UV-A induced oxidative stress is more prominent in naturally pigmented aged human RPE cells compared to non-pigmented human RPE cells independent of zinc treatment

Journal of Photochemistry and Photobiology B: Biology

Volumn 90, Issue 2, 2008, Pages 113-120

  Biesemeier, Antje ^a   Kokkinou, Despina ^a   Julien, Sylvie ^a   Heiduschka, Peter ^a   Berneburg, Mark ^b   Bartz Schmidt, Karl Ulrich ^a   Schraermeyer, Ulrich ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Human retinal pigment epithelial cells; Lipofuscin; Melanin; Melanolipofuscin; Oxidative stress; UV A irradiation

Indexed keywords

HYDROGEN PEROXIDE; LIPOFUSCIN; MELANIN; ZINC CHLORIDE;

ADULT; AGED; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL ASSAY; CELL GRANULE; CELL STRESS; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; EYE PROTECTION; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RADIATION EXPOSURE; RETINA CELL; ULTRAVIOLET A RADIATION;

AGED; APOPTOSIS; CELL AGING; CELL SURVIVAL; HUMANS; HYDROGEN PEROXIDE; MIDDLE AGED; OXIDATIVE STRESS; PIGMENT EPITHELIUM OF EYE; PIGMENTATION; ULTRAVIOLET RAYS; ZINC;

EID: 38949130408     PISSN: 10111344     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2007.11.005     Document Type: Article

References (68)

