N-acetylcysteine amide (NACA) prevents retinal degeneration by up-regulating reduced glutathione production and reversing lipid peroxidation

American Journal of Pathology

Volumn 178, Issue 5, 2011, Pages 2032-2043

  Schimel, Andrew M ^a   Abraham, Linu ^b   Cox, Douglas ^a   Sene, Abdoulaye ^a   Kraus, Courtney ^a   Dace, Dru S ^a   Ercal, Nuran ^b   Apte, Rajendra S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MISSOURI UNIVERSITY OF SCIENCE AND TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE AMIDE; ACETYLCYSTEINE DERIVATIVE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; MALONALDEHYDE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; CELL DAMAGE; CELL DEATH; CELL NUCLEUS; CONTROLLED STUDY; DETOXIFICATION; ELECTRORETINOGRAPHY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO CULTURE; LIPID PEROXIDATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHOTORECEPTOR; PHOTOTOXICITY; PIGMENT CELL; PRIORITY JOURNAL; RETINA DEGENERATION; UPREGULATION; VISUAL IMPAIRMENT;

EID: 79959232837     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.01.036     Document Type: Article

References (77)

1. Marmorstein AD, Finnemann SC, Bonilha VL, Rodriguez-Boulan E: Morphogenesis of the retinal pigment epithelium: toward understanding retinal degenerative diseases. Ann N Y Acad Sci 1998, 857:1-12 (Pubitemid 28526251)
2. Tate DJ Jr., Miceli MV, Newsome DA: Phagocytosis and H2O2 induce catalase and metallothionein gene expression in human retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 1995, 36:1271-1279
3. Dorey CK, Delori FC, Akeo K: Growth of cultured RPE and endothelial cells is inhibited by blue light but not green or red light. Curr Eye Res 1990, 9:549-559 (Pubitemid 20316715)
4. Alder VA, Cringle SJ: The effect of the retinal circulation on vitreal oxygen tension. Curr Eye Res 1985, 4:121-129 (Pubitemid 15171830)
5. Kennedy CJ, Rakoczy PE, Constable IJ: Lipofuscin of the retinal pigment epithelium: a review. Eye 1995, 9(pt 6):763-771 (Pubitemid 26018204)
6. 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
7. Bressler NM, Munoz B, Maguire MG, Vitale SE, Schein OD, Taylor HR, West SK: Five-year incidence and disappearance of drusen and retinal pigment epithelial abnormalities: Waterman study. Arch Ophthalmol 1995, 113:301-308
8. Zhou J, Jang YP, Kim SR, Sparrow JR: Complement activation by photooxidation products of A2E, a lipofuscin constituent of the retinal pigment epithelium. Proc Natl Acad Sci U S A 2006, 103:16182-16187 (Pubitemid 44715171)
9. Yu DY, Cringle SJ, Su EN, Yu PK: Intraretinal oxygen levels before and after photoreceptor loss in the RCS rat. Invest Ophthalmol Vis Sci 2000, 41:3999-4006
10. Yu DY, Cringle S, Valter K, Walsh N, Lee D, Stone J: Photoreceptor death, trophic factor expression, retinal oxygen status, and photoreceptor function in the P23H rat. Invest Ophthalmol Vis Sci 2004, 45:2013-2019 (Pubitemid 38869001)
11. Shen J, Yang X, Dong A, Petters RM, Peng YW, Wong F, Campochiaro PA: Oxidative damage is a potential cause of cone cell death in retinitis pigmentosa. J Cell Physiol 2005, 203:457-464 (Pubitemid 40629006)
12. Komeima K, Rogers BS, Lu L, Campochiaro PA: Antioxidants reduce cone cell death in a model of retinitis pigmentosa. Proc Natl Acad Sci U S A 2006, 103:11300-11305 (Pubitemid 44159928)
13. Green WR, Key SN III: Senile macular degeneration: a histopathologic study. Trans Am Ophthalmol Soc 1977, 75:180-254
14. Green WR, McDonnell PJ, Yeo JH: Pathologic features of senile macular degeneration. Ophthalmology 1985, 92:615-627 (Pubitemid 15060973)
15. Spraul CW, Lang GE, Grossniklaus HE: Morphometric analysis of the choroid, Bruch's membrane, and retinal pigment epithelium in eyes with age-related macular degeneration. Invest Ophthalmol Vis Sci 1996, 37:2724-2735
