMALS; ANTIOXIDANTS; BLOTTING, WESTERN; CELL SURVIVAL; DIETARY SUPPLEMENTS; DRUG EVALUATION, PRECLINICAL; EYE PROTEINS; LIGHT; MALE; RADIATION INJURIES, EXPERIMENTAL; RATS; RATS, SPRAGUE-DAWLEY; RETINA; RETINAL DEGENERATION; RHODOPSIN;

EID: 85032020710     PISSN: None     EISSN: 10900535     Source Type: Journal    
DOI: None     Document Type: Article

References (73)

1. Eye Disease Case-Control Study Group. Risk factors for neovascular age-related macular degeneration. Arch Ophthalmol 1992; 110:1701-8. [PMID: 1281403].
2. Zarbin M, Sunness JS. Dry age-related macular degeneration and age-related macular degeneration pathogenesis. In: Levin LA, Albert DM, editors. Ocular Disease: Mechanisms and Management. London: Saunders Elsevier; 2010. p. 527–535.
3. Lederer DE, Cousins SW, Csaky KG. Neovascular age-related macular degeneration. In: Levin LA, Albert DM, editors. Ocular Disease: Mechanisms and Management. London: Saunders Elsevier; 2010. p. 536–543.
4. Seddon JM, Ajani UA, Sperduto RD, Hiller R, Blair N, Burton TC, Farber MD, Gragoudas ES, Haller J, Miller DT, Yannuzzi LA, Willett W. Eye Disease Case-Control Study Group. Dietary carotenoids, vitamin A, C, and E, and advanced age-related macular degeneration. JAMA 1994; 272:1413-20. [PMID: 7933422].
5. Berrow EJ, Bartlett HE, Eperjesi F, Gibson JM. Risk factors for age-related macular degeneration. European Ophthalmic Rev 2011; 5:143-53.
6. Age-Related Eye Disease Study Research Group. A randomized, placebo-controlled, clinical trial of high-dose supplementation with vitamins C and E, beta carotene and zinc for age related macular degeneration. AREDS Report 8. Arch Ophthalmol 2001; 119:1417-36. [PMID: 11594942].
7. McGwin G, Xei A, Owsley C. The use of cholesterol-lowering medications and age-related macular degeneration. Ophthalmology 2005; 112:488-94. [PMID: 15745779].
8. Wilson HL, Schwartz DM, Bhatt HRF, McCulloch CE, Duncan JL. Statin and aspirin therapy are associated with decreased rates of choridal neovascularization among patients with age-related macular degeneration. Am J Ophthalmol 2004; 137:615-24. [PMID: 15059698].
9. Crabb JW, Miyagi M, Gu X, Shadrach K, West KA, Sakaguchi H, Kamei M, Hasan A, Yan L, Rayborn ME, Solomon RG, Hollyfield JG. Drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc Natl Acad Sci USA 2002; 99:14682-7. [PMID: 12391305].
10. Gu X, Meer SG, Miyagi M, Rayborn ME, Hollyfield JG, Crabb JW, Salomon RG. Carboxyethylpyrrole protein adducts and autoantibodies, biomarkers for age-related macular degeneration. J Biol Chem 2003; 278:42027-35. [PMID: 12923198].
11. Klein RJ, Zeiss C, Chew EY, Tsai J-Y, Sackler RS, Haynes C, Henning AK, SanGiovanni JP, Mane SM, Mayne ST, Bracken MB, Ferris FL, Ott J, Barnstable C, Hoh J. Complement factor H polymorphism in age-related macular degeneration. Science 2005; 308:385-9. [PMID: 15761122].
12. Donoso LA, Kim D, Frost A, Callahan A, Hageman G. The role of inflammation in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 2006; 51:137-52. [PMID: 16500214].
