Age-Related Retinal Degeneration in Animal Models of Aging: Possible Involvement of Taurine Deficiency and Oxidative Stress

Neurochemical Research volume 29, pages151–160(2004)Cite this article

Abstract

There is strong evidence that the retina degenerates with age. Electroretinogram deficits and photoreceptor cell death and structural abnormalities have been observed in both animal and human studies of aging. The mechanism behind this phenomenon is a very interesting area for scientific and medical study. Current data support the link between retinal degeneration and increased oxidative stress. Taurine is a free amino acid found in high millimolar concentrations in the retina, and age-related deficiency in retinal levels of taurine may contribute to the retinal degeneration associated with age. Taurine acts as an antioxidant and taurine replenishment is known to alleviate oxidative stress in the retina. Thus taurine supplementation may be useful in the treatment of age-related retinal dysfunction.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

REFERENCES

  1. 1.

    Huxtable, R. J. 1992. Physiological actions of taurine. Physiol. Rev. 72:101–163.

    Google Scholar 

  2. 2.

    Huxtable, R. J. 1989. Taurine in the central nervous system and the mammalian actions of taurine. Prog. Neurobiol. 32:471–533.

    Google Scholar 

  3. 3.

    Sturman, J. A. 1981. Origin of taurine in developing rat brain. Brain Res. 254:111–128.

    Google Scholar 

  4. 4.

    Huxtable, R. J. and Sebring, L. A. 1986. Towards a unifying theory for the actions of taurine. TIPS. 7:481–485.

    Google Scholar 

  5. 5.

    Wallace, D. R. and Dawson, R., Jr. 1990. Decreased plasma taurine in aged rats. Gerontology 36:19–27.

    Google Scholar 

  6. 6.

    Dawson, R., Jr. and Wallace, D. R. 1992. Taurine content in tissues from aged Fischer 344 rats. Age. 15:73–81.

    Google Scholar 

  7. 7.

    Dawson, R., Jr., Liu, S., Eppler, B., and Patterson, T. 1999. Effects of dietary taurine supplementation or deprivation in aged male Fischer 344 rats. Mech. Ageing Dev. 107:73–91.

    Google Scholar 

  8. 8.

    Corman, B., Pratz, J., and Puojeol, P. 1985. Changes in anatomy, glomerular filtration, and solute excretion in aging rat kidney. Am. J. Physiol. 248:R282–R287.

    Google Scholar 

  9. 9.

    Dawson, R., Jr., Eppler, B., Patterson, T. A., Shih, D., and Liu, S. 1996. The effects of taurine in a rodent model of aging. Adv. Exp. Med. Biol. 403:37–50.

    Google Scholar 

  10. 10.

    Eppler, B. and Dawson, R., Jr. 2001. Dietary taurine manipulations in aged male Fischer 344 rat tissue: Taurine concentration, taurine biosynthesis, and oxidative markers. Biochem. Pharmacol. 62:29–39.

    Google Scholar 

  11. 11.

    Banay-Schwartz, M., Lajtha, A., and Palkovits, M. 1989. Changes with aging in the levels of amino acids in rat CNS structural elements: II. Taurine and small neutral amino acids. Neurochem. Res. 14:563–570.

    Google Scholar 

  12. 12.

    Eppler, B. and Dawson, R., Jr. 1999. Cysteine sulfinate decarboxylase and cysteine dioxygenase activities do not correlate with strain-specific changes in hepatic and cerebellar taurine content in aged rats. Mech. Ageing Dev. 110:57–72.

    Google Scholar 

  13. 13.

    Benedetti, M. S., Russo, A., Marrari, P., and Dostert, P. 1991. Effects of ageing on the content in sulfur-containing amino acids in rat brain. J. Neural. Transm. Gen. Sect. 86:191–203.

    Google Scholar 

  14. 14.

    Dawson, R., Jr., Pelleymounter, M. A., Cullen, M. J., Gollub, M., and Liu, S. 1999. An age-related decline in striatal taurine is correlated with a loss of dopaminergic markers. Brain Res. Bull. 48: 319–324.

    Google Scholar 

  15. 15.

