Skip to main content
Log in

Environmental light and heredity are associated with adaptive changes in retinal DHA levels that affect retinal function

  • Published:
Lipids

Abstract

Retinas of rats and mice react to environmental and genetic stimuli by altering the level of DHA in their rod outer segment membranes. We propose that this adaptation is a neuroprotective response to control the number of photons captured by rhodopsin and the efficiency of visual transduction, under conditions where excessive activation of the transduction cascade could lead to cell death.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

ERG:

electroretinogram

G:

transducin

prcd :

progressive rodcone degeneration

PUFA:

polyunsaturated fatty acid

ROS:

rod outer segments

References

  1. Fliesler, S.J., and Anderson, R.E. (1983) Chemistry and metabolism of lipids in the vertebrate retina, in Progress in Lipid Research (Holman, R.T., ed.), Vol. 22, pp. 79–131, Pergamon Press, Elmsford, New York.

    Google Scholar 

  2. Anderson, R.E., and Sperling, L. (1971) Lipids of ocular tissues: VII. Positional distribution of the fatty acids in the phospholipids of bovine retina rod outer segments, Arch. Biochem. Biophys. 144, 673–677.

    Article  PubMed  CAS  Google Scholar 

  3. Stinson, A.M., Wiegand, R.D., and Anderson, R.E. (1991) Fatty acid and molecular species compositions of phospholipids and diacylglycerols from rat retinal membranes, Exp. Eye. Res. 52, 213–218.

    Article  PubMed  CAS  Google Scholar 

  4. Anderson, R.E., and Maude, M.B. (1972) Lipids of ocular tissues: VII. The effects of essential fatty acid deficiency on the phospholipids of the photoreceptor membranes of rat retina, Arch. Biochem. Biophys. 151, 270–276.

    Article  PubMed  CAS  Google Scholar 

  5. Wiegand, R.D., Koutz, C.A., Chen, H., and Anderson, R.E. (1995) Effect of dietary fat and environmental lighting on the phospholipid molecular species of rat photoreceptor membranes, Exp. Eye Res. 60, 291–306.

    Article  PubMed  CAS  Google Scholar 

  6. Koutz, C.A., Anderson, R.E., Rapp, L.M., and Wiegand, R.D. (1995) Effect of dietary fat and environmental lighting on the response of the rat retina to chronic and acute light stress, Exp. Eye Res. 60, 307–316.

    Article  PubMed  CAS  Google Scholar 

  7. Benolken, R.M., Anderson, R.E., and Wheeler, T.G. (1973) Membrane fatty acids associated with the electrical response in visual excitation, Science 182, 1253–1254.

    Article  PubMed  CAS  Google Scholar 

  8. Niu, S.L., Mitchell, D.C., Lim, S.Y., Wen, Z.M., Kim, H.Y., Salem, N., Jr., and Litman, B.J. (2004) Reduced G protein-coupled to n−3 fatty acid deficiency, J. Biol. Chem. 279, 31098–31104.

    Article  PubMed  CAS  Google Scholar 

  9. Moriguchi, T., Lim, S.Y., Greiner, R., Lefkowitz, W., Loewke, J., Hoshiba, J., and Salem, N., Jr. (2004) Effects of an n−3-deficient diet on brain, retina, and liver fatty acyl composition in artificially reared rats, J. Lipid Res. 45, 1437–1445.

    Article  PubMed  CAS  Google Scholar 

  10. Wheeler, T.G., Benolken, R.M., and Anderson, R.E. (1975) Visual membranes: Specificity of fatty acid precursors for the electrical response to illumination, Science 188, 1312–1314.

    Article  PubMed  CAS  Google Scholar 

  11. Watanabe, I., Kato, M., Aonuma, H., Hishimoto, A., Naito, Y., Moriuchi, A., and Okuyama, H. (1987) Effect of dietary alphalinolenate/linoleate balance on the lipid composition and electroretinographic responses in rats, in Advances in the Biosciences, Vol. 62: Research in Retinitis Pigmentosa (Zrenner, E., Krastel, H., and Goebel, H.H., eds.), pp. 563–570, Pergamon Journals Ltd., Oxford, United Kingdom.

    Google Scholar 

  12. Bourre, J., Francois, M., Youyou, A., Doumont, O., Piciotti, M., Pascal, G., and Durand, G. (1989) The effects of dietary α-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance poisons and performance of learning tasks in rats, J. Nutr. 119, 1880–1892.

    PubMed  CAS  Google Scholar 

  13. Weisinger, H., Vingrys, A., and Sinclair, A. (1996) Effect of dietary n−3 deficiency on the electroretinogram in the guinea pig. Ann. Nutr. Metab. 40, 91–98.

    Article  PubMed  CAS  Google Scholar 

  14. Weisinger, H., Vingrys, A., and Sinclair, A. (1996) The effect of docosahexaenoic acid on the electroretinogram of the guinea pig. Lipids 31, 65–70.