13. Haines JL, Hauser MA, Schmidt S, Scott WK, Olsen LM, Gallins P, Spencer KL, Kwan SY, Noureddine M, Gilbert JR, Schnetz-Boutaud N, Agarwal A, Postel EA, Pericak-Vance MA. Complement factor H variant increases the risk of age-related macular degeneration. Science 2005; 308:419-21. [PMID: 15761120].
14. Edwards AO, Ritter R, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and age-related macular degeneration. Science 2005; 308:421-4. [PMID: 15761121].
15. Weismann D, Hartvigen K, Lauer N, Bennet KL, Scholl HPN, Charbel Issa P, Cano M, Brandstatter H, Tsimikas S, Skerka C, Superti-Fuga G, Handa JT, Zipfe PF, Witztum JL, Binder CJ. Complement factor H binds malondialdehyde epitopes and protects from oxidative stress. Nature 2011; 478:76-81. [PMID: 21979047].
16. Blom AM, Kask L, Ramesh B, Hillarp A. Effect of zinc on factor I cofactor activity of C4b-binding protein and factor H. Arch Biochem Biophys 2003; 418:108-18. [PMID: 14522582].
17. Donoso LA, Vrabec T, Kuivaniemi H. The role of complement factor H in age-related macular degeneration: a review. Surv Ophthalmol 2010; 55:227-46. [PMID: 20385334].
18. Age Related Eye Disease Study 2 Research Group. Lutein + zeaxanthin and omega-3 fatty acids for age-related macular degeneration; the Age-Related Eye Disease Study 2 (AREDS2) randomized clinical trial. JAMA 2013; 309:2005-15. [PMID: 23644932].
19. Chew EY. Nutrition effects on ocular diseases in the aging eye. Invest Ophthalmol Vis Sci 2013; 54:ORSF42-7.
20. Seddon JM. Genetic and environmental underpinnings to age-related ocular diseases. Invest Ophthalmol Vis Sci 2013; 54:ORSF28-30.
21. Collier RJ, Wang Y, Smith S, Martin E, Ornberg R, Rhoades K, Romano C. Complement deposition and microglial activation in the outer retina in light-induced retinopathy: inhibition by a 5-HT 1A agonist. Invest Ophthalmol Vis Sci 2011; 52:8108-16. [PMID: 21467172].
22. Rutar M, Natoli R, Kozulin P, Valter K, Gatenby P, Provis JM. Analysis of complement expression in light-induced retinal degeneration: Synthesis and deposition of C3 by microglia/macrophages is associated with focal photoreceptor degeneration. Invest Ophthalmol Vis Sci 2011; 52:5347-58. [PMID: 21571681].
23. Marc RE, Jones B, Watt C, Vazquez-Chona F, Vaughan DK, Organisciak DT. Extreme retinal remodeling triggered by light damage: implications for age related macular degeneration. Mol Vis 2008; 14:782-806. [PMID: 18483561].
24. Hollyfield JG, Boniha VL, Rayborn ME, Yang X, Shadrach KG, Lu L, Ufret RL, Salomon RG, Perez VL. Oxidative damage-induced inflammation initiates age-related macular degeneration. Nat Med 2008; 14:194-8. [PMID: 18223656].
25. Organisciak D, Wong P, Rapp C, Darrow R, Ziesel A, Rangarajan R, Lang J. Light-induced retinal degeneration is prevented by zinc, a component in the age-related eye disease study formulation. Photochem Photobiol 2012; 88:1396-407. [PMID: 22385127].
26. Organisciak DT, Darrow RM, Rapp CM, Smuts JP, Armstrong DW, Lang JC. Prevention of retinal light damage by zinc oxide combined with rosemary extract. Mol Vis 2013; 19:1433-45. [PMID: 23825923].
27. Kowluru RA, Kanwar M, Chan P-S, Zhang JP. Inhibition of retinopathy and retinal metabolic abnormalities in diabetic rats with AREDS-based micronutrients. Arch Ophthalmol 2008; 126:1266-72. [PMID: 18779489].