    Yeung, J. M. and Friedman, E. 1991. Effect of aging and diet restriction on monoamines and amino acids in cerebral cortex of Fischer-344 rats. Growth Dev. Aging 55:275–283.

    Google Scholar 

  16. 16.

    Benuck, M., Banay-Schwartz, M., DeGuzman, T., and Lajtha, A. 1995. Effect of food deprivation on glutathione and amino acid levels in brain and liver of young and aged rats. Brain Res. 678:259–264.

    Google Scholar 

  17. 17.

    Massie, H. R., Williams, T. R., and DeWolfe, L. K. 1989. Changes in taurine in aging fruit flies and mice. Exp. Gerontol. 24:57–65.

    Google Scholar 

  18. 18.

    Tohgi, H., Takahashi, S., and Abe, T. 1993. The effect of age on concentrations of monoamines, amino acids, and their related substances in the cerebrospinal fluid. J. Neural. Transm. Park. Dis. Dement. Sect. 5:215–226.

    Google Scholar 

  19. 19.

    Lepage, N., McDonald, N., Dallaire, L., and Lambert, M. 1997. Age-specific distribution of plasma amino acid concentrations in a healthy pediatric population. Clin. Chem. 43:2397–2402.

    Google Scholar 

  20. 20.

    Chih-Kuang, C. Shuan-Pei, L., Shyue-Jye, L, and Tuan-Jen, W. 2002. Plasma free amino acids in Taiwan Chinese: The effect of age. Clin. Chem. Lab. Med. 40:378–382.

    Google Scholar 

  21. 21.

    Heinamaki, A. A. 1988. Endogenous synthesis of taurine and GABA in rat ocular tissues. Acta Chem. Scand. 42:39–42.

    Google Scholar 

  22. 22.

    Saransaari, P. and Oja, S. S. 1992. Taurine transport in the mouse cerebral cortex during development and ageing. Adv. Exp. Med. Biol. 315:215–220.

    Google Scholar 

  23. 23.

    Macaione, S., Ruggeri, P., De Luca, F., and Tucci, G. 1974. Free amino acids in developing rat retina. J. Neurochem. 22:887–891.

    Google Scholar 

  24. 24.

    Voaden, M. J., Lake, N., Marshall, J., and Morjaria, B. 1977. Studies on the distribution of taurine and other neuroactive amino acids in the retina. Exp. Eye Res. 25:249–257.

    Google Scholar 

  25. 25.

    Altshuler, D., Lo Turco, J. J., Rush, J., and Cepko, C. 1993. Taurine promotes the differentiation of a vertebrate retinal cell type in vitro. Development 119:1317–1328.

    Google Scholar 

  26. 26.

    Militante, J. D. and Lombardini, J. B. 2002. Taurine: Evidence of physiological function in the retina. Nutr. Neurosci. 5:75–90.

    Google Scholar 

  27. 27.

    Macaione, S., Tucci, G., and Di Giorgio, R. M. 1975. Taurine distribution in rat tissues during development. Ital. J. Biochem. 24:162–174.

    Google Scholar 

  28. 28.

    Baskin, S. I., Cohn, E. M. and Kocsis, J. 1977. The effect of age on taurine levels in eye tissues. Exp. Eye Res. 24:315–319.

    Google Scholar 

  29. 29.

    Parmer, R., Sheikh, K. H., Dawson, W. W., and Toskes, P. 1982. A parallel change of taurine and the ERG in the developing rat retina. Comp. Biochem. Physiol. 72:109–111.

    Google Scholar 

  30. 30.

    Rapp, L. M., Tolman, B. L., Koutz, C. A. and Thum, L. A. 1990. Predisposing factors to light-induced photoreceptor cell damage: Retinal changes in maturing rats. Exp. Eye Res. 51:177–184.

    Google Scholar 

  31. 31.

    Gupta, K., and Mathur, R. L. 1982. Taurine in development and aging of ocular tissues. Exp. Eye Res. 34:835–839.

    Google Scholar 

  32. 32.

    Delbarre, B., Delbarre, G., and Calinon, F. 1996. Taurine in gerbil retina: Changes during ischemia reperfusion/insult (I.R.I.) and aging. J. Ocul. Pharmacol. Ther. 12:65–73.

    Google Scholar 

  33. 33.