1. Bird A.C., Bressler N.M., Bressler S.B., Chisholm I.H., Coscas G., Davis M.D., de Jong P.T., Klaver C.C., Klein B.E., and Klein R. An international classification and grading system for age-related maculopathy and age-related macular degeneration. The international ARM epidemiological study group. Surv. Ophthalmol. 39 (1995) 367-374
2. Smith W., Assink J., Klein R., Mitchell P., Klaver C.C.W., Klein B.E.K., Hofman A., Jensen S., Wang J.J., and De Jong P.T.V.M. Risk factors for age related macular degeneration - pooled findings from three continents. Ophthalmology 108 (2001) 697-704
3. Berendschot T.T.J.M., Willemse-Assink J.J.M., Bastiaanse M., De Jong P.T.V.M., and van Norren D. Macular pigment and melanin in age-related maculopathy in a general population. Invest. Ophth. Vis. Sci. 43 (2002) 1928-1932
4. Klein R., Klein B.E., and Cruickshanks K.J. The prevalence of age-related maculopathy by geographic region and ethnicity. Prog. Retin. Eye Res. 18 (1999) 371-389
5. Weiter J.J., Delori F.C., Wing G.L., and Fitch K.A. Relationship of senile macular degeneration to ocular pigmentation. Am. J. Ophthalmol. 99 (1985) 185-187
6. Pauleikhoff D., and Holz F.G. Age-related macular degeneration. 1. Epidemiology, pathogenesis and differential diagnosis. Ophthalmologe 93 (1996) 299-315
7. Gregor Z., and Joffe L. Senile macular changes in the black African. Br. J. Ophthalmol. 62 (1978) 547-550
8. Ambati J., Ambati B.K., Yoo S.H., Ianchulev S., and Adamis A.P. Age-related macular degeneration: etiology, pathogenesis, and therapeutic strategies. Surv. Ophthalmol. 48 (2003) 257-293
9. Schraermeyer U., and Heimann K. Current understanding on the role of retinal pigment epithelium and its pigmentation. Pigment Cell Res. 12 4 (1999) 219-236
10. Sarna T. Properties and function of the ocular melanin - a photobiophysical view. J. Photochem. Photobiol. B 12 (1992) 215-258
11. Sakina N.L., Dontsov A.E., Afanas'ev G.G., Ostrovski M.A., and Pelevina I.I. The accumulation of lipid peroxidation products in the eye structures of mice under whole-body X-ray irradiation. Radiobiologia 30 (1990) 28-31
12. Felix C.C., Hyde J.S., Sarna T., and Sealy R.C. Melanin photoreactions in aerated media: electron spin resonance evidence for production of superoxide and hydrogen peroxide. Biochem. Biophys. Res. Commun. 84 (1978) 335-341
13. Korytowski W., Pilas B., Sarna T., and Kalyanaraman B. Photoinduced generation of hydrogen peroxide and hydroxyl radicals in melanins. Photochem. Photobiol. 45 (1987) 185-190
14. Glickman R.D., Sowell R., and Lam K.W. Kinetic properties of light-dependent ascorbic acid oxidation by melanin. Free Radic. Biol. Med. 15 (1993) 453-457
15. Rozanowska M., Bober A., Burke J.M., and Sarna T. The role of retinal pigment epithelium melanin in photoinduced oxidation of ascorbate. Photochem. Photobiol. 65 (1997) 472-479
16. Robison Jr. W.G., Kuwabara T., and Cogan D.G. Lysosomes and melanin granules of the retinal pigment epithelium in a mouse model of the Chediak-Higashi syndrome. Invest. Ophthalmol. 14 (1975) 312-317
17. van Norren D., and Tiemeijer L.F. Spectral reflectance of the human eye. Vis. Res. 26 (1986) 313-320
18. D.A. Samuelson, S. Konkal, P. Lewis, M. Chisholm, Changes of metal binding in human RPE melanin and lipofuscin associated with aging and drusen (ARVO Abstract), Invest. Ophthalmol. Vis. Sci. 37(3) 15-2-1996 Ref Type: Abstract.
19. Boulton M., Rozanowska M., Rozanowski B., and Wess T. The photoreactivity of ocular lipofuscin. Photochem. Photobiol. Sci. 3 (2004) 759-764
20. Brunk U.T., Jones C.B., and Sohal R.S. A novel hypothesis of lipofuscinogenesis and cellular aging based on interactions between oxidative stress and autophagocytosis. Mutat. Res. 275 (1992) 395-403
21. Boulton M., Dontsov A., Jarvis-Evans J., Ostrovsky M., and Svistunenko D. Lipofuscin is a photoinducible free radical generator. J. Photochem Photobiol. B 19 (1993) 201-204