28. Kowluru RA, Zhong Q. beyond AREDS: is there a place for antioxidant therapy in the prevention/treatment of eye disease? Invest Ophthalmol Vis Sci 2011; 52:8665-71. [PMID: 22065212].
29. Komeima K, Rogers BS, Lu L, Campochiaro PA. Antioxidants reduce cone cell death in a model of retinitis pigmentosa. Proc Natl Acad Sci USA 2006; 103:11300-5. [PMID: 16849425].
30. Ziess CJ. Animals as models of age-related macular degeneration: an imperfect measure of the truth. Vet Pathol 2011; 47:396-413. [PMID: 20382825].
31. Organisciak D, Vaughan D. Retinal light damage: mechanisms and protection. Prog Retin Eye Res 2010; 29:113-34. [PMID: 19951742].
32. Bedolla DE, Torre V. A component of retinal light adaptation mediated by the thyroid hormone cascade. PLoS One 2011; 6:e26334-[PMID: 22039463].
33. Liu Y, Fu L, Chen D-G, Deeb SS. Identification of novel retinal target genes of thyroid hormone in the human WERI cells by expression microarray analysis. Vision Res 2007; 47:2314-26. [PMID: 17655910].
34. Sharanjeet-Kaur. Dickinson CM, O’Donoghue E, Murray IJ. (1997) Spectral sensitivity in patients with dysthyroid eye disease. Ophthalmic Physiol Opt 1997; 17:232-8. [PMID: 9196665].
35. Feng Y, Wang Y, Li L, Wu L, Hoffmann S, Gretz N, Hammes HP. Gene expression profiling of vasoregression in the retina–involvement of microglial cells. PLoS One 2011; 6:e16865-[PMID: 21379381].
36. Agudo M, Pérez-Marín MC, Lönngren U, Sobrado P, Conesa A, Canovas I, Salinas-Navarro M, Miralles-Imperial J, Hallbook F, Vidal-Sanz M. Time course profiling of the retinal transcriptome after optic nerve transection and optic nerve crush. Mol Vis 2008; 14:1050-63. [PMID: 18552980].
37. Vázquez-Chona F, Song BK, Geisert EE Jr. Temporal changes in gene expression after injury in the rat retina. Invest Ophthalmol Vis Sci 2004; 45:2737-46. [PMID: 15277499].
38. Vázquez-Chona FR, Lu L, Williams RW, Geisert EE. Genomic loci modulating the retinal transcriptome in wound healing. Gene Regul Syst Bio 2008; 1:327-48. [PMID: 19936100].
39. Lee NE, Park YJ, Chung IY, Seo SW, Park JM, Yoo JM, Song JK. Gene expression changes in a rat model of oxygen-induced retinopathy. Korean J Ophthalmol 2011; 25:42-7. [PMID: 21350694].
40. Ishikawa K, Yoshida S, Kadota K, Nakamura T, Niiro H, Arakawa S, Yoshida A, Akashi K, Ishibashi T. Gene expression profile of hyperoxic and hypoxic retinas in a mouse model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 2010; 51:4307-19. [PMID: 20220049].
41. Hossain MN, Sakemura R, Fujii M, Ayusawa D. G-protein gamma subunit GNG11 strongly regulates cellular senescence. Biochem Biophys Res Commun 2006; 351:645-50. [PMID: 17092487].
42. Zhang Y. Smuts JP, Dodbiba E, Rangarajan R, Lang JC, Armstrong DW. Degradation study of carnosic acid, rosemarinic acid and rosemary extract (Rosmarinus officinalis L.) assessed using HPLC. J Agric Food Chem 2012; 60:9305-14. [PMID: 22881034].
43. Haruta M, Bush RA, Kjellstrom S, Vijayasarathy C, Zeng Y, Le Y-Z, Sieving P. Depleting Rac1 in mouse photoreceptors protects them from photo-oxidative stress without affecting their structure or function. Proc Natl Acad Sci USA 2009; 106:9397-402. [PMID: 19470639].
