Free Radicals and Antioxidants in the Pathogenesis of Eye Diseases

  • G. E. Marak
  • Y. de Kozak
  • J. P. Faure
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 264)

Abstract

The eye is uniquely exposed to, susceptible to and protected against the damaging effects of free radicals. The lens absorbs increasing amounts of ultra-violet light with aging.1 The eye is exposed to the photogeneration of free radicals by the photosensitization of reducing substances in the retina and the interaction of photosensitizers such as retinal with oxygen to generate singlet oxygen.2–4 The vertebrate retina consumes 5–10 times more oxygen per mg than any other tested tissue.5 Photoreceptors contain high concentrations of polyunsaturated fatty acids: for example compare the 50% concentration of docosahexanoic acid of retinal rod phospholipids to the 20% concentration found in vertebrate brain tissue.6–7.

Keywords

Glutathione Adenosine Disulfide Hydroperoxide Guanine 

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References

  1. 1.
    S. Lerman, Biophysical aspects of corneal and lenticular transparency, Curr. Eye Res. 3, 3–14 (1984).PubMedCrossRefGoogle Scholar
  2. 2.
    M. Delmelle, Generation of singlet oxygen by retinal, Photochem, Photobiol. 27, 731–734 (1978).CrossRefGoogle Scholar
  3. 3.
    A.A. Shvedova, O. Alekseeva, I.Y.Kuliev, K.O. Muranov, Y.P. Kozlov and V.E. Kagan, Damage of photoreceptor membrane lipids and proteins induced by photosensitized generation of singlet oxygen, Curr. Eye Res. 2, 683–689 (1983).CrossRefGoogle Scholar
  4. 4.
    J.L. Calkins and B.F. Hochheimer, Retinal light exposure from ophtalmoscopes, slit lamps and overhead surgical lamps, Invest. Ophthalmol. Vis. Sci. 19, 1009–1015 (1980) .PubMedGoogle Scholar
  5. 5.
    W. Sickel, Retinal metabolism in dark and light, in “The Handbook of Sensory Physiology”, 7, M. Fuortes, ed., Springer Verlag, Berlin, 667–727 (1972).Google Scholar
  6. 6.
    W.L. Stone, C.C. Farnsworth and E.A. Dratz, A reinvestigation of the fatty acid content of bovine, rat and frog retinal rod outer segments, Exp. Eye Res. ,28, 387–397 (1979).PubMedCrossRefGoogle Scholar
  7. 7.
    J. Tinoco, Dietary requirements and function of linolenic acid in animals, Prog. Lipid Res. ,21, 1–45 (1982).PubMedCrossRefGoogle Scholar
  8. 8.
    K.C. Bhuyan and D.K. Bhuyan, Molecular mechanism of cataractogenesis: Toxic metabolites of oxygen as initiators of lipid peroxidation and cataract, Curr. Eye Res., 3, 67–81 (1984).PubMedCrossRefGoogle Scholar
  9. 9.
    R. Fried and P. Mandel, Superoxide dismutase of bovine and frog rod outer segments, J. Neurochem. 24, 433–438 (1975) .PubMedCrossRefGoogle Scholar
  10. 10.
    D. Armstrong, B. Santangelo and F. Connole, The distribution of peroxide regulatory enzymes in the canine eye, Curr. Eye Res. ,1, 225–242 (1981).PubMedCrossRefGoogle Scholar
  11. 11.
    K.C. Bhuyan and D.C. Bhuyan, Regulation of hydrogen peroxide in eye humors. Effect of 3-amino 1-H, 1, 2, 4 triazole in catalase and glutathione peroxidase of rabbit eye, Biochem. Biophys. Acta 497, 641–651 (1977).PubMedCrossRefGoogle Scholar
  12. 12.
    W.L. Stone and E.A. Dratz, Selenium and non-selenium glutathione peroxidase activities in selected ocular and non-ocular rat tissues, Exp. Eye Res. 35, 405–412 (1982).PubMedCrossRefGoogle Scholar
  13. 13.
    N.A. Rao, L.G.Thaete, J.M. Delmage and A. Sevanian, Superoxide dismutase in ocular structures, Invest.Ophthalmol. Vis. Sci. ,26, 1778–1781 (1985).PubMedGoogle Scholar
  14. 14.
    F. Attala, M.A. Fernandez and N.A. Rao, Immunohistochemical localization of catalase in ocular tissue, Curr. Eye Res. ,6, 1181–1187(1987).CrossRefGoogle Scholar
  15. 15.
    L.R. Atalla, A. Sevanian and N.A. Rao, Immunohistochemical localization of glutathione peroxidase in ocular tissue, Curr. Eye Res. ,7, 1023–1028 (1988).PubMedCrossRefGoogle Scholar
  16. 16.