    Article  PubMed  CAS  Google Scholar 

  15. Weisinger, H.S., Vingrys, A.J., Abedin, L., and Sinclair, A.J. (1998) Effect of diet on the rate of depletion of n−3 fatty acids in the retina of the guinea pig, J. Lipid Res. 39, 1274–1279.

    PubMed  CAS  Google Scholar 

  16. Weisinger, H.S., Vingrys, A.J., Bui, B.V., and Sinclair, A.J. (1999) Effects of dietary n−3 fatty acid deficiency and repletion in the guinea pig retina, Invest. Ophthalmol. Vis. Sci. 40, 327–338.

    PubMed  CAS  Google Scholar 

  17. Neuringer, M., Connor, W.E., Van Patten, C., and Barstad, L. (1984) Dietary omega-3 fatty acid deficiency and visual loss in infant rhesus monkeys, J. Clin. Invest. 73, 272–276.

    Article  PubMed  CAS  Google Scholar 

  18. Neuringer, M., Connor, W.E., Lin, D.S., Barstad, L., and Luck, S. (1986) Biochemical and functional effects of prenatal and postnatal ω-3 fatty acid deficiency on retina and brain in rhesus monkeys, Proc. Natl. Acad. Sci. USA 83, 4021–4025.

    Article  PubMed  CAS  Google Scholar 

  19. Neuringer, M., and Connor, W.E. (1986) n−3 fatty acids in the brain and retina: Evidence for their essentiality, Nutr. Rev. 44, 285–294

    Article  PubMed  CAS  Google Scholar 

  20. Neuringer, M., and Connor, W.E. (1987) The importance of dietary n−3 fatty acids in the development of the retina and nervous system, in Proceedings of the AOCS Short Course on Polyunsaturated Fatty Acids and Eicosanoids (Lands, W.E.M. ed.), pp. 301–311, American Oil Chemists' Society, Champaign, Illinois.

    Google Scholar 

  21. Neuringer, M., Connor, W.E., Lin, D.S., Anderson, G.J., and Barstad, L. (1991) Dietary omega-3 fatty acids: effects on retinal lipid composition and function in primates, in Retinal Degenerations, (Anderson, R.E., Hollyfield, J.G., and LaVail, M.M., eds.), pp. 1–13, CRC Press, New York.

    Google Scholar 

  22. Uauy, R.D., Birch, D.G., Birch, E.E., Tyson, J.E., and Hoffman, D.R. (1990) Effect of dietary omega-3 fatty acids on retinal function of very-low-birth-weight neonates, Pediatr. Res. 58, 485–492.

    Article  Google Scholar 

  23. Carlson, S.E., Werkman, S.H., Rhodes, P.G., and Tolley, E.A. (1993) Visual-acuity development in healthy preterm infants: Effect of marine oil supplementation, Am. J. Clin. Nutr. 58, 35–42.

    PubMed  CAS  Google Scholar 

  24. Carlson, S.E., Cooke, R.J., Werkman, S.H., and Tolley, E.A. (1992) First year growth of preterm infants fed standard compared to marine oil n−3 supplemented formula, Lipids 27, 901–907.

    Article  PubMed  CAS  Google Scholar 

  25. Carlson, S.E., Werkman, S.H., Peeples, J.M., Cooke, R.J., and Tolley, E.A. (1993). Arachidonic acid status correlates with first year growth in preterm infants, Proc. Natl. Acad. Sci. USA 90, 1073–1077.

    Article  PubMed  CAS  Google Scholar 

  26. Gibson, R.A., and Makrides, M. (1998) The role of long chain polyunsaturated fatty acids (LCPUFA) in neonatal nutrition, Acta Paediatr. 87, 1017–1022.

    Article  PubMed  CAS  Google Scholar 

  27. Birch, E.E., Birch, D.G., Hoffman, D.R., and Uauy, R. (1992) Dietary essential fatty acid supply and visual acuity development, Invest. Ophthalmol. Vis. Sci. 33, 3242–3253.

    PubMed  CAS  Google Scholar 

  28. Birch, E.E., Hoffman, D.R., Uauy, R., Birch, D.G., and Prestidge, C. (1998) Visual acuity and the essentiality of docosahexaenoic acid and arachidonic acid in the diet of term infants, Pediatr. Res. 44, 201–209.

    Article  PubMed  CAS  Google Scholar 

  29. Uauy, R.D., Birch, E.E., Birch, D.G., and Peiran, P. (1992) Visual and brain function measurements in studies of n−3 fatty acid requirements of infants, J. Pediatr. 120, S168-S178.

    Article  PubMed  CAS  Google Scholar 

  30. Penn, J.S., and Anderson, R.E. (1987) Effect of light history on rod outer-segment membrane composition in the rat, Exp. Eye Res. 44, 767–778.