16. Zarbin MA: Age-related macular degeneration: review of pathogenesis. Eur J Ophthalmol 1998, 8:199-206
17. Lu L, Oveson BC, Jo YJ, Lauer TW, Usui S, Komeima K, Xie B, Campochiaro PA: Increased expression of glutathione peroxidase 4 strongly protects retina from oxidative damage. Antioxid Redox Signal 2009, 11:715-724
18. Resnikoff S, Pascolini D, Etya'ale D, Kocur I, Pararajasegaram R, Pokharel GP, Mariotti SP: Global data on visual impairment in the year 2002. Bull World Health Organ 2004, 82:844-851
19. Wang L, Li CM, Rudolf M, Belyaeva OV, Chung BH, Messinger JD, Kedishvili NY, Curcio CA: Lipoprotein particles of intraocular origin in human Bruch membrane: an unusual lipid profile. Invest Ophthalmol Vis Sci 2009, 50:870-877
20. Huang JD, Curcio CA, Johnson M: Morphometric analysis of lipoprotein-like particle accumulation in aging human macular Bruch's membrane. Invest Ophthalmol Vis Sci 2008, 49:2721-2727
21. Jager RD, Mieler WF, Miller JW: Age-related macular degeneration. N Engl J Med 2008, 358:2606-2617
22. Pauleikhoff D, Sheraidah G, Marshall J, Bird AC, Wessing A: Biochemical and histochemical analysis of age related lipid deposits in Bruch's membrane [in German]. Ophthalmologe 1994, 91:730-734
23. Pauleikhoff D, Harper CA, Marshall J, Bird AC: Aging changes in Bruch's membrane: a histochemical and morphologic study. Ophthalmology 1990, 97:171-178 (Pubitemid 20051380)
24. Yanoff M, Duker JS, Augsburger JJ: Ophthalmology. St. Louis MO, Mosby, 2004.
25. Klein R, Peto T, Bird A, Vannewkirk MR: The epidemiology of age-related macular degeneration. Am J Ophthalmol 2004, 137:486-495 (Pubitemid 38328641)
26. Coleman H, Chew E: Nutritional supplementation in age-related macular degeneration. Curr Opin Ophthalmol 2007, 18:220-223 (Pubitemid 46624920)
27. 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 and vision loss: AREDS report no. 8. Arch Ophthalmol 2001, 119:1417-1436
28. Zeitz O, Schlichting L, Richard G, Strauss O: Lack of antioxidative properties of vitamin C and pyruvate in cultured retinal pigment epithelial cells. Graefes Arch Clin Exp Ophthalmol 2007, 245:276-281 (Pubitemid 46291458)
29. Marc RE, Jones BW, Watt CB, 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
30. Wu Z, Rogers B, Kachi S, Hackett SF, Sick A, Campochiaro PA: Reduction of p66Shc suppresses oxidative damage in retinal pigmented epithelial cells and retina. J Cell Physiol 2006, 209:996-1005 (Pubitemid 44665722)
31. Wenzel A, Grimm C, Marti A, Kueng-Hitz N, Hafezi F, Niemeyer G, Reme CE: c-fos controls the "private pathway" of light-induced apoptosis of retinal photoreceptors. J Neurosci 2000, 20:81-88
32. Abler AS, Chang CJ, Ful J, Tso MO, Lam TT: Photic injury triggers apoptosis of photoreceptor cells. Res Commun Mol Pathol Pharmacol 1996, 92:177-189 (Pubitemid 26164506)
33. Hafezi F, Marti A, Munz K, Reme CE: Light-induced apoptosis: differential timing in the retina and pigment epithelium. Exp Eye Res 1997, 64:963-970 (Pubitemid 27314771)
34. Reme CE, Grimm C, Hafezi F, Marti A, Wenzel A: Apoptotic cell death in retinal degenerations. Prog Retin Eye Res 1998, 17:443-464 (Pubitemid 28432977)
35. Penugonda S, Mare S, Goldstein G, Banks WA, Ercal N: Effects of N-acetylcysteine amide (NACA), a novel thiol antioxidant against glutamate-induced cytotoxicity in neuronal cell line PC12. Brain Res 2005, 1056:132-138 (Pubitemid 41557700)
36. Wu W, Abraham L, Ogony J, Matthews R, Goldstein G, Ercal N: Effects of N-acetylcysteine amide (NACA), a thiol antioxidant on radiation-induced cytotoxicity in Chinese hamster ovary cells. Life Sci 2008, 82:1122-1130