    Wright, C. E., Williams, D. E., Drasdo, N., and Harding, G. F.1985. The influence of age on the electroretinogram and visual evoked potential. Doc. Ophthalmol. 59:365–384.

    Google Scholar 

  34. 34.

    Brecelj, J., Strucl, M., Zidar, I., and Tekavcic-Pompe, M. 2002. Pattern ERG and VEP maturation in schoolchildren. Clin. Neurophysiol. 113:1764–1770.

    Google Scholar 

  35. 35.

    Weleber, R. G. 1981. The effect of age on human cone and rod ganzfeld electroretinograms. Invest. Ophthalmol. Vis. Sci. 20: 392–399.

    Google Scholar 

  36. 36.

    Birch, D. G., Hood, D. C., Locke, K. G., Hoffman, D. R., and Tzekov, R. T. 2002. Quantitative electroretinogram measures of phototransduction in cone and rod photoreceptors: normal aging, progression with disease, and test-retest variability. Arch. Ophthalmol. 120:1045–1051.

    Google Scholar 

  37. 37.

    DiLoreto, D., Jr., Ison, J. R., Bowen, G. P., Cox, C., and del Cerro, M. 1995. A functional analysis of the age-related degeneration in the Fischer 344 rat. Curr. Eye Res. 14:303–310.

    Google Scholar 

  38. 38.

    DiLoreto, D., Jr., Cox, C., Grover, D. A., Lazar, E., del Cerro, C., and del Cerro, M. 1994. The influences of age, retinal topography, and gender on retinal degeneration in the Fisher 344 rat. Brain Res. 647:181–191.

    Google Scholar 

  39. 39.

    Lake, N. 1982. Depletion of taurine in the adult rat retina. Neurochem. Res. 7:1385–1390.

    Google Scholar 

  40. 40.

    Quesada, O., Huxtable, R. J., and Pasantes-Morales, H. 1984. Effect of guanidinoethane sulfonic acid on taurine uptake by rat retina. J. Neurosci. Res. 11:179–186.

    Google Scholar 

  41. 41.

    Lake, N. 1986. Electroretinographic deficits in rats treated with guanidinoethyl sulfonate, a depletor of taurine. Exp. Eye Res. 42:87–91.

    Google Scholar 

  42. 42.

    Cocker, S. E. and Lake, N. 1987. Electroretinographic alterations and their reversal in rats treated with guanidinoethyl sulfonate, a taurine depletor. Exp. Eye Res. 45:977–987.

    Google Scholar 

  43. 43.

    Shimada, C., Tanaka, S., Hasegawa, M., Kuroda, S., Isaka, K., Sano, M., and Araki, H. 1992. Beneficial effect of intravenous infusion on electroretinographic disorder in taurine deficient rats. Jpn. J. Pharmacol. 59:43–50.

    Google Scholar 

  44. 44.

    Lombardini, J. B., Young, R. S. L., and Props, C. L. 1996. Taurine depletion increases phosphorylation of a specific protein in the rat retina. Amino Acids. 10:153–165.

    Google Scholar 

  45. 45.

    Lake, N. and Malik, N. 1987. Retinal morphology in rats treated with a taurine transport antagonist. Exp. Eye Res. 44:331–346.

    Google Scholar 

  46. 46.

    Cocker, S. E. and Lake, N. 1989. Effects of dark maintenance on retinal biochemistry and function during taurine depletion in the adult rat. Vis. Neurosci. 3:33–38.

    Google Scholar 

  47. 47.

    Lai, Y. L., Jocoby, R. O., and Jonas, A. M. 1978. Age-related and light-associated retinal changes in Fischer rats. Invest. Ophthalmal. Vis. Sci. 17:634–638.

    Google Scholar 

  48. 48.

    Lai, Y. L., Jocoby, R. O., and Yao, P. C. 1979. Animal model: Peripheral retinal degeneration in rats. Am. J. Pathol. 97:449–452.

    Google Scholar 

  49. 49.

    Katz, M. L. and Robison, W. G. Jr. 1986. Evidence of cell loss from the rat retina during senescence. Exp. Eye Res. 42:293–304.

    Google Scholar 

  50. 50.