22. Bray T.M., and Bettger W.J. The physiological role of zinc as an antioxidant. Free Radic. Biol. Med. 8 (1990) 281-291
23. Deng Z., Liu X., Chen J., and Yang R. Zinc protective effects on pig retinal pigment epithelial cell damage of lipid peroxide induced by 2450 MHz microwave. Wei Sheng Yan Jiu 29 (2000) 129-131
24. 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. 119 (2001) 1417-1436.
25. Potts A.M., and Au P.C. The affinity of melanin for inorganic ions. Exp. Eye Res. 22 (1976) 487-491
26. Brewer G.J., Hill G.M., Prasad A.S., and Cossack Z.T. Biological roles of ionic zinc. Prog. Clin. Biol. Res. 129 (1983) 35-51
27. Tate D.J., Miceli M.V., and Newsome D.A. Zinc induces catalase expression in cultured fetal human retinal pigment epithelial cells. Curr. Eye Res. 16 (1997) 1017-1023
28. Miceli M.V., Tate D.J., Alcock N.W., and Newsome D.A. Zinc deficiency and oxidative stress in the retina of pigmented rats. Invest. Ophthal. Vis. Sci. 40 (1999) 1238-1244
29. Samuelson D.A., Armstrong D., and Jolly R. X-ray microprobe analysis of the retina and RPE in sheep with ovine ceroid-lipofuscinosis. Neurobiol. Aging 11 (1990) 663-667
30. Borovansky J., and Riley P.A. Cytotoxicity of zinc in vitro. Chem. Biol. Interact. 69 (1989) 279-291
31. Lengyel I., Flinn J.M., Peto T., Linkous D.H., Cano K., Bird A.C., Lanzirotti A., Frederickson C.J., and van Kuijk F.J. High concentration of zinc in sub-retinal pigment epithelial deposits. Exp. Eye Res. 84 (2007) 772-780
32. Osborne N.N., and Wood J.P.M. The beta-adrenergic receptor antagonist metipranolol blunts zinc-induced photoreceptor and RPE apoptosis. Invest. Ophthal. Vis. Sci. 47 (2006) 3178-3186
33. Wood J.P.M., and Osborne N.N. The influence of zinc on caspase-3 and DNA breakdown in cultured human retinal pigment epithelial cells. Arch. Ophthal. 119 (2001) 81-88
34. Winkler B.S., Boulton M.E., Gottsch J.D., and Sternberg P. Oxidative damage and age-related macular degeneration. Mol. Vis. 5 (1999)
35. Cai J.Y., Nelson K.C., Wu M., Sternberg P., and Jones D.P. Oxidative damage and protection of the RPE. Prog. Retin. Eye Res. 19 (2000) 205-221
36. Hogg R., and Chakravarthy U. AMD and micronutrient antioxidants. Curr. Eye Res. 29 (2004) 387-401
37. Beatty S., Koh H., Phil M., Henson D., and Boulton M.E. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv. Ophthalmol. 45 (2000) 115-134
38. Friedman D.S., O'Colmain B.J., Munoz B., Tomany S.C., McCarty C., de Jong P.T., Nemesure B., Mitchell P., and Kempen J. Prevalence of age-related macular degeneration in the United States. Arch. Ophthalmol. 122 (2004) 564-572
39. Green W.R., McDonnell P.J., and Yeo J.H. Pathologic features of senile macular degeneration. Ophthalmology 92 (1985) 615-627
40. Young R.W. Solar radiation and age-related macular degeneration. Surv. Ophthalmol. 32 (1988) 252-269
41. Rozanowska M., Jarvis-Evans J., Korytowski W., Boulton M.E., Burke J.M., and Sarna T. Blue light-induced reactivity of retinal age pigment. In vitro generation of oxygen-reactive species. J. Biol. Chem. 270 (1995) 18825-18830
42. West S.K., Rosenthal F.S., Bressler N.M., Bressler S.B., Munoz B., Fine S.L., and Taylor H.R. Exposure to sunlight and other risk factors for age-related macular degeneration. Arch. Ophthalmol. 107 (1989) 875-879
43. Reme C., Reinboth J., Clausen M., and Hafezi F. Light damage revisited: converging evidence, diverging views?. Graefes Arch. Clin. Exp. Ophthalmol. 234 (1996) 2-11
44. Zuclich J.A. Ultraviolet-induced photochemical damage in ocular tissues. Health Phys. 56 (1989) 671-682
45. Glickman R.D., and Lam K.W. Oxidation of ascorbic acid as an indicator of photooxidative stress in the eye. Photochem. Photobiol. 55 (1992) 191-196
46. Scott G. Atmospheric oxidation and antioxidants. In: Sarna T S.H. (Ed). Interactions of Melanin with Oxygen (and related) Species vol. III (1993), Elsevier, Amsterdam 129-169
