Photooxidation of A2-PE, a photoreceptor outer segment fluorophore, and protection by lutein and zeaxanthin

Experimental Eye Research

Volumn 82, Issue 5, 2006, Pages 828-839

  Kim, So Ra ^a   Nakanishi, Koji ^a   Itagaki, Yasuhiro ^a   Sparrow, Janet R ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

A2 PE; A2E; Carotenoids; Lutein; Photooxidation; Photoreceptor cells; Quenching; RPE lipofuscin precursor; Zeaxanthin

Indexed keywords

A2 PE; ALPHA TOCOPHEROL; UNCLASSIFIED DRUG; VISUAL PIGMENT; XANTHOPHYLL; ZEAXANTHIN;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BLUE LIGHT; CELL DAMAGE; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IRRADIATION; MOUSE; NONHUMAN; PHOTOOXIDATION; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA DEGENERATION; RETINA MACULA LUTEA;

ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; LIGHT; LUTEIN; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; OXIDATION-REDUCTION; PYRIDINIUM COMPOUNDS; RETINOIDS; ROD OUTER SEGMENTS; XANTHOPHYLLS;

EID: 31644442048     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2005.10.004     Document Type: Article

References (70)

1. R. Allikmets, N. Singh, H. Sun, N.F. Shroyer, A. Hutchinson, A. Chidambaram, B. Gerrard, L. Baird, D. Stauffer, A. Peiffer, A. Rattner, P. Smallwood, Y. Li, K.L. Anderson, R.A. Lewis, J. Nathans, M. Leppert, M. Dean, and J.R. Lupski A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy Nat. Genet. 15 1997 236 246
2. AREDS Study Group Risk factors for neovascular age-related macular degeneration Arch. Ophthalmol. 110 1992 1701 1708
3. J. Baldas, Q.N. Porter, L. Cholnoky, J. Szabolos, and B.C.L. Weedon Mass spectrometry of carotenoid epoxides and furanoid oxides Chem. Commun. 23 1966 852 854
4. S. Beatty, I.J. Murray, D.B. Henson, D. Carden, H.H. Koh, and M.E. Boulton Macular pigment and risk for age-related macular degeneration in subjects from a Northern European population Invest. Ophthalmol. Vis. Sci. 42 2001 439 446
5. S. Beatty, J. Nolan, H. Kavanagh, and O. O'Donovan Macular pigment optical density and its relationship with serum and dietary levels of lutein and zeaxanthin Arch. Biochem. Biophys. 430 2004 70 76
6. S. Ben-Shabat, Y. Itagaki, S. Jockusch, J.R. Sparrow, N.J. Turro, and K. Nakanishi Formation of a nona-oxirane from A2E, a lipofuscin fluorophore related to macular degeneration, and evidence of singlet oxygen involvement Angew. Chem. Int. Ed. 41 2002 814 817
7. S. Ben-Shabat, C.A. Parish, H.R. Vollmer, Y. Itagaki, N. Fishkin, K. Nakanishi, and J.R. Sparrow Biosynthetic studies of A2E, a major fluorophore of RPE lipofuscin J. Biol. Chem. 277 2002 7183 7190
8. P.S. Bernstein, F. Khachik, L.S. Carvalho, G.J. Muir, D.Y. Zhao, and N.B. Katz Identification and quantitation of carotenoids and their metabolites in the tissues of the human eye Exp. Eye Res. 72 2001 215 223
9. P.S. Bernstein, D.Y. Zhao, S.W. Wintch, I.V. Ermakov, R.W. McClane, and W. Gellerman Resonance raman measurement of macular carotenoids in normal subjects and in age-related macular degeneration patients Ophthalmology 109 2002 1780 1787
10. P. Bhosale, A.J. Larson, J.M. Frederick, K. Southwick, C.D. Thulin, and P.S. Bernstein Identification and characterization of a Pi isoform of glutathioine S-transferase (GSTP1) as a zeaxanthin-binding protein in the macula of the human eye J. Biol. Chem. 279 2004 49447 49454
11. C.D. Birnbach, M. Jarvelainen, D.E. Possin, and A.H. Milam Histopathology and immunocytochemistry of the neurosensory retina in fundus flavimaculatus Ophthalmology 101 1994 1211 1219
12. R.A. Bone, J.T. Landrum, and S.L. Tarsis Preliminary identification of the human macular pigment Vision Res. 25 1985 1531 1535