    L.R. Atalla, A. Sevanian and N.A. Rao, Hydrogen peroxide localization in ocular tissue, an electron microscopic cytochemical study, Curr. Eye Res. ,7, 931–936 (1988).PubMedCrossRefGoogle Scholar
  17. 17.
    H. Heath, The distribution and possible functions of ascorbic acid in the eye, Exp. Eye Res. ,1, 3 62–367 (1962).Google Scholar
  18. 18.
    M.O.M. Tso, A.J. Woodford and K.W. Lam, The distribution of ascorbate in the normal primate retina and after photic injury: A biochemical morphologic correlated study, Curr. Eye Res. ,3, 181–191 (1984).PubMedCrossRefGoogle Scholar
  19. 19.
    S.D. Varma, D. Chand, Y.R. Sharma, J.F. Kuch and R.D. Richards, Oxidative stress on the lens and cataract formation : Role of light and oxygen, Curr. Eye Res. ,3, 35–57 (1984).PubMedCrossRefGoogle Scholar
  20. 20.
    K. Kirschfeld, Carotenoid pigments : Their possible role in protection against photooxidation in eyes and photoreceptor cells, Proc. Roy Soc, London B. ,216, 71–85 (1982).CrossRefGoogle Scholar
  21. 21.
    J. Nishiyama, E.C. Ellison, G.R. Mizuno and J.R. Chipault, Microdetermination of a tocopherol in tissue lipids, J. Nutr. Sci. Vitaminol. 21, 355–361 (1975).PubMedCrossRefGoogle Scholar
  22. 22.
    D.F. Hunt, D.T. Organisciak, H.M. Wang and R.L. Wu, a tocopherol in the developing rat retina : A high pressure liquid Chromatographie analysis, Curr. Eye Res. ,3, 1281–1288 (1984).PubMedCrossRefGoogle Scholar
  23. 23.
    E.L. Paulter, J.A. Maga and A. Tengerdy, A pharmacologically potent natural product in the bovine retina, Exp. Eye Res. ,42, 285–288 (1986).CrossRefGoogle Scholar
  24. 24.
    J.J. Weiter and S. Subramanian, Free radicals produced in human lenses by a biphotonic process, Invest. Ophthalmol. Vis. Sci. ,17, 869–873 (1978).PubMedGoogle Scholar
  25. 25.
    A. Spector and W.H. Garner, Hydrogen peroxide and human cataract, Exp. Eye Res. ,33, 673–681 (1981).PubMedCrossRefGoogle Scholar
  26. 26.
    W.H. Garner, M.H. Garner and A. Spector, H2O2 induced uncoupling of bovine lens Na+, K+ ATPase, Proc. Natl. Acad. Sci. U.S.A. 80, 2044 (1983).PubMedCrossRefGoogle Scholar
  27. 27.
    S.D. Varma and J.M. Mooney, Photodamage to the lens in vitro: Implications of the Haber-Weiss reaction, Free Radical Biol. Med. ,2, 57–62 (1986).Google Scholar
  28. 28.
    S.D. Varma, V.K. Srivastava and R.D. Richards, Photoperoxidation in lens and cataract formation; Preventive role of Superoxide dismutase, catalase and vitamin C., Ophthalmic Res.14 ,167–175 (1982).PubMedCrossRefGoogle Scholar
  29. 29.
    S. Lerman, M. Jacoy and R.F. Borkman, Photosensitization of the lens by 8-methoxysporalen, Invest. Ophthalmol. Vis. Sci. 16, 1065–1068 (1977).PubMedGoogle Scholar
  30. 30.
    A. Spector and D. Roy, Disulfide linked high molecular weight protein associated with human cataract, Proc. Natl. Acad. Sci U.S.A. 75, 3244–3248 (1978).PubMedCrossRefGoogle Scholar
  31. 31.
    A. Spector, The search for a solution to senile cataracts. Invest.Ophthalmol. Vis. Sci. 25, 130–146 (1984).PubMedGoogle Scholar
  32. 32.
    A Taylor and K.V.A. Davies, Protein oxidation and loss of protease activity may lead to cataract formation in the aged lens, Free Radical Biol. Med. 3, 371–377 (1987).CrossRefGoogle Scholar
  33. 33.
    C.Ohrloff, O.Hockwin, R.O. Olsen and S. Dickman, Glutathione peroxidase, glutathione reductase and Superoxide dismutase in the aging lens, Curr. Eye Res. 3, 109–116 (1984).PubMedCrossRefGoogle Scholar
  34. 34.
    F. Giblin and J. Mc-Cready. The effect of inhibition of glutathione reductase on detoxification of H2O2 by rabbit lens, Invest. Ophthalmol. Vis. Sci. 24, 113–118 (1983).PubMedGoogle Scholar
  35. 35.