47. Davies S., Elliott M.H., Floor E., Truscott T.G., Zareba M., Sarna T., Shamsi F.A., and Boulton M.E. Photocytotoxicity of lipofuscin in human retinal pigment epithelial cells. Free Radic. Biol. Med. 31 (2001) 256-265
48. Reszka K., Eldred G.E., Wang R.H., Chignell C., and Dillon J. The photochemistry of human retinal lipofuscin as studied by EPR. Photochem. Photobiol. 62 (1995) 1005-1008
49. Katz M.L., Parker K.R., Handelman G.J., Bramel T.L., and Dratz E.A. Effects of antioxidant nutrient deficiency on the retina and retinal pigment epithelium of albino rats: a light and electron microscopic study. Exp. Eye Res. 34 (1982) 339-369
50. Weiter J.J., Delori F.C., Wing G.L., and Fitch K.A. Retinal pigment epithelial lipofuscin and melanin and choroidal melanin in human eyes. Invest. Ophthalmol. Vis. Sci. 27 (1986) 145-152
51. Fite K.V., Bengston L., and Donaghey B. Experimental light damage increases lipofuscin in the retinal pigment epithelium of Japanese quail (Coturnix coturnix japonica). Exp. Eye Res. 57 (1993) 449-460
52. Borovansky J., Horcicko J., and Duchon J. The hair melanosome: another tissue reservoir of zinc. Physiol. Bohemoslov. 25 (1976) 87-91
53. Borovansky J., Vedralova E., and Hach P. An estimate of melanosome concentration in pigment tissues. Pigment Cell Res. 4 (1991) 222-224
54. Galin M.A., Nano H.D., and Hall T. Ocular zinc concentration. Invest. Ophthalmol. 1 (1962) 142-148
55. Sarks J.P., Sarks S.H., and Killingsworth M.C. Evolution of soft drusen in age-related macular degeneration. Eye 8 Pt 3 (1994) 269-283
56. Kokkinou D., Kasper H.U., Schwarz T., Bartz-Schmidt K.U., and Schraermeyer U. Zinc uptake and storage: the role of fundus pigmentation. Graefes Arch. Clin. Exp. Ophthalmol. 243 (2005) 1050-1055
57. Kokkinou D., Kasper H.U., Bartz-Schmidt K.U., and Schraermeyer U. The pigmentation of human iris influences the uptake and storing of zinc. Pigment Cell Res. 17 (2004) 515-518
58. Ha K.N., Chen Y., Cai J.Y., and Sternberg P. Increased glutathione synthesis through an ARE-Nrf2-dependent pathway by zinc in the RPE: Implication for protection against oxidative stress. Invest. Ophthal.Vis. Sci. 47 (2006) 2709-2715
59. 2+ ions on mitochondrial electron transport. Arch. Biochem. Biophys. 165 (1974) 121-125
60. Ugarte M., and Osborne N.N. The localization of endogenous zinc and the in vitro effect of exogenous zinc on the GABA immunoreactivity and formation of reactive oxygen species in the retina. Gen. Pharmacol. 30 (1998) 297-303
61. Yoo M.H., Lee J.Y., Lee S.E., Koh J.Y., and Yoon Y.H. Protection by pyruvate of rat retinal cells against zinc toxicity in vitro, and pressure-induced ischemia in vivo. Invest. Ophthalmol. Vis. Sci. 45 (2004) 1523-1530
62. Samuelson D.A., Smith P., Ulshafer R.J., Hendricks D.G., Whitley R.D., Hendricks H., and Leone N.C. X-ray microanalysis of ocular melanin in pigs maintained on normal and low zinc diets. Exp. Eye Res. 56 (1993) 63-70
63. Boulton M., and Dayhaw-Barker P. The role of the retinal pigment epithelium: topographical variation and ageing changes. Eye 15 (2001) 384-389
64. Sarna T., Burke J.M., Korytowski W., Rozanowska M., Skumatz C.M., Zareba A., and Zareba M. Loss of melanin from human RPE with aging: possible role of melanin photooxidation. Exp. Eye Res. 76 (2003) 89-98
65. Larsson B.S. Interaction between chemicals and melanin. Pigment Cell Res. 6 (1993) 127-133
66. Feeney-Burns L., Hilderbrand E.S., and Eldridge S. Aging human RPE: morphometric analysis of macular, equatorial, and peripheral cells. Invest. Ophthalmol. Vis. Sci. 25 (1984) 195-200
67. Zareba M., Raciti M.W., Henry M.M., Sarna T., and Burke J.M. Oxidative stress in ARPE-19 cultures: do melanosomes confer cytoprotection?. Free Radic. Biol. Med. 40 (2006) 87-100
68. Tate D.J., Miceli M.V., Newsome D.A., Alcock N.W., and Oliver P.D. Influence of zinc on selected cellular functions of cultured human retinal pigment epithelium. Curr. Eye Res. 14 (1995) 897-903