37. Price TO, Uras F, Banks WA, Ercal N: A novel antioxidant N-acetylcysteine amide prevents gp120- and Tat-induced oxidative stress in brain endothelial cells. Exp Neurol 2006, 201:193-202 (Pubitemid 44223475)
38. Am J, Atlas D, Fibach E: N-acetylcysteine amide (AD4) attenuates oxidative stress in β-thalassemia blood cells. Biochim Biophys Acta 2008, 1780:249-255
39. Grinberg L, Fibach E, Am J, Atlas D: N-acetylcysteine amide, a novel cell-permeating thiol, restores cellular glutathione and protects human red blood cells from oxidative stress. Free Radic Biol Med 2005, 38:136-145 (Pubitemid 39626919)
40. Wang XM, Terasaki PI, Rankin GW Jr., Chia D, Zhong HP, Hardy S: A new microcellular cytotoxicity test based on calcein AM release. Hum Immunol 1993, 37:264-270 (Pubitemid 23343716)
41. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C: A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 1995, 184:39-51
42. Wang H, Joseph JA: Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 1999, 27:612-616 (Pubitemid 29408648)
43. Winters RA, Zukowski J, Ercal N, Matthews RH, Spitz DR: Analysis of glutathione, glutathione disulfide, cysteine, homocysteine, and other biological thiols by high-performance liquid chromatography following derivatization by n-(1-pyrenyl)maleimide. Anal Biochem 1995, 227:14-21
44. Draper HH, Squires EJ, Mahmoodi H, Wu J, Agarwal S, Hadley M: A comparative evaluation of thiobarbituric acid methods for the determination of malondialdehyde in biological materials. Free Radic Biol Med 1993, 15:353-363 (Pubitemid 23283552)
45. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254
46. Peachey NS, Ball SL: Electrophysiological analysis of visual function in mutant mice. Doc Ophthalmol 2003, 107:13-36 (Pubitemid 36896235)
47. Zhu Y, Zhang Y, Ojwang BA, Brantley MA Jr., Gidday JM: Long-term tolerance to retinal ischemia by repetitive hypoxic preconditioning: role of HIF-1α and heme oxygenase-1. Invest Ophthalmol Vis Sci 2007, 48:1735-1743 (Pubitemid 351261360)
48. Beatty S, Koh H, Phil M, Henson D, Boulton M: The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 2000, 45:115-134
49. Seddon JM, Hennekens CH: Vitamins, minerals, and macular degeneration: promising but unproven hypotheses. Arch Ophthalmol 1994, 112:176-179 (Pubitemid 24058396)
50. Evereklioglu C, Er H, Doganay S, Cekmen M, Turkoz Y, Otlu B, Ozerol E: Nitric oxide and lipid peroxidation are increased and associated with decreased antioxidant enzyme activities in patients with age-related macular degeneration. Doc Ophthalmol 2003, 106:129-136 (Pubitemid 36355954)
51. Seddon JM, George S, Rosner B: Cigarette smoking, fish consumption, omega-3 fatty acid intake, and associations with age-related macular degeneration: the US Twin Study of Age-Related Macular Degeneration. Arch Ophthalmol 2006, 124:995-1001 (Pubitemid 44036322)
52. Evans JR: Risk factors for age-related macular degeneration. Prog Retin Eye Res 2001, 20:227-253
53. Offen D, Gilgun-Sherki Y, Barhum Y, Benhar M, Grinberg L, Reich R, Melamed E, Atlas D: A low molecular weight copper chelator crosses the blood-brain barrier and attenuates experimental autoimmune encephalomyelitis. J Neurochem 2004, 89:1241-1251 (Pubitemid 38715842)
54. Penugonda S, Mare S, Lutz P, Banks WA, Ercal N: Potentiation of lead-induced cell death in PC12 cells by glutamate: protection by N-acetylcysteine amide (NACA), a novel thiol antioxidant. Toxicol Appl Pharmacol 2006, 216:197-205 (Pubitemid 44466001)
55. Dunn KC, Aotaki-Keen AE, Putkey FR, Hjelmeland LM: ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp Eye Res 1996, 62:155-169 (Pubitemid 26140102)
56. Thornalley PJ, Trotta RJ, Stern A: Free radical involvement in the oxidative phenomena induced by tert-butyl hydroperoxide in erythrocytes. Biochim Biophys Acta 1983, 759:16-22 (Pubitemid 13013116)