13. R.A. Bone, J.T. Landrum, L. Fernandez, and S.L. Tarsis Analysis of the macular pigment by HPLC: retinal distribution and age study Invest. Ophthalmol. Vis. Sci. 29 1988 843 849
14. R.A. Bone, J.T. Landrum, L.M. Friedes, C.M. Gomez, M.D. Kilburn, E. Menendez, I. Vidal, and W. Wang Distribution of lutein and zeaxanthin stereoisomers in the human retina Exp. Eye Res. 64 1997 211 218
15. R.A. Bone, J.T. Landrum, S.T. Mayne, C.M. Gomez, S.E. Tibor, and E.E. Twaroska Macular pigment in donor eyes with and without AMD: a case-control study Invest. Ophthalmol. Vis. Sci. 42 2001 235 240
16. A.H. Bunt-Milam, R.E. Kalina, and R.A. Pagon Clinical-ultrastructural study of a retinal dystrophy Invest. Ophthalmol. Vis. Sci. 24 1983 458 469
17. R.A. Dilley, and D.G. McConnell Alpha-tocopherol in the retinal outer segments of bovine eyes J. Membr. Biol. 2 1970 317 323
18. J. Dillon, Z. Wang, L.B. Avalle, and E.R. Gaillard The photochemical oxidation of A2E results in the formation of a 5,8,5′,8′-bis- furanoid oxide Exp. Eye Res. 79 2004 537 542
19. N. Fishkin, J.R. Sparrow, R. Allikmets, and K. Nakanishi Isolation and characterization of a retinal pigment epithelial cell fluorophore: an all-trans-retinal dimer conjugate Proc. Natl Acad. Sci. USA 102 2005 7091 7096
20. C. Grimm, A. Wenzel, T.P. Williams, P.O. Rol, F. Hafezi, and C.E. Reme Rhodopsin-mediated blue-light damage to the rat retina: effect of photoreversal of bleaching Invest. Ophthalmol. Vis. Sci. 42 2001 497 505
21. B.R. Hammond, E.J. Johnson, R.M. Russell, N.I. Krinsky, K.J. Yeum, R.B. Edwards, and D.M. Snodderly Dietary modification of human macular pigment density Invest. Ophthalmol. Vis. Sci. 38 1997 1795 1801
22. Jang, YP., Matsuda, H., Itagaki, Y., Nakanishi, K., Sparrow, J.R. 2005. Characterization of peroxy-A2E and furan-A2E photooxidation products and detection in human and mouse retinal pigment epithelial cells lipofuscin. J. Biol. Chem.
23. A. Junghans, H. Sies, and W. Stahl Macular pigments lutein and zeaxanthin as blue light filters studied in liposomes Arch. Biochem. Biophys. 391 2001 160 164
24. S. Kaiser, P.D. Mascio, M.E. Murphy, and H. Sies Physical and chemical scavenging of singlet molecular oxygen by tocopherols Arch. Biochem. Biophys. 277 1990 101 108
25. T.A. Kennedy, and D.C. Liebler Peroxyl radical oxidation of b-carotene: formation of b-carotene epoxides Chem. Res. Toxicol. 4 1991 290 295
26. F. Khachik, P.S. Bernstein, and D.L. Garland Identification of lutein and zeaxanthin oxidation products in human and monkey retinas Invest. Ophthalmol. Vis. Sci. 38 1997 1802 1811
27. S.R. Kim, N. Fishkin, J. Kong, K. Nakanishi, R. Allikmets, and J.R. Sparrow The Rpe65 Leu450Met variant is associated with reduced levels of the RPE lipofuscin fluorophores A2E and iso-A2E Proc. Natl Acad. Sci. USA 101 2004 11668 11672
28. N.I. Krinsky Possible biologic mechanisms for a protective role of zanthophylls J. Nutr. 132 2002 540S 542S
29. J.T. Landrum, and R.A. Bone Lutein, zeaxanthin and the macular pigment Arch. Biochem. Biophys. 385 2001 28 40
30. J.T. Landrum, R.A. Bone, H. Joa, M.D. Kilburn, L.L. Moore, and K.E. Sprague A one year study of the macular pigment: the effect of 140 days of a lutein supplement Exp. Eye Res. 65 1997 57 62
31. I.Y.F. Leung, M.M. Sandstrom, C.L. Zucker, M. Neuringer, and D.M. Snodderly Nutritional manipulation of primate retinas, II: effects of age, n-3 fatty acids, lutein and zeaxanthin on retinal pigment epithelium Exp. Eye Res. 45 2004 3244 3256
