Idebenone Prevents Oxidative Stress, Cell Death and Senescence of Retinal Pigment Epithelium Cells by Stabilizing BAX/Bcl-2 Ratio

Ophthalmologica

Volumn 234, Issue 2, 2015, Pages 73-82

  Arend, Nicole ^a   Wertheimer, Christian ^a   Laubichler, Peter ^a   Wolf, Armin ^a   Kampik, Anselm ^a   Kernt, Marcus ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Age related macular degeneration; Apoptosis; Cell death; Oxidative stress; Retinal pigment epithelium cells

Indexed keywords

BETA GALACTOSIDASE; DNA FRAGMENT; HISTONE; HYDROGEN PEROXIDE; IDEBENONE; MESSENGER RNA; OXIDOREDUCTASE; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; ANTIOXIDANT; BAX PROTEIN, HUMAN; BCL2 PROTEIN, HUMAN; OXIDIZING AGENT; UBIQUINONE;

ARTICLE; CELL AGING; CELL DEATH; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; OXIDATIVE STRESS; PIGMENT EPITHELIUM; PROTEIN EXPRESSION; ANALOGS AND DERIVATIVES; CELL CULTURE; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; RETINAL PIGMENT EPITHELIUM; WESTERN BLOTTING;

ANTIOXIDANTS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CELL AGING; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; HUMANS; HYDROGEN PEROXIDE; OXIDANTS; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; RETINAL PIGMENT EPITHELIUM; RNA, MESSENGER; UBIQUINONE;

EID: 84942197119     PISSN: 00303755     EISSN: 14230267     Source Type: Journal    
DOI: 10.1159/000381726     Document Type: Article

References (54)