    N. Orzalesi, R.Sorcinelli and G. Guiso, Increased incidence of cataracts in male subjects deficient in glucose-6-phosphate dehydrogenase, Arch. Ophthalmol. 99, 69–71 (1981).PubMedCrossRefGoogle Scholar
  36. 36.
    S.K. Srivastava, H.H. Ansari and Y.C. Awasthi, Lens glutathione depletion of 1-chloro-2,4 dinitrobenzene and oxidative stress, Curr. Eye Res. 3, 112–119 (1984).CrossRefGoogle Scholar
  37. 37.
    H.H. Ansari, A. Schulter and S.K.Srivastava, Antioxidant (BHT) significantly delays galactose cataract formation in rats, Invest. Ophthalmol. Vis. Sci. 28 (Suppl.), 192 (1987) .Google Scholar
  38. 38.
    S.Zigman and W.Vaughn, Near U-V light effects on the lenses and retinas of mice, Invest. Ophthalmol. 13, 462–465 (1974).PubMedGoogle Scholar
  39. 39.
    S. Lerman, Human U-V radiation cataracts, Ophthalmic Res. 12, 303–314 (1980).CrossRefGoogle Scholar
  40. 40.
    S.Duke-Elder and P.A. Mac-Faul, “System of Ophthalmology” Vol.9, Kimpton, London, 985–1001(1972).Google Scholar
  41. 41.
    S.S. Schocket, J.Esterson, B. Bradford, M. Michaelis and R.D. Richards, Induction of cataracts in mice by exposure to oxygen, Isr. J. Med. Sci. 8, 1596–1601 (1972).PubMedGoogle Scholar
  42. 42.
    A. Pirie and J.N. Rees, Diquat cataract in the rat, Exp Eye Res. 9, 198–203 (1970).PubMedCrossRefGoogle Scholar
  43. 43.
    F. Hollows and D. Moran, Cataract- The ultraviolet risk factor, Lancet 2 ,1249–1250 (1981).PubMedCrossRefGoogle Scholar
  44. 44.
    L.B. Brilliant, N.C. Grassett, R.P. Pokhrel, A. Kolstad, J.M. Lepkowski, G.E. Brilliant, W.N. Hawkes and R. Parajosegaram, Associations among cataract prevalence, sunlight and altitude in the Himalayas, Am. J. Epidemiol. 118, 250–264 (1983).PubMedGoogle Scholar
  45. 45.
    R. Hiller, R.D. Spurduto and F. Ederer, Epidemiologie associations with cataract in the 1971–1972 National Health and Nutrition Survey, Am. J. Epidemiol. 118, 239–249 (1983).PubMedGoogle Scholar
  46. 46.
    J.L. Calkins, B.F. Hockheimer and S.A. D’Anna, Potential hazards from specific ophtalmic devices, Vision Res. 20, 2039–2053 (1980).CrossRefGoogle Scholar
  47. 47.
    J.L. Calkins and B.F. Hockheimer, Retinal light exposure from operating microscopes, Arch. Ophthalmol. 97, 23 63–2367 (1979).Google Scholar
  48. 48.
    H.R. McDonald and A.R. Irvine, Light induced maculopathy from the operating microscope in extracapsular cataract extraction and intraocular lens implantation, Ophthalmology 90, 945–951, (1983).PubMedGoogle Scholar
  49. 49.
    D.M. Robertson and R.B. Feldman, Photic retinopathy from the operating microscope, Am. J. Ophthalmol. 101, 561–569 (1986).PubMedGoogle Scholar
  50. 50.
    M.O.M. Tso, “Retinal Diseases”, Lippincott, Philadelphia, 187–214 (1988).Google Scholar
  51. 51.
    M.O.M. Tso, Pathogenic factors of aging macular degeneration, Ophthalmology 92, 628–635 (1985).PubMedGoogle Scholar
  52. 52.
    F.L. Ferris, Senile macular degeneration : Review of epidemiologic features, Am. J. Epidemiol. ,118, 132–1 51(1983).PubMedGoogle Scholar
  53. 53.
    L.G. Hayman, Senile macular degeneration : A case control study, Am. J. Epidemiol. 118, 213–227 (1983).Google Scholar
  54. 54.
    J. Von der Hoeve, Eye lesions produced by light rich in ultraviolet rays, senile cataract, senile degeneration of the macula, Am. J. Ophthalmol.3, 178–194 (1920).Google Scholar
  55. 55.
    H.G.A. Gjessing, Is there an antagonism between senile cataract and senile macular degeneration?, Acta Ophthalmol. 31, 401–421 (1953).Google Scholar
  56. 56.