44. Belmonte MA, Santos MF, Kihara AH, Yan CYI, Hamassaki DA. Light-induced photoreceptor degeneration in the mouse involves activation of the small GTPase Rac1. Invest Ophthalmol Vis Sci 2006; 47:1193-200. [PMID: 16505058].
45. Winkler BS. The electroretinogram of the isolated rat retina. Vision Res 1972; 12:1183-98. [PMID: 5043568].
46. Organisciak D, Darrow R, Gu X, Barsalou L, Crabb JW. Genetic, age and light-mediated effects on crystallin protein expression in the retina. Photochem Photobiol 2006; 82:1088-96. [PMID: 16602829].
47. Mandal MNA, Moiseyev GP, Elliott MH, Kasus-Jacobi A, Li X, Chen H, Zheng L, Nikolaeva O, Floyd RA, Ma J-X, Anderson RE. α-phenyl-N-tert-butylnitrone (PBN) prevents light-induced degeneration of the retina by inhibiting RPE65 protein isomerohydrolase activity. J Biol Chem 2011; 286:32491-501. [PMID: 21785167].
48. Carvalho BS, Irizarry RA. A Framework for oligonucleotide microarray preprocessing. Bioinformatics 2010; 26:2363-7. [PMID: 20688976].
49. Smyth GK. Limma: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions using R and Bioconductor. Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W. editors, Springer, New York; 2005. p. 397–420.
50. Emig D, Salomonis N, Baumbach J, Lengauer T, Conklin BR, Albrecht M. AltAnalyze and DomainGraph: analyzing and visualizing exon expression data. Nucleic Acids Res 2010; 38:W755-62-.
51. Ng L, Hurley JB, Dierks B, Srinivas M, Salto C, Vennstrom B, Reh TA, Forrest D. A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat Genet 2001; 27:94-8. [PMID: 11138006].
52. Iwagawa T, Tanaka Y, Iida A, Itoh T, Watanabe S. Enhancer/promoter activities of the long/middle wavelength-sensitive opsins of vertebrates mediated by thyroid hormone receptor β2 and COUP-TFII. PLoS One 2013;8-[PMID: 24058409].
53. Kroeze WK, Sheffler DJ, Roth BL. G-protein-coupled receptors at a glance. J Cell Sci 2003; 116:4867-9. [PMID: 14625380].
54. Sugawara T, Sieving PA, Bush RA. Quantitative relationship of the scotopic and photopic ERG to photoreceptor cell loss in light damaged rats. Exp Eye Res 2000; 70:693-705. [PMID: 10870528].
55. John SK, Smith JE, Aguirre GD, Milam AH. Loss of cone molecular markers in rhodopsin-mutant human retinas with retinitis pigmentosa. Mol Vis 2000; 6:204-15. [PMID: 11063754].
56. Zhu X, Li A, Brown B, Weiss ER, Osawa S, Craft CM. Mouse cone arrestin expression pattern: light induced translocation in cone photoreceptors. Mol Vis 2002; 8:462-71. [PMID: 12486395].
57. Broekhuyse RM, Tolhuizen EFJ, Janssen APM, Winkes HJ. Light induced shift and binding of S-antigen in retinal rods. Curr Eye Res 1985; 4:613-8. [PMID: 2410196].
58. Whelan JP, McGinnis JF. Light-dependent subcellular movement of photoreceptor proteins. J Neurosci Res 1988; 20:263-70. [PMID: 3172281].
59. Glaschke A, Weiland J, Del Turco D, Steiner M, Peichl L, Glosmann M. Thyroid hormone controls cone opsin expression in the retina of adult rodents. J Neurosci 2011; 31:4844-51. [PMID: 21451022].
60. Rezaie T, McKercher SR, Kosaka K, Seki M, Wheeler L, Viswanath V, Chun T, Joshi R, Valencia M, Sasaki S, Tozawa T, Satob T, Lipton SA. Protective effect of carnosic acid, a pro-electrophilic compound, in models of oxidative stress and light-induced retinal degeneration. Invest Ophthalmol Vis Sci 2012; 54:7847-54. [PMID: 23081978].