    Article  PubMed  CAS  Google Scholar 

  31. Penn, J.S., Thum, L.A., and Naash, M.I. (1989) Photoreceptor physiology in the rat is governed by the light environment, Exp. Eye Res. 49, 205–215.

    Article  PubMed  CAS  Google Scholar 

  32. Aguirre, G.D., Acland, G.M., Maude, M.B., and Anderson, R.E. (1997) Diets enriched in docosahexaenoic acid fail to correct progressive rod-cone degeneration (prcd) phenotype, Invest. Ophthalmol. Vis. Sci. 38, 2387–2407.

    PubMed  CAS  Google Scholar 

  33. Anderson, R.E., Maude, M.B., and Bok, D. (2001) Low docosahexaenoic acid levels in rod outer segment membranes of mice with rds/peripherin and P216L peripherin mutations, Invest. Ophthalmol. Vis. Sci. 42, 1715–1720.

    PubMed  CAS  Google Scholar 

  34. Anderson, R.E., Sieving, P.A., Maude, M.B., and Naash, M.I. (2001) Mice with G90D rhodopsin mutations have lower DHA in rod outer segment membranes than control mice, in New Insights into Retinal Degenerative Diseases (Anderson, R.E., Hollyfield, J.G., and LaVail, M.M. eds.), pp. 235–245, Plenum Press, New York.

    Chapter  Google Scholar 

  35. Anderson, R.E., Maude, M.B., McClellan, M., Matthes, M.T., Yasumura, D., and LaVail, M.M. (2002) Low docosahexaenoic acid levels in rod outer segments of rats with P23H and S334ter rhodopsin mutations, Mol. Vis. 8, 351–358.

    PubMed  CAS  Google Scholar 

  36. Galli, C., Trzeciak, H.I., and Paoletti, R. (1971) Effects of dietary fatty acids on the fatty acid composition of the brain ethanolamine phosphoglyceride: reciprocal replacement of n−6 and n−3 polyunsaturated fatty acids, Biochim. Biophys. Acta 248, 449–454.

    CAS  Google Scholar 

  37. Anderson, R.E., and Maude, M.B. (1972) Lipids of ocular tissues: VII. The effects of essential fatty acid deficiency on the phospholipids of the photoreceptor membranes of rat retina, Arch. Biochem. Biophys. 151, 270–276.

    Article  PubMed  CAS  Google Scholar 

  38. Martin, R.E., Ranchon-Cole, I., Brush, R.S., Williamson, C.R., Hopkins, S.A., Li, F., and Anderson, R.E. (2004) P23H and S334ter opsin mutations: Increasing photoreceptor outer segment n−3 fatty acid content does not affect the course of retinal degeneration, Molec. Vis. 10, 199–207.

    PubMed  CAS  Google Scholar 

  39. Penn, J.S., and Williams, T.P. (1986) Photostasis: Regulation of daily photon-catch by rat retinas in response to various cyclic illuminances, Exp. Eye Res. 43, 915–928.

    Article  PubMed  CAS  Google Scholar 

  40. Noell, W.K., Walker, V.S., Kang, B.S., and Berman, S. (1966) Retinal damage by light in rats, Invest. Ophthalmol. 5, 450–473.

    PubMed  CAS  Google Scholar 

  41. Sanyal, S., and Hawkins, R.K. (1986) Development and degeneration of retina in rds mutant mice: effects of light on the rate of degeneration in albino and pigmented homozygous and heterozygous mutant and normal mice, Vision Res. 26, 1177–1785.

    Article  PubMed  CAS  Google Scholar 

  42. LaVail, M.M., Gorrin, G.M., Yasumura, D., and Matthes, M.T. (1999) Increased susceptibility to constant light in nr and pcd mice with inherited retinal degeneration, Invest. Ophthalmol Vis. Sci. 40, 1020–1024.

    PubMed  CAS  Google Scholar 

  43. 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.

    Article  PubMed  CAS  Google Scholar 

  44. Penn, J.S., and Anderson, R.E. (1992) Effects of light history on the rat retina, in Progress in Retinal Research (Osborne, N. and Chader, G., eds.), Vol. 11, pp. 75–98, Pergamon Press, New York.

    Google Scholar 

  45. Dudley, P.A., Landis, D.J., and Anderson, R.E. (1975) Further studies on the chemistry of photoreceptor membranes of rats fed an essential fatty acid deficient diet, Exp. Eye Res. 21, 523–530.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert E. Anderson.

About this article

Cite this article

Anderson, R.E., Penn, J.S. Environmental light and heredity are associated with adaptive changes in retinal DHA levels that affect retinal function. Lipids 39, 1121–1124 (2004). https://doi.org/10.1007/s11745-004-1338-8

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-004-1338-8

Keywords

Navigation