57. Masaki N, Kyle ME, Farber JL: Tert-butyl hydroperoxide kills cultured hepatocytes by peroxidizing membrane lipids. Arch Biochem Biophys 1989, 269:390-399 (Pubitemid 19075751)
58. Comporti M: Glutathione depleting agents and lipid peroxidation. Chem Phys Lipids 1987, 45:143-169
59. Cai J, Wu M, Nelson KC, Sternberg P Jr., Jones DP: Oxidant-induced apoptosis in cultured human retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 1999, 40:959-966 (Pubitemid 29153262)
60. Omatsu T, Naito Y, Handa O, Hayashi N, Mizushima K, Qin Y, Hirata I, Adachi S, Okayama T, Kishimoto E, Takagi T, Kokura S, Ichikawa H, Yoshikawa T: Involvement of reactive oxygen species in indomethacin-induced apoptosis of small intestinal epithelial cells. J Gastroenterol 2009, 44(Suppl 19):30-34
61. Young RW: Pathophysiology of age-related macular degeneration. Surv Ophthalmol 1987, 31:291-306
62. Feeney-Burns L, Berman ER, Rothman H: Lipofuscin of human retinal pigment epithelium. Am J Ophthalmol 1980, 90:783-791 (Pubitemid 11199131)
63. Terman A, Brunk UT: Oxidative stress, accumulation of biological "garbage," and aging. Antioxid Redox Signal 2006, 8:197-204 (Pubitemid 43324546)
64. Terman A, Gustafsson B, Brunk UT: Mitochondrial damage and intralysosomal degradation in cellular aging. Mol Aspects Med 2006, 27:471-482 (Pubitemid 44466654)
65. Sparrow JR, Fishkin N, Zhou J, Cai B, Jang YP, Krane S, Itagaki Y, Nakanishi K: A2E, a byproduct of the visual cycle. Vision Res 2003, 43:2983-2990 (Pubitemid 37377610)
66. Spaide RF, Ho-Spaide WC, Browne RW, Armstrong D: Characterization of peroxidized lipids in Bruch's membrane. Retina 1999, 19:141-147 (Pubitemid 30368160)
67. Moore K, Roberts LJ II: Measurement of lipid peroxidation. Free Radic Res 1998, 28:659-671 (Pubitemid 28454258)
68. Finkel T, Holbrook NJ: Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408:239-247
69. Sternberg P Jr., Davidson PC, Jones DP, Hagen TM, Reed RL, Drews-Botsch C: Protection of retinal pigment epithelium from oxidative injury by glutathione and precursors. Invest Ophthalmol Vis Sci 1993, 34:3661-3668 (Pubitemid 24012006)
70. Nelson KC, Armstrong JS, Moriarty S, Cai J, Wu MW, Sternberg P Jr., Jones DP: Protection of retinal pigment epithelial cells from oxidative damage by oltipraz, a cancer chemopreventive agent. Invest Ophthalmol Vis Sci 2002, 43:3550-3554 (Pubitemid 35334364)
71. Gong X, Celsi G, Carlsson K, Norgren S, Chen M: N-acetylcysteine amide protects renal proximal tubular epithelial cells against iohexol-induced apoptosis by blocking p38 MAPK and iNOS signaling. Am J Nephrol 31:178-188
72. Heverly-Coulson GS, Boyd RJ: Reduction of hydrogen peroxide by glutathione peroxidase mimics: reaction mechanism and energetics. J Phys Chem A 2010, 114:1996-2000
73. Lu L, Oveson BC, Jo YJ, Lauer T, Usui S, Komeima K, Xie B, Campochiaro PA: Increased expression of glutathione peroxidase 4 strongly protects retina from oxidative damage. Antioxid Redox Signal 2009, 11:715-724
74. Organisciak DT, Vaughan DK: Retinal light damage: mechanisms and protection. Prog Retin Eye Res 2010, 29:113-134
75. Gao H, Hollyfield JG: Aging of the human retina: differential loss of neurons and retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 1992, 33:1-17
76. Curcio CA, Millican CL, Allen KA, Kalina RE: Aging of the human photoreceptor mosaic: evidence for selective vulnerability of rods in central retina. Invest Ophthalmol Vis Sci 1993, 34:3278-3296 (Pubitemid 23346660)
77. Dorey CK, Wu G, Ebenstein D, Garsd A, Weiter JJ: Cell loss in the aging retina: relationship to lipofuscin accumulation and macular degeneration. Invest Ophthalmol Vis Sci 1989, 30:1691-1699 (Pubitemid 19214989)