    W.K. Noell, There are different kinds of retinal light damage in the rat, in “The Effects of Constant Light on the Visual Process”, T. Williams and B. Baker eds., Plenum Press, New-York, 3–28 (1980).Google Scholar
  57. 57.
    W.T. Ham, Jr., J.J. Ruffolo, H.A. Mueller, A.M.Clark and M.E. Moore, Histologie analysis of photochemical lesions produced in rhesus retina by short-wavelength light, Invest. Ophthalmol. Vis. Sci. 17, 1029–1035 (1978).PubMedGoogle Scholar
  58. 58.
    W.T. Ham, Jr., J.J. Ruffolo, H.A. Mueller, D. Guerry, The nature of retinal light damage. Dependence on wave length, power level and exposure time, Vision Res. 20, 1105–1111 (1980).PubMedCrossRefGoogle Scholar
  59. 59.
    W.T. Ham, H.A. Mueller, Retinal sensitivity to damage from short wave length light, Nature ,253–255 (1976).Google Scholar
  60. 60.
    J.J. Wolken, Biophysics and biochemistry of the retinal photoreceptors, in “Vision” : Thomas, Springfield, 52–61 (1966).Google Scholar
  61. 61.
    W.K. Noell, V.S. Walker, B.S. Kang and S. Berman, Retinal damage by light in rats, Invest. Ophthalmol. 5, 450–463 (1966).PubMedGoogle Scholar
  62. 62.
    R.J. Wiegland, N.M. Giusto, L.M.Rapp and R.E. Anderson, Evidence for rod outer segment lipid peroxidation following constant illumination of the rat retina, Invest. Ophthalmol. Vis. Sci. 24, 1433–1435 (1983).Google Scholar
  63. 63.
    V.E. Kagan, “Lipid Peroxidation in Biomembranes”, CRC Press, Boca Raton, 139–140 (1988).Google Scholar
  64. 64.
    W.L. Stone, M.L. Katz, M. Lurie, M.M. Marmor and E.A. Dratz, Effects of dietary vitamin E and selenium on light damage to the rat retina, Photochem. Photobiol. 29, 725–730 (1979).PubMedCrossRefGoogle Scholar
  65. 65.
    V.E. Kagan, I.Y. Kuliev, V.B., Spiriche , A.D.Shvedova and Y.P. Kozlov, Accumulation of lipid peroxidation products and depression of electrical activity in vitamin E deficient rats exposed to high intensity light, Bull. Exp. Biol. Med. 91, 144–147.Google Scholar
  66. 66.
    G.J. Handleman and E.A. Dratz, The role of antioxidants in the retina and retinal pigment epithelium and the nature of prooxidant-induced damage, Free Radical Biol. Med. 2, 1–90 (1986).Google Scholar
  67. 67.
    J. Weiter, E. Dratz, K. Fitch and G. Handleman, Role of selenium nutrition in senile macular degeneration, Invest. Ophthalmol. Vis. Sci. 26, (suppl.) 58 (1985).Google Scholar
  68. 68.
    D.T. Organisciak, H.M. Wang, Z.Y. Li and M.O.M. Tso, The protective effect of ascorbate in retinal light damage of rats, Invest. Ophthalmol. Vis. Sci. 26, 2580–2588 (1985).Google Scholar
  69. 69.
    Z.Y. Li, M.O.M. Tso, H.M. Wang and D.T. Organisciak, The amelioration of photic injury in rat retina by ascorbic acid, a histopathologic study, Invest. Ophthalmol. Vis. Sci. 26, 1589–1598 (1985).PubMedGoogle Scholar
  70. 70.
    W.T. Ham, H.A. Mueller, J.J. Ruffolo, Jr, J.E. Millen, S.F. Cleary, R.K. Guerry and D. Guerry, III, Basic mechanism underlying the production of photochemical lesions in the mammalian retina, Curr. Eye Res. 3, 165–174 (1984).PubMedCrossRefGoogle Scholar
  71. 71.
    T.W. Sery and R. Petrillo, Superoxide anion radical as an indirect mediator in ocular inflammatory disease, Curr. Eye Res. 3, 243–252 (1984).PubMedCrossRefGoogle Scholar
  72. 72.
    D. Armstrong, T. Hiramitsu, J. Gutteridge and S.E Nilsson, Studies on experimentally induced retinal degeneration; Effects of lipid peroxides on electroretinographic activity in the albino rabbit, Exp. Eye Res. 35, 157–171 (1982) .PubMedCrossRefGoogle Scholar
  73. 73.
    W.K. Noell, Metabolic injuries of the visual cell, Am.J. Ophthalmol. 40, 60–68 (1955).PubMedGoogle Scholar
  74. 74.