1. Klein R, Peto T, Bird A, Vannewkirk MR: The epidemiology of age-related macular degeneration. Am J Ophthalmol 2004;137:486-495.
2. World Health Organization: Visual Impairment and Blindness. WHO, 2011.
3. Coleman HR, Chan CC, Ferris FL 3rd, Chew EY: Age-related macular degeneration. Lancet 2008;372:1835-1845.
4. Zarbin MA: Current concepts in the pathogenesis of age-related macular degeneration. Arch Ophthalmol 2004;122:598-614.
5. Wang Y, Shen D, Wang VM, Yu CR, Wang RX, Tuo J, Chan CC: Enhanced apoptosis in retinal pigment epithelium under inflammatory stimuli and oxidative stress. Apoptosis 2012;17:1144-1155.
6. Nilsson SE, Sundelin SP, Wihlmark U, Brunk UT: Aging of cultured retinal pigment epithelial cells: oxidative reactions, lipofuscin formation and blue light damage. Doc Ophthalmol 2003;106:13-16.
7. Bazan NG, Calandria JM, Serhan CN: Rescue and repair during photoreceptor cell renewal mediated by docosahexaenoic acid-derived neuroprotectin D1. J Lipid Res 2010;51:2018-2031.
8. 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.
9. Kansagara D, Gleitsmann K, Gillingham M, Freeman M, Quinones A: Nutritional Supplements for Age-Related Macular Degeneration: A Systematic Review. Washington, Department of Veterans Affairs, 2012.
10. Lynch DR, Perlman SL, Meier T: A phase 3, double-blind, placebo-controlled trial of idebenone in Friedreich ataxia. Arch Neurol 2010;67:941-947.
11. Mancuso M, Orsucci D, Choub A, Siciliano G: Current and emerging treatment options in the management of Friedreich ataxia. Neuropsychiatr Dis Treat 2010;6:491-499.
12. Klopstock T, Yu-Wai-Man P, Dimitriadis K, Rouleau J, Heck S, Bailie M, Atawan A, Chattopadhyay S, Schubert M, Garip A, Kernt M, Petraki D, Rummey C, Leinonen M, Metz G, Griffiths PG, Meier T, Chinnery PF: A randomized placebo-controlled trial of idebenone in Leber's hereditary optic neuropathy. Brain 2011;134(Pt 9):2677-2686.
13. Gerhardt E, Graber S, Szego EM, Moisoi N, Martins LM, Outeiro TF, Kermer P: Idebenone and resveratrol extend lifespan and improve motor function of HtrA2 knockout mice. PLoS One 2011;6:e28855.
14. Palumbo M, Russo A, Cardile V, Renis M, Paolino D, Puglisi G, Fresta M: Improved antioxidant effect of idebenone-loaded polyethyl-2-cyanoacrylate nanocapsules tested on human fibroblasts. Pharm Res 2002;19:71-78.
15. Becker C, Bray-French K, Drewe J: Pharmacokinetic evaluation of idebenone. Expert Opin Drug Metab Toxicol 2010;6:1437-1444.
16. Kernt M, Neubauer AS, Ulbig MW, Kampik A, Welge-Lussen U: In vitro safety of intravitreal moxifloxacin for endophthalmitis treatment. J Cataract Refract Surg 2008;34:480-488.
17. Haefeli RH, Erb M, Gemperli AC, Robay D, Courdier Fruh I, Anklin C, Dallmann R, Gueven N: NQO1-dependent redox cycling of idebenone: effects on cellular redox potential and energy levels. PLoS One 2011;6:e17963.
18. Rego AC, Santos MS, Oliveira CR: Influence of the antioxidants vitamin E and idebenone on retinal cell injury mediated by chemical ischemia, hypoglycemia, or oxidative stress. Free Radic Biol Med 1999;26:1405-1417.
19. Kernt M, Arend N, Buerger A, Mann T, Haritoglou C, Ulbig MW, Kampik A, Hirneiss C: Idebenone prevents human optic nerve head astrocytes from oxidative stress, apoptosis, and senescence by stabilizing BAX/Bcl-2 ratio. J Glaucoma 2013;22:404-412.
20. Ali SA, Aly HF, Faddah LM, Zaidi ZF: Dietary supplementation of some antioxidants against hypoxia. World J Gastroenterol 2012;18:6379-6386.
21. Abdel Baky NA, Zaidi ZF, Fatani AJ, Sayed-Ahmed MM, Yaqub H: Nitric oxide pros and cons: the role of L-arginine, a nitric oxide precursor, and idebenone, a coenzyme-Q analogue in ameliorating cerebral hypoxia in rat. Brain Res Bull 2010;83:49-56.
22. Shivaram KN, Winklhofer-Roob BM, Straka MS, Devereaux MW, Everson G, Mierau GW, Sokol RJ: The effect of idebenone, a coenzyme Q analogue, on hydrophobic bile acid toxicity to isolated rat hepatocytes and hepatic mitochondria. Free Radic Biol Med 1998;25:480-492.
23. Mosmann T: Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63.
24. Kernt M, Neubauer AS, Liegl R, Eibl KH, Alge CS, Lackerbauer CA, Ulbig MW, Kampik A: Cytoprotective effects of a blue light-filtering intraocular lens on human retinal pigment epithelium by reducing phototoxic effects on vascular endothelial growth factor-alpha, Bax, and Bcl-2 expression. J Cataract Refract Surg 2009;35:354-362.
25. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O, et al: A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 1995;92:9363-9367.
26. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M: Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000;404:787-790.
27. Kernt M, Hirneiss C, Neubauer AS, Ulbig MW, Kampik A: Coenzyme Q10 prevents human lens epithelial cells from light-induced apoptotic cell death by reducing oxidative stress and stabilizing BAX/Bcl-2 ratio. Acta Ophthalmol 2010;88:e78-e86.
28. Kernt M, Liegl RG, Rueping J, Neubauer AS, Haritoglou C, Lackerbauer CA, Eibl KH, Ulbig MW, Kampik A: Sorafenib protects human optic nerve head astrocytes from light-induced overexpression of vascular endothelial growth factor, platelet-derived growth factor, and placenta growth factor. Growth Factors 2010;28:211-220.