32. J. Liu, Y. Itagaki, S. Ben-Shabat, K. Nakanishi, and J.R. Sparrow The biosynthesis of A2E, a fluorophore of aging retina, involves the formation of the precursor, A2-PE, in the photoreceptor outer segment membrane J. Biol. Chem. 275 2000 29354 29360
33. M.R. Malinow, L. Feeney-Burns, L.H. Peterson, M.L. Klein, and M. Neuringer Diet-related macular anomalies in monkeys Invest. Ophthalmol. Vis. Sci. 19 1980 857 863
34. J.A. Mares-Perlman, W.F. Brady, R. Klein, B.E.K. Klein, P. Bowen, M. Stacewicz-Sapuntzakis, and M. Palta Serum antioxidants and age-related macular degeneration in a population-based case-control study Arch. Ophthalmol. 113 1995 1518 1523
35. H.D. Martin, C. Ruck, M. Schmidt, S. Sell, S. Beutner, B. Mayer, and R. Walsh Chemistry of carotenoid oxidation and free radical reactions Pure Appl. Chem. 71 1999 2253 2262
36. P.D. Mascio, M.E. Murphy, and H. Sies Antioxidant defense systems: the role of carotenoids, tocopherols, and thiols Am. J. Clin. Nutr. 53 1991 194S 200S
37. N.L. Mata, J. Weng, and G.H. Travis Biosynthesis of a major lipofuscin fluorophore in mice and humans with ABCR-mediated retinal and macular degeneration Proc. Natl Acad. Sci. USA 97 2000 7154 7159
38. N.L. Mata, R.T. Tzekov, X. Liu, J. Weng, D.G. Birch, and G.H. Travis Delayed dark adaptation and lipofuscin accumulation in abcr±mice: implications for involvement of ABCR in age-related macular degeneration Invest. Ophthalmol. Vis. Sci. 42 2001 1685 1690
39. M. Neuringer, M.M. Sandstrom, E.J. Johnson, and D.M. Snodderly Nutritional manipulation of primate retinas, I: effects of lutein and zeaxanthin supplements on serum and macular pigment in xanthophyll-free rhesus monkeys Exp. Eye Res. 45 2004 3234 3243
40. S.A.R. Paiva, and R.M. Russell B-carotene and other carotenoids as antioxidants Am. Coll. Nutr. 18 1999 426 433
41. P. Palozza, and N.I. Krinsky Beta-carotene and alpha-tocopherol are synergistic antioxidants Arch. Biochem. Biophys. 297 1992 184 187
42. C.A. Parish, M. Hashimoto, K. Nakanishi, J. Dillon, and J.R. Sparrow Isolation and one-step preparation of A2E and iso-A2E, fluorophores from human retinal pigment epithelium Proc. Natl Acad. Sci. USA 95 1998 14609 14613
43. J.K. Prasain, R. Moore, J.S. Hurst, S. Barnes, and F.J.G.M. van Kuijk Electrospray tandem mass spectrometric analysis of zeaxanthin and its oxidation products J. Mass. Spectrom. 40 2005 916 923
44. L.M. Rapp, S.S. Maple, and J.H. Choi Lutein and zeaxanthin concentrations in rod outer segment membranes from perifoveal and peripheral human retina Invest. Ophthalmol. Vis. Sci. 41 2000 1200 1209
45. V.M. Reading, and R.A. Weale Macular pigment and chromatic aberration J. Opt. Soc. Am. 64 1974 231 234
46. J.M. Seddon, U.A. Ajani, R.D. Sperduto, R. Hiller, N. Blair, T.C. Burton, M.D. Farber, E.S. Gragoudas, J. Haller, and D.T. Miller Dietary carotenoids, vitamins A, C and E and advanced age-related macular degeneration. Eye disease case-control study group J. Am. Med. Assoc. 272 1994 1413 1420
47. D.M. Snodderly, J.D. Auran, and F.C. Delori The macular pigment, II: spatial distribution in primate retinas Invest. Ophthalmol. Vis. Sci. 25 1984 674 685
48. D.M. Snodderly, G.J. Handelman, and A.J. Adler Distribution of individual macular pigment carotenoids in central retina of macaque and squirrel monkeys Invest. Ophthalmol. Vis. Sci. 32 1991 268 279
49. O.G. Sommerburg, W.G. Siems, J.S. Hurst, J.W. Lewis, D.S. Kliger, and F.J. van Kuijk Lutein and zeaxanthin are associated with photoreceptors in the human retina Curr. Eye Res. 19 1999 491 495
50. J.R. Sparrow, and B. Cai Blue light-induced apoptosis of A2E-containing RPE: involvement of caspase-3 and protection by Bcl-2 Invest. Ophthalmol. Vis. Sci. 42 2001 1356 1362