    C.C. Beehler, N.L. Newton, J.F. Culver and T.J. Tredici, Retinal detachment in dogs resulting from oxygen toxicity, Arch. Ophthalmol. 71, 665–670 (1964).PubMedCrossRefGoogle Scholar
  75. 75.
    W.K. Noell, Studies on visual cell viability and differenciation, Ann. N.Y. Acad. Sci. 74, 337–361 (1958).CrossRefGoogle Scholar
  76. 76.
    C.W. Nichols and C.J. Lambertson, Effects of high oxygen pressures on the eye, N. Eng. J. Med. 281, 25–30 (1969).CrossRefGoogle Scholar
  77. 77.
    C.C. Beehler and W. Roberts, Experimental retinal detachment induced by oxygen and phenothiazines, Arch. Ophthalmol. 79, 759–762 (1968).PubMedCrossRefGoogle Scholar
  78. 78.
    P.A. Libis and T. Yamashita, Experimental aspects of ocular siderosis, Am. J. Ophthalmol. 48, 465–479 (1959).Google Scholar
  79. 79.
    A.M. Roth, R.Y. Foos, Ocular pathologic changes in primary hemochromatosis, Arch. Ophthalmol. 87, 507–514 (1972).PubMedCrossRefGoogle Scholar
  80. 80.
    R.E. Anderson, L.M. Rapp and R.D. Wiegand, Lipid peroxidation and retinal degeneration, Curr. Eye Res. 3, 223–228 (1984) .PubMedCrossRefGoogle Scholar
  81. 81.
    J. Legros, I.Rosner and C.Berger, Influence du niveau d’éclairement ambiant sur les modifications oculaires induites par l’hydroxychloroquine chez le rat, Arch. Ophtalmol. (Paris) 33, 417–424 (1973).Google Scholar
  82. 82.
    S.Lerman, K. Megaw, Y.U. Gardner, Y.Tadei, Y.Franks and Gammon, Photobinding of 3H 8-methoxypsoralen to monkey intracular tissues, Invest. Ophthalmol. Vis. Sci. 25, 1267–1274 (1984).PubMedGoogle Scholar
  83. 83.
    J.Winther and N. Ehlers, The combined effect of hematoporphyrin derivative and light on the normal mouse retina, Arch. Ophthalmol. 62, 112–122 (1984).Google Scholar
  84. 84.
    C.J. Gomer, D.R. Dorion, L. While, J.V. Jester, S. Dunn, B.C. Szirth, J.J. Razum and A.L. Murphee, Hematoporphyrin derivative photoradiation induced damage to normal and tumor tissue of the pigmented rabbit eye, Curr. Eye Res. 3, 229–237 (1984).PubMedCrossRefGoogle Scholar
  85. 85.
    S.J. Weiss and P.A. Ward, Immune complex induced generation of oxygen metabolites by human neutrophils. J. Immunol. 129, 209–213 (1982).Google Scholar
  86. 86.
    K.J. Johnson and P.A. Ward, Role of oxygen metabolites in immune complex injury of the lung, J. Immunol. 126, 2365–2369 (1981).PubMedGoogle Scholar
  87. 87.
    A. Rehan, K.J. Johnson, R.C. Wiggins, R.G. Kunkel, P.A. Ward, Evidence for the role of oxygen metabolites in acute nephrotoxic nephritis, Lab. Invest. 51, 39 6–403 (1984).Google Scholar
  88. 88.
    G.E. Marak, N.A. Rao, J.M. Scott, R. Duque and P.A. Ward, Free radicals and phacoanaphylaxis, in “Advances in Immunology and Immunopathology of the Eye”,G. R. O’Connor and J. Chandler, eds., Masson, New York, 144–145 (1985).Google Scholar
  89. 89.
    B.M. Babior, Oxygen dependent microbial killing by phagocytes, New England J. Med. 298, 659–668 (1978).CrossRefGoogle Scholar
  90. 90.
    C. Nathan and Z. Cohn, Role of oxygen dependent mechanisms in antibody induced lysis of tumor cells by activated macrophages, J. Exp. Med. 152,198–208 (1980).PubMedCrossRefGoogle Scholar
  91. 91.
    I. Fridovich, Oxygen radicals, hydrogen peroxide and oxygen toxicity, in “Free Radicals in Biology”, W. Pryor, ed., Academic Press, New York, 259–277 (1976).Google Scholar
  92. 92.
    S.J. Klebanoff, Oxygen dependent cytotoxic mechanisms of phagocytes, in “Advances in Host Defense Mechanisms”, R. Galin and A. Fauci, eds. Vol 1. Phagocytic cells, 111–162, Raven Press, New York (1982).Google Scholar
  93. 93.
    B.A. Freeman and V.S. Crapo, Free radicals and tissue injury, Lab.Invest. 47, 412–426 (1982).PubMedGoogle Scholar
  94. 94.