29. Levine AJ: p53, the cellular gatekeeper for growth and division. Cell 1997;88:323-331.
30. McKinnon SJ, Lehman DM, Kerrigan-Baumrind LA, Merges CA, Pease ME, Kerrigan DF, Ransom NL, Tahzib NG, Reitsamer HA, Levkovitch-Verbin H, Quigley HA, Zack DJ: Caspase activation and amyloid precursor protein cleavage in rat ocular hypertension. Invest Ophthalmol Vis Sci 2002;43:1077-1087.
31. Hinton DR, He S, Lopez PF: Apoptosis in surgically excised choroidal neovascular membranes in age-related macular degeneration. Arch Ophthalmol 1998;116:203-209.
32. Shan H, Ji D, Barnard AR, Lipinski DM, You Q, Lee EJ, Kamalden TA, Sun X, MacLaren RE: AAV-mediated gene transfer of human X-linked inhibitor of apoptosis protects against oxidative cell death in human RPE cells. Invest Ophthalmol Vis Sci 2011;52:9591-9597.
33. Xu GZ, Li WW, Tso MO: Apoptosis in human retinal degenerations. Trans Am Ophthalmol Soc 1996;94:411-430, discussion 430-431.
34. Dunaief JL, Dentchev T, Ying GS, Milam AH: The role of apoptosis in age-related macular degeneration. Arch Ophthalmol 2002;120:1435-1442.
35. Faghiri Z, Bazan NG: PI3K/Akt and mTOR/p70S6K pathways mediate neuroprotectin D1-induced retinal pigment epithelial cell survival during oxidative stress-induced apoptosis. Exp Eye Res 2010;90:718-725.
36. Cao X, Liu M, Tuo J, Shen D, Chan CC: The effects of quercetin in cultured human RPE cells under oxidative stress and in Ccl2/Cx3cr1 double deficient mice. Exp Eye Res 2010;91:15-25.
37. Savory J, Rao JK, Huang Y, Letada PR, Herman MM: Age-related hippocampal changes in Bcl-2:Bax ratio, oxidative stress, redox-active iron and apoptosis associated with aluminum-induced neurodegeneration: increased susceptibility with aging. Neurotoxicology 1999;20:805-817.
38. Naderi J, Hung M, Pandey S: Oxidative stress-induced apoptosis in dividing fibroblasts involves activation of p38 MAP kinase and over-expression of Bax: resistance of quiescent cells to oxidative stress. Apoptosis 2003;8:91-100.
39. Chen J, Chu Y, Cao J, Yang Z, Guo X, Wang Z: T-2 toxin induces apoptosis, and selenium partly blocks, T-2 toxin induced apoptosis in chondrocytes through modulation of the Bax/Bcl-2 ratio. Food Chem Toxicol 2006;44:567-573.
40. Borner C: The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol Immunol 2003;39:615-647.
41. Lee JE, Kang JS, Shin IC, Lee SJ, Hyun DH, Lee KS, Koh HC: Fluazinam-induced apoptosis of SH-SY5Y cells is mediated by p53 and Bcl-2 family proteins. Neurotoxicology 2011;32:702-710.
42. Huang XR, Qi MX, Wang ZY, Chen Y: Inhibition effects of compound leech eye drops on apoptosis of lens epithelial cells and expressions of Bcl-2 and Bax genes in rats (in Chinese). Zhong Xi Yi Jie He Xue Bao 2007;5:681-685.
43. Singh M, Piekorz RP: Senescence-associated lysosomal α-L-fucosidase (SA-α-Fuc): a sensitive and more robust biomarker for cellular senescence beyond SA-β-Gal. Cell Cycle 2013;12:1996.
44. Ravelojaona V, Robert AM, Robert L: Expression of senescence-associated β-galactosidase (SA-β-Gal) by human skin fibroblasts, effect of advanced glycation end-products and fucose or rhamnose-rich polysaccharides. Arch Gerontol Geriatr 2009;48:151-154.
45. Sin HP, Liu DT, Lam DS: Lifestyle modification, nutritional and vitamins supplements for age-related macular degeneration. Acta Ophthalmol 2013;91:6-11.
46. Mordente A, Martorana GE, Minotti G, Giardina B: Antioxidant properties of 2,3-dime-thoxy-5-methyl-6-(10-hydroxydecyl)-1,4-benzoquinone (idebenone). Chem Res Toxicol 1998;11:54-63.
47. Ojano-Dirain CP, Antonelli PJ: Prevention of gentamicin-induced apoptosis with the mitochondria-targeted antioxidant mitoquinone. Laryngoscope 2012;122:2543-2548.
48. Sergi B, Fetoni AR, Paludetti G, Ferraresi A, Navarra P, Mordente A, Troiani D: Protective properties of idebenone in noise-induced hearing loss in the guinea pig. Neuroreport 2006;17:857-861.
49. Deigner HP, Haberkorn U, Kinscherf R: Apoptosis modulators in the therapy of neurodegenerative diseases. Expert Opin Investig Drugs 2000;9:747-764.
50. Yamazaki N, Take Y, Nagaoka A, Nagawa Y: Beneficial effect of idebenone (CV-2619) on cerebral ischemia-induced amnesia in rats. Jpn J Pharmacol 1984;36:349-356.
51. Al-Rasheed NM, Faddah LM, Mohamed AM, Abdel Baky NA, Mohammad RA: Potential impact of quercetin and idebenone against immuno-inflammatory and oxidative renal damage induced in rats by titanium dioxide nanoparticles toxicity. J Oleo Sci 2013;62:961-971.
52. Heitz FD, Erb M, Anklin C, Robay D, Pernet V, Gueven N: Idebenone protects against retinal damage and loss of vision in a mouse model of Leber's hereditary optic neuropathy. PLoS One 2012;7:e45182.
53. Klopstock T, Metz G, Yu-Wai-Man P, Buchner B, Gallenmuller C, Bailie M, Nwali N, Griffiths PG, von Livonius B, Reznicek L, Rouleau J, Coppard N, Meier T, Chinnery PF: Persistence of the treatment effect of idebenone in Leber's hereditary optic neuropathy. Brain 2013;136(Pt 2):e230.
54. Buyse GM, Van der Mieren G, Erb M, D'Hooge J, Herijgers P, Verbeken E, Jara A, Van Den Bergh A, Mertens L, Courdier-Fruh I, Barzaghi P, Meier T: Long-term blinded placebo-controlled study of SNT-MC17/idebenone in the dystrophin deficient mdx mouse: cardiac protection and improved exercise performance. Eur Heart J 2009;30:116-124.