    O'Steen, W. K., Sweatt, A. J., and Brodish, A. 1987. Effects of acute and chronic stress on the neural retina of young, mid-age, and aged Fischer-344 rats. Brain Res. 426:37–46.

    Google Scholar 

  51. 51.

    Pasantes-Morales, H., Quesada, O., Cárabez, A., and Huxtable, R. J. 1983. Effects of the taurine transport antagonist, guanidinoethane sulfonate, and β-alanine on the morphology of rat retina. J. Neurosci. Res. 9:135–143.

    Google Scholar 

  52. 52.

    Quesada, O., Picones, A., and Pasantes-Morales, H. 1988. Effect of light deprivation on the ERG responses of taurine deficient rats. Exp. Eye Res. 46:13–20.

    Google Scholar 

  53. 53.

    Rapp, L. M., Thum, L. A., and Anderson, R. E. 1988. Synergism between environment lighting and taurine depletion in causing photoreceptor cell degeneration. Exp. Eye Res. 46:229–238.

    Google Scholar 

  54. 54.

    Pasantes-Morales, H., Urban, P. F., Klethi, J., and Mandel, P. 1973. Light stimulated release of [35S]taurine from chicken retina. Brain Res. 51:375–378.

    Google Scholar 

  55. 55.

    Salceda, R., López-Colomé, A. M. and Pasantes-Morales, H. 1977. Light-stimulated release of [35S]taurine from frog retinal rod outer segments. Brain Res. 135:186–191.

    Google Scholar 

  56. 56.

    Schmidt, S. Y. 1978. Taurine fluxes in isolated cat and rat retinas: Effects of illumination. Exp. Eye Res. 26:529–535.

    Google Scholar 

  57. 57.

    Wasowicz, M., Morice, C., Ferrari, P., Callebert, J., and Versaux-Botteri, C. 2002 Long-term effects of light damage on the retina of albino and pigmented rats. Invest. Ophthalmol. Vis. Sci. 2002 43:813–820.

    Google Scholar 

  58. 58.

    Oraedu, A. C., Voaden, M. J., and Marshall, J. 1980. Photochemical damage in the albino rat retina: Morphological changes and endogenous amino acids. J. Neurochem. 35:1361–1369.

    Google Scholar 

  59. 59.

    Voaden, M. J., Hussain, A. A., and Lalji, K. 1984. Photochemical damage in the albino rat retina: Oral taurine has no effect on DNA and protein loss from severely damaged photoreceptor cells. J. Neurochem. 42:582–583.

    Google Scholar 

  60. 60.

    Penn, J. S., Naash, M. I., and Anderson, R. E. 1987. Effect of light history on retinal antioxidants and light damage susceptibility in the rat. Exp. Eye Res. 44:779–788.

    Google Scholar 

  61. 61.

    Wang, L., Lam, T. T., Lam, K. W., and Tso, M. O. 1994. Correlation of phospholipid hydroperoxide glutathione peroxidase activity to the sensitivity of rat retinas to photic injury. Ophthalmic Res. 26:60–64.

    Google Scholar 

  62. 62.

    Organisciak, D. T., Darrow, R. M., Barsalou, L., Darrow, R. A., Kutty, R. K., Kutty, G., and Wiggert, B. 1998. Light history and age-related changes in retinal light damage. Invest. Ophthalmol. Vis. Sci. 39:1107–1116.

    Google Scholar 

  63. 63.

    Zhang, L. P., Maiorino, M., Roveri, A., and Ursini, F. 1989. Phospholipid hydroperoxide glutathione peroxidase: Specific activity in tissues of rats of different age and comparison with other glutathione peroxidases. Biochem. Biophys. Acta. 1006:140–143.

    Google Scholar 

  64. 64.

    Rao, G., Xia, E., and Richardson, A. 1990. Effect of age on the expression of antioxidant enzymes in male Fischer F344 rats. Mech. Ageing Dev. 53:49–60.

    Google Scholar 

  65. 65.

    Carrillo, M. C., Kanai, S., Sato, Y., and Kitani, K. 1992. Age-related changes in antioxidant enzyme activities are region and organ, as well as sex, selective in the rat. Mech. Ageing Dev. 65: 187–198.

    Google Scholar 

  66. 66.