61. Prunty MC, Aung MH, Hanif AM, Allen RS, Chrenek MA, Boatright JH, Thule PM, Kundu K, Murthy N, Pardue MT. In vivo imaging of retinal oxidative stress using a reactive oxygen species-activated fluorescent probe. Invest Ophthalmol Vis Sci 2015; 56:5862-70. [PMID: 26348635].
62. Cherny VV, DeCoursey TE. pH-dependent inhibition of voltage-gated H+ currents in rat alveolar epithelial cells by Zn2+ and other divalent cations. J Gen Physiol 1999; 114:819-38. [PMID: 10578017].
63. Downes GB, Gautam N. The G protein subunit gene families. Genomics 1999; 15:544-52. [PMID: 10644457].
64. Rath MF, Bailey MJ, Kim JS, Coon SL, Klein DC, Møller M. Developmental and daily expression of the Pax4 and Pax6 homeobox genes in the rat retina: localization of Pax4 in photoreceptor cells. J Neurochem 2009; 108:285-94. [PMID: 19012751].
65. Smith SB, Ee HC, Conners JR, German M. Paired-homeodomain transcription factor PAX4 acts as a transcriptional repressor in early pancreatic development. Mol Cell Biol 1999; 19:8272-80. [PMID: 10567552].
66. Petersen HV, Jørgensen MC, Andersen FG, Jensen J, Nielsen TF, Jørgensen R, Madsen OD, Serup P. Pax4 represses pancreatic glucagon gene expression. Mol Cell Biol Res Commun 2000; 3:249-54. [PMID: 10891400].
67. Marquardt T, Ashery-Padan R, Andrejewski N, Scardigli R, Guillemot F, Gruss P. Pax6 is required for the multipotent state of retinal progenitor cells. Cell 2001; 105:43-55. [PMID: 11301001].
68. Wong P, Organisciak DT, Ziesel AC, Chrenek MA, Patterson ML. Circadian effects on Retinal Light Damage. In The Retina and Circadian Rhythms. Eds. G Tosini, PM Iuvone, DG McMahon, SP Collin. Springer Science+Business Media New York; 2014. p. 131–170.
69. Nir I, Harrison JM, Haque R, Low MJ, Grandy DK, Rubinstein M, Iuvone PM. Dysfunctional light-evoked regulation of cAMP in photoreceptors and abnormal retinal adaptation in mice lacking dopamine D4 receptors. J Neurosci 2002; 22:2063-73. [PMID: 11896146].
70. Jackson CR, Chaurasia SS, Zhou H, Haque R, Storm DR, Iuvone PM. Essential roles of dopamine D4 receptors and the type 1 adenylyl cyclase in photic control of cyclic AMP in photoreceptor cells. J Neurochem 2009; 109:148-57. [PMID: 19166506].
71. Jackson CR, Chaurasia SS, Hwang CK, Iuvone PM. Dopamine D4 receptor activation controls circadian timing of the adenylyl cyclase 1/cyclic AMP signaling system in mouse retina. Eur J Neurosci 2011; 34:57-64. [PMID: 21676039].
72. Wenzel A, Grimm C, Marti A, Kueng-Hitz N, Hafezi F, Niemeyer G, Remé CE. c-fos controls the “private pathway” of light-induced apoptosis of retinal photoreceptors. J Neurosci 2000; 20:81-8. [PMID: 10627584].
73. Elachouri G, Lee-Rivera I, Clerin E, Argentini M, Fridich R, Blond F, Ferracane V, Yang Y, Raffelsberger W, Wan J, Bennett J, Sahel J-A, Zack DJ, Leveillard T. Thioredoxin rod-derived cone viability factor protects against photo-oxidative retinal damage. Free Radic Biol Med 2015; 81:22-9. [PMID: 25596499].