    S.J. Weiss and A.F. LoBuglio, Phagocyte-generated oxygen metabolites and cellular injury, Lab. Invest. 44, 5–18 (1982).Google Scholar
  95. 95.
    T.W. Mittag, Role of free radicals in ocular inflammation and cellular damage, Exp. Eye Res. 39, 759–767 (1984).PubMedCrossRefGoogle Scholar
  96. 96.
    T.W. Mittag, B.R. Hammond, K.E. Eakins and P. Bhattacherjee, Ocular responses to Superoxide generated by intraocular injection of xanthine oxidase, Exp. Eye Res. 40, 411–419 (1985).PubMedCrossRefGoogle Scholar
  97. 97.
    L. Feeney and E.R. Berman, Oxygen toxicity : Membrane damage by free radicals, Invest. Ophthalmol. 15, 7 89–7 92 (1976).Google Scholar
  98. 98.
    T.W. Sery, A.W. Vogel, R. Folberg and R. Petrillo, Oxygen free radicals in ocular inflammatory disease, in “Uveitis Update”, K.M. Saari, ed., Elsevier Science Publishers, Amsterdam, 39–45 (1984).Google Scholar
  99. 99.
    J. Guy, E.A. Ellis, G.M. Hope and N.A. Rao, Influence of anti-oxidant enzymes in reduction of optic disc edema in experimental optic neuritis, Free Radical Biol. Med. 2, 349–351 (1986).CrossRefGoogle Scholar
  100. 100.
    W.B. Wacker, N.A. Rao and G.E. Marak, Experimental sympathetic ophthalmia, in “Immunology and Immunopathology of the Eye”, A.M. Silverstein and G.R. O’Connor,eds, Masson, New York, 121–126 (1979).Google Scholar
  101. 101.
    G.E. Marak, R.L. Font, L.N. Czawlytko and F.P. Alepa, Experimental lens induced granulomatous endophtalmitis : Preliminary histopathologic observations, Exp. Eye Res. 19, 311–16 (1974).PubMedCrossRefGoogle Scholar
  102. 102.
    N.A. Rao, W.B. Wacker and G.E. Marak, Experimental allergic uveitis : Clinicopathologic features associated with varying doses of S-antigen, Arch. Ophthalmol. 97, 1954–1958 (1979).PubMedCrossRefGoogle Scholar
  103. 103.
    J.P. Faure, Autoimmunity and the retina, Curr. Topics Eye Res. 2, 215–302 (1980).Google Scholar
  104. 104.
    G.E. Marak, W.B. Wacker, N.A. Rao, R. Jack, and P.A. Ward, Effect of complement depletion on experimental allergic uveitis, Ophthalmic Res. 11, 97–107 (1979).CrossRefGoogle Scholar
  105. 105.
    G.E. Marak, R.L. Font, and N.A. Rao, Strain differences in autoimmunity to lens protein, Ophthalmic Res. 13, 320–329 (1981).CrossRefGoogle Scholar
  106. 106.
    G.E. Marak, N.A. Rao, G. Antonakou and A. Slewinski, Experimental lens-induced granulomatous endophthalmitis in common laboratory animals, Ophthalmic Res. 14, 292–297 (1982).PubMedCrossRefGoogle Scholar
  107. 107.
    G.E. Marak, Abrogation of tolerance to lens protein, in “New Directions in Ophtalmic Research”,M. Sears, ed., Yale Univ. Press, New Haven, 47–61 (1981).Google Scholar
  108. 108.
    G.E. Marak, R.L. Font and F.P. Alepa, Arthus-type panophtalmitis in rats sensitized to heterologous lens protein, Ophthalmic Res., 162–170 (1977).Google Scholar
  109. 109.
    G.E. Marak, N.A. Rao, (unpublished observations).Google Scholar
  110. 110.
    N.A. Rao, A.J. Calandra, A. Sevanian, B. Bowe, J.A. Delmage and G.E. Marak, Modulation of lens induced uveitis by Superoxide dismutase, Ophthalmic Res. 18, 41–46 (1986).PubMedCrossRefGoogle Scholar
  111. 111.
    N.A. Rao, M.A. Fernandez, A. Sevanian, G.O. Till and G.E. Marak, Antiphlogistic effect of catalase on experimental phocoanaphylactic endophthalmitis, Ophthalmic Res. 18, 185–191 (1986) .PubMedCrossRefGoogle Scholar
  112. 112.
    N.A. Rao, B.E. Bowe, A. Sevanian, G.O. Till and G.E. Marak, Modulation of lens induced uveitis by dimethyl sulfoxide, Ophthalmic Res. 18, 193–198 (1986).PubMedCrossRefGoogle Scholar
  113. 113.