    Tian, L, Cai, Q., and Wei, H. 1998. Alterations of antioxidant enzymes and oxidative damage to macromolecules in different organs of rats during aging. Free Radic. Biol. Med. 24:1477–1484.

    Google Scholar 

  67. 67.

    Baek, B. S., Kwon, H. J., Lee, K. H., Yoo, M. A., Kim, E. W., Ikeno, Y., Yu, B. P., and Chung, H. Y. 1999. Regional difference of ROS generation, lipid peroxidation, and antioxidant enzyme activity in rat brain and their dietary modulation. Arch. Pharm. Res. 22:361–366.

    Google Scholar 

  68. 68.

    Ohia, S. E., Bagchi, M., and Stohs, S. J. 1994. Age-related oxidative damage in Long-Evans rat retina. Res. Commun. Mol. Pathol. and Pharmacol. 85:21–31.

    Google Scholar 

  69. 69.

    Castorina, C., Campisi, A., Di Giacomo, C., Sorrenti, V., Russo, A., and Vanella, A. 1992. Lipid peroxidation and antioxidant enzymatic systems in rat retina as a function of age. Neurochem. Res. 17: 599–604.

    Google Scholar 

  70. 70.

    Bagchi, M., Bagchi, D., Patterson, E. B., Tang, L., and Stohs, S. J. 1996. Age-related changes in lipid peroxidation and antioxidant defense in Fischer 344 rats. Ann. N Y Acad. Sci. 793:449–452.

    Google Scholar 

  71. 71.

    Cao, G., Giovanoni, M., and Prior, R. L. 1996. Antioxidant capacity in different tissues of young and old rats. Proc. Soc. Exp. Biol. Med. 211:359–365.

    Google Scholar 

  72. 72.

    Demaree, S. R., Lawler, J. M., Linehan, J., and Delp, M. D. 1999. Ageing alters aortic antioxidant enzyme activities in Fischer-344 rats. Acta Physiol. Scand. 166:203–208.

    Google Scholar 

  73. 73.

    Pasantes-Morales, H. and Cruz, C. 1985. Taurine and hypotaurine inhibit light-induced lipid peroxidation and protect rod outer segment structure. Brain Res. 330:154–157.

    Google Scholar 

  74. 74.

    Tadolini, B., Pintus, G., Pinna, G. G., Bennardini, F., and Franconi, F. 1995. Effects of taurine and hypotaurine on lipid peroxidation. Biochem. Biophys. Res. Commun. 213:820–826.

    Google Scholar 

  75. 75.

    Pasantes-Morales, H. and Cruz, C. 1984. Protective effect of taurine and zinc on peroxidation-induced damage in photoreceptor outer segments. J. Neurosci. Res. 11:303–311.

    Google Scholar 

  76. 76.

    Zhou, M., Ma, T., and Tseng, M. T. 1991. Effects of taurine and ketamine on bovine retinal membrane lipid peroxidation. Neuroscience 45:461–465.

    Google Scholar 

  77. 77.

    Keys, S. A. and Zimmerman, W. F. 1999. Antioxidant activity of retinol, glutathione, and taurine in bovine photoreceptor cell membranes. Exp. Eye Res. 68:693–702.

    Google Scholar 

  78. 78.

    Vilchis, C. and Salceda, R. 1996 Effect of diabetes on levels and uptake of putative amino acid neurotransmitters in rat retina and retinal pigment epithelium. Neurochem. Res. 21:1167–1171.

    Google Scholar 

  79. 79.

    Obrosova, I. G., Minchenko, A. G., Marinescu, V., Fathallah, L., Kennedy, A., Stockert, C. M., Frank, R. N., and Stevens, M. J. 2001 Antioxidants attenuate early up regulation of retinal vascular endothelial growth factor in streptozotocin-diabetic rats. Diabetologia 2001 44:1102–1110.

    Google Scholar 

  80. 80.

    Colantuoni, A., Longoni, B., and Marchiafava, P. L. 2002. Retinal photoreceptors of Syrian hamsters undergo oxidative stress during streptozotocin-induced diabetes. Diabetologia 45:121–124.

    Google Scholar 

  81. 81.