51. J.R. Sparrow, and M. Boulton RPE lipofuscin and its role in retinal photobiology Exp. Eye Res. 80 2005 595 606
52. J.R. Sparrow, K. Nakanishi, and C.A. Parish The lipofuscin fluorophore A2E mediates blue light-induced damage to retinal pigmented epithelial cells Invest. Ophthalmol. Vis. Sci. 41 2000 1981 1989
53. J.R. Sparrow, J. Zhou, S. Ben-Shabat, H. Vollmer, Y. Itagaki, and K. Nakanishi Involvement of oxidative mechanisms in blue light induced damage to A2E-laden RPE Invest. Ophthalmol. Vis. Sci. 43 2002 1222 1227
54. J.R. Sparrow, H.R. Vollmer-Snarr, J. Zhou, Y.P. Jang, S. Jockusch, Y. Itagaki, and K. Nakanishi A2E-epoxides damage DNA in retinal pigment epithelial cells. Vitamin E and other antioxidants inhibit A2E-epoxide formation J. Biol. Chem. 278 2003 18207 18213
55. J.R. Sparrow, J. Zhou, and B. Cai DNA is a target of the photodynamic effects elicited in A2E-laden RPE by blue light illumination Invest. Ophthalmol. Vis. Sci. 44 2003 2245 2251
56. W. Stahl, and H. Sies Antioxidant activity of carotenoids Mol. Aspect Med. 24 2003 345 351
57. W. Stahl, S. Nicolai, K. Briviba, M. Hanusch, G. Broszeit, M. Peters, H.D. Martin, and H. Sies Biological activities of natural and synthetic carotenoids: induction of gap junctional communication and singlet oxygen quenching Carcinogenesis 18 1997 89 92
58. S.P. Stratton, W.H. Schaefer, and D.C. Liebler Isolation and identification of singlet oxygen oxidation products of b-carotene Chem. Res. Toxicol. 6 1993 542 547
59. A. Sujak, P. Mazurek, and W.I. Gruszecki Xanthophyll pigments lutein and zeaxanthin in lipid multilayers formed with dimyristoylphosphatidylcholine J. Photochem. Photobiol. B 68 2002 39 44
60. R.B. Szamier, and E.L. Berson Retinal ultrastructure in advanced retinitis pigmentosa Invest. Ophthalmol. Vis. Sci. 16 1977 947 962
61. L.R. Thomson, Y. Toyodaa, F.C. Delori, K.M. Garnett, Z.Y. Wonga, C.R. Nichols, K.M. Cheng, N.E. Craft, and C.K. Dorey Long term dietary supplementation with zeaxanthin reduces photoreceptor death in light-damaged Japanese quail Exp. Eye Res. 75 2002 529 542
62. M. Trieschmann, G. Spital, A. Lommatzsch, E. van Kuijk, F.W. Fitzke, A.C. Bird, and D. Pauleikhoff Macular pigment: quantitative analysis on autofluorescence images Graefe's Arch. Clin. Exp. Ophthalmol. 241 2003 1006 1012
63. N.J. Turro, M.-F. Chow, and J. Rigaudyo Mechanism of thermolysis of endoperoxides of aromatic compounds. Activation parameters, magnetic field, and magnetic isotope effects J. Am. Chem. Soc. 103 1981 7218 7222
64. X.D. Wang, and R.M. Russell Procarcinogenic and anticarcinogenic effects of b-carotene Nutr. Rev. 57 1999 263 272
65. J.J. Weiter, F.C. Delori, and C.K. Dorey Central sparing in annular macular degeneration Am. J. Ophthalmol. 106 1988 286 290
66. A. Wenzel, C. Grimm, M. Samardzija, and C.E. Reme Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration Prog. Retin. Eye Res. 24 2005 275 306
67. R.D. Wiegand, C.D. Joel, L.M. Rapp, J.C. Nielsen, M.B. Maude, and R.E. Anderson Polyunsaturated fatty acids and vitamin E in rat rod outer segments during light damage Invest. Ophthalmol. Vis. Sci. 27 1986 727 733
68. A. Wyss Carotene oxygenases: a new family of double bond cleavage enzymes J. Nutr. 134 2004 246S 250S
69. A.J. Young, and H.A. Frank Energy transfer reactions involving carotenoids: quenching of chlorophyl fluorescence J. Photochem. Photobiol. B Biol. 36 1996 3 15
70. J. Zhou, B. Cai, Y.P. Jang, S. Pachydaki, A.M. Schmidt, and J.R. Sparrow Mechanisms for the induction of HNE- MDA- and AGE-adducts, RAGE and VEGF in retinal pigment epithelial cells Exp. Eye Res. 80 2005 567 580