    N.A. Rao, J.L. Romero, M.A. Fernandez, A. Sevanian and G.E. Marak, Effect of iron chelation on severity of ocular inflammation in an animal model, Arch. Ophthalmol. 104, 1369–1371 (1986) .PubMedCrossRefGoogle Scholar
  114. 114.
    N.A. Rao, A. Sevanian, M.A. Fernandez, J.L. Romero, J.P. Faure, Y. de Kozak, G.O. Till and G.E. Marak, Role of oxygen radicals in experimental allergic uveitis, Invest. Ophthalmol. Vis Sci. 28, 886–892 (1987).PubMedGoogle Scholar
  115. 115.
    N.A. Rao, J.L. Romero, A. Sevanian, M.A. Fernandez, C. Wang, P.A. Ward and G.E. Marak, Anti-inflammatory effect of glutathione peroxidase on experimental lens induced uveitis, Ophtalmic Res. 20, 106–11 (1988).CrossRefGoogle Scholar
  116. 116.
    N.A. Rao, M.A. Fernandez, A. Sevanian, J.L. Romero, G.O. Toll and G.E. Marak, Treatment of experimental lensinduced uveitis by dimethylthiourea, Ophthalmic Res. 20, 106–111 (1988).PubMedCrossRefGoogle Scholar
  117. 117.
    G.E. Marak, N.A. Rao, J.M. Scott, R. Duque and P.A. Ward, Free radicals and phocoanaphylaxis, in “Advances in Immunology and Immunopathology of the Eye”, G.R. O’Connor and J. Chandler, eds, Masson, New York, 144–145 (1985).Google Scholar
  118. 118.
    Y. de Kozak, J.P. Nordmann, J.P. Faure, N.A. Rao and G.E. Marak, The effect of anti-oxidant enzymes on experimental uveitis in rats, Ophthalmic Res. (in press).Google Scholar
  119. 119.
    G.E. Marak, N.A. Rao, A. Sevanian, V. Zdravkovich, G.O. Till and P.A. Ward, Modulation of experimental phacoanaphylactic endophthalmitis with the anti-oxidants sodium benzoate and 2,3,dihydroxybenzoic acid, Ophthalmic Res. 19, 120–128 (1987).PubMedCrossRefGoogle Scholar
  120. 120.
    J.A. Badway and J.L. Karnovsky, Production of Superoxide by phagocytic leukocytes: A paradigm for stimulus response phenomena, Curr. Topics in Cell Regulation 28, 183–208 (1986) .Google Scholar
  121. 121.
    S.L. Kunkel, J.C. Fantone, P.A. Ward and R.B. Zurier, Modulation of inflammatory reactions by prostaglandins, Prog. Lipid Res. 20, 633–640 (1981).PubMedCrossRefGoogle Scholar
  122. 122.
    G.O. Till and P.A. Ward (unpublished observations).Google Scholar
  123. 123.
    G.E. Marak, Y. de Kozak, J.P. Faure, N.A. Rao, J.L. Romero, P.A. Ward and G.O. Till, Pharmacological modulation of acute ocular inflammation I. Adenosine, Ophthalmic Res. 20, 220–226 (1988).PubMedCrossRefGoogle Scholar
  124. 124.
    B.N. Cronstein, S.G. Kramer, B. Weissman, R. Hirschorn, Adenosine : A physiologic modulation of Superoxide anion generation of human neutrophils, J. Exp. Med. 158, 1160–1177 (1983).PubMedCrossRefGoogle Scholar
  125. 125.
    G.O. Till and P.A. Ward, (unpublished observations).Google Scholar
  126. 126.
    S. Cockcroft and B.D. Gambers, The role of guanine nuceotide binding protein in the activation of phosphoinositide phosphodiesterase, Nature ,314, 534–536 (1985).PubMedCrossRefGoogle Scholar
  127. 127.
    A.G. Gilman, G-proteins and dual control of adenylate cyclase, Cell 36, 557–579 (1984).CrossRefGoogle Scholar
  128. 128.
    K. Kraus, W. Schlagel, C. Wollheim, T. Anderson, F. Waldvogel and P. Lew, Chemotactic peptide activation of human neutrophils and HL-60 cells, J. Clin. Invest. 76, 1348–1354 (1985).CrossRefGoogle Scholar
  129. 129.
    T. Matsumoto, T. Molski, C. Valpi, Y. Pelz, Y. Kanako, E.L. Becker, M. Feinstein, P. Naccache and R. Saafi, Treatment of rabbit neutrophils with phorbol esters results in increased ADP ribosylation catalyzed by pertussis toxin and inhibition of the GTPase stimulated by F-met-leu-phe, FEBS Lett. 198, 295–300 (1986).PubMedCrossRefGoogle Scholar
  130. 130.