    Di Leo, M. A. S., Santini, S. A., Cercone, S., Lepore, D., Gentiloni Silveri, N., Caputo, S., Greco, A. V., Giardina, B., Franconi, F., and Ghirlanda, G. 2002. Chronic taurine supplementation ameliorates oxidative stress and Na(+)K(+)ATPase impairment in the retina of diabetic rats. Amino Acids. 23: 401–406.

    Google Scholar 

  82. 82.

    Di Leo, M. A., Ghirlanda, G., Gentiloni Silveri, N., Giardina, B., Franconi, F., and Santini, S. A. 2003. Potential therapeutic effect of antioxidants in experimental diabetic retina: A comparison between chronic taurine and vitamin E plus selenium supplementations. Free Radic. Res. 37:323–330.

    Google Scholar 

  83. 83.

    Obrosova, I. G., Fathallah, L., and Stevens, M. J. 2001. Taurine counteracts oxidative stress and nerve growth factor deficit in early experimental diabetic neuropathy. Exp. Neurol. 172: 211–219.

    Google Scholar 

  84. 84.

    Schuller-Levis, G. B. and Sturman, J. A. 1992. “Activation” of alveolar leukocytes isolated from cats fed taurine-free diets. Pages 83–90, in Lombardini, J. B., Schaffer, S. W., and Azuma, J. (eds.), Taurine: Nutritional value and mechanisms of action. New York: Plenum Press.

    Google Scholar 

  85. 85.

    Zhang, X. and Lombardini, J. B. 1998. Effects of in vivo taurine depletion on induced-chemiluminescence production in macrophages isolated from rat lungs. Amino Acids. 15: 179–186.

    Google Scholar 

  86. 86.

    Devamanoharan, P. S, Ali, A. H., and Varma, S. D. 1997. Prevention of lens protein glycation by taurine. Mol. Cell. Biochem. 177:245–250.

    Google Scholar 

  87. 87.

    Devamanoharan, P. S., Ali, A. H., and Varma, S. D. 1998. Oxidative stress to rat lens in vitro: Protection by taurine. Free Radic. Res. 29:189–195.

    Google Scholar 

  88. 88.

    Kilic, F., Bhardwaj, R., Caulfeild, J., and Trevithick, J. R. 1999. Modelling cortical cataractogenesis 22: Is in vitro reduction of damage in model diabetic rat cataract by taurine due to its antioxidant activity? Exp. Eye Res. 69:291–300.

    Google Scholar 

  89. 89.

    Obrosova, I. G. and Stevens, M. J. 1999. Effect of dietary taurine supplementation on GSH and NAD(P)-redox status, lipid peroxidation, and energy metabolism in diabetic precataractous lens. Invest. Ophthalmol. Vis. Sci. 40:680–688.

    Google Scholar 

  90. 90.

    Messina, S. A. and Dawson, R., Jr. 2000. Attenuation of oxidative damage to DNA by taurine and taurine analogs. Adv. Exp. Med. Biol. 483:355–367.

    Google Scholar 

  91. 91.

    Heaton, P. R., Reed, C. F., Mann, S. J., Ransley, R., Stevenson, J., Charlton, C. J., Smith, B. H., Harper, E. J., and Rawlings, J. M. 2002. Role of dietary antioxidants to protect against DNA damage in adult dogs. J. Nutr. 132(6 Suppl 2):1720S–1724S.

    Google Scholar 

Download references

Author information

Affiliations

  1. Department of Pharmacology, Texas Tech University, Lubbock, Texas

    Julius Militante & John B. Lombardini

  2. Department of Ophthalmology and Visual Sciences, Texas Tech University Health Sciences Center, Lubbock, Texas

    John B. Lombardini

Authors
  1. Julius Militante
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John B. Lombardini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John B. Lombardini.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Militante, J., Lombardini, J.B. Age-Related Retinal Degeneration in Animal Models of Aging: Possible Involvement of Taurine Deficiency and Oxidative Stress. Neurochem Res 29, 151–160 (2004). https://doi.org/10.1023/B:NERE.0000010444.97959.1b

Download citation

  • Age-related retinal degeneration
  • taurine deficiency
  • oxidative stress
  • electroretinogram changes
  • antioxidant properties of taurine
  • changes in taurine levels with age