    T. Molski, P. Naccache, M. Marsh, J. Germode, E. Becker and R. Saafi, Pertussis toxin inhibits the rise in the intracellular concentration of free calcium that is induced by chemotactic factors in rabbit neutrophils : Possible role of the G-proteins in calcium mobilization, Biochem. Biophys. Res. Comm. 121, 644–650 (1984).CrossRefGoogle Scholar
  131. 131.
    M.W. Verghese, C.D. Smith and R. Snyderman, Potential role for a guanine nucleotide regulatory protein in chemoattractant receptor mediated polyphosphoinositide metabolism, Ca++ mobilization and cellular response by leukocytes, Biochem. Biophys. Res. Comm. 127, 450–457 (1985).PubMedCrossRefGoogle Scholar
  132. 132.
    G.E. Marak et al (unpublished observations).Google Scholar
  133. 133.
    G.E. Marak, P.A. Ward and G.O. Till (unpublished observations).Google Scholar
  134. 134.
    S.T. Tamara, Y. Nakanisi, A. Kojima, M. Otokawa, N. Uchida, H. Sato and Y. Sato, Effect of pertussis toxin (Pt) on T cell populations sensitized for delayed-type hypersensitivity in mice, Cell. Immunol. 85, 3 51–363 (1984).Google Scholar
  135. 135.
    G.J. Spangrude, B.A. Araneo and R.A. Daynes, Site selected homing of antigen primed lymphocyte population can play a critical role in the efferent limb of cell mediated immune responses in vivo. J. Immunol. 134, 29 002907 (1985).Google Scholar
  136. 136.
    B.D. Cheson, R.L. Christenson and R. Sperling, The origin of the chemiluminescence of phagocytosing granulocytes, J. Clin. Invest. 58, 789–796 (1976).PubMedCrossRefGoogle Scholar
  137. 137.
    J.G. Bender and D.E. Van Epps, Inhibition of human neutrophil function by-6-aminonicotinamide : The role of the hexose monophosphate shunt in cell activation, Immunopharmacol. 10, 191–199 (1985).CrossRefGoogle Scholar
  138. 138.
    G.E. Marak et al. (unpublished observations).Google Scholar
  139. 139.
    S.J. Berger, I. Manory, D.C. Sudar, D. Krothapalli and D. Berger, Pyridine nucleotide analog interference with metabolic processes in mitogen stimulated human T lymphocytes, Exp. Cell. Res. 173, 389–387 (1987).Google Scholar
  140. 140.
    C. Pagonis, A.I. Tauber, N. Pavlotsky and E.R. Simons, Flavinoid impairment of neutrophil response, Biochem. Pharmacol. 35, 237–245 (1985).CrossRefGoogle Scholar
  141. 141.
    A.I. Tauber, J.R. Fay, M.A. Marietta, Flavinoid inhibition of the human neutrophil NADPH-oxidase, Biochem. Pharmacol.,33, 1367–1369 (1984).PubMedCrossRefGoogle Scholar
  142. 142.
    G. Berton, C. Schneider and D. Romeo, Inhibition by quercetin of activation of polymorphonuclear leukocyte functions : Stimulus-specific effects, Biochem. Biophys. Äcta. 595, 47–56 (1980).PubMedCrossRefGoogle Scholar
  143. 143.
    T. Iizuka, S. Kanegasaki, R. Makino, T. Tanaka and Y. Ishimura, Pyridine and imidazole reversibly inhibit the respiratory burst of porcine and human neutrophils, Biochem. Biophys. Res. Comm. 30, 621–626 (1985).CrossRefGoogle Scholar
  144. 144.
    J. Romero, G.E. Marak and N.A. Rao, Pharmacologic modulation of acute ocular inflammation with quercetin, Ophthalmic Res. (in press).Google Scholar
  145. 145.
    G.E. Marak et al. (unpublished observations).Google Scholar
  146. 146.
    W.W. Busse, D.E. Kopp, E. Middleton, Flavinoid modulation of human neutrophil function, J. Allerg. Clin. Immunol. 73, 801–09 (1984)CrossRefGoogle Scholar
  147. 147.
    G.O. Till and P.A. Ward (unpublished observations).Google Scholar
  148. 148.
    H.A. Kahn and H.B. Moorehead, Statistics on blindness in the model reporting area 19 69–1970, DHEQ Publication No (NIH) 73–427.Google Scholar

Copyright information

© Plenum Press, New York 1990

Authors and Affiliations

  • G. E. Marak
    • 1
  • Y. de Kozak
    • 2
  • J. P. Faure
    • 2
  1. 1.Center for SightGeorgetown UniversityUSA
  2. 2.Unité de Recherche d’OphtalmologieINSERM U 86ParisFrance

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