Neurochemical Research

, Volume 22, Issue 4, pp 445–453 | Cite as

Lipid Metabolism in Photoreceptor Membranes: Regulation and Mechanisms

  • N. M. Giusto
  • P. I. Castagnet
  • M. G. Ilincheta
  • M. E. Roque
  • S. J. Pasquaré


Lipid metabolism in photoreceptor rod outer segments has attracted considerable attention because of its importance in providing the appropriate environment for supporting an efficient phototransduction mechanism. Recent studies suggest that lipid metabolism in these membranes is involved in the generation of second messengers and in signal transduction mechanisms. Phospholipid turnover is tightly regulated by phosphorylation-dephosphorylation reactions and light, and provides, in turn, with molecules capable of activating protein kinases and cellular processes such as membrane fusion or light-adaptation. These findings suggest that photoreceptor membrane lipids are more than just important structural components of the visual cell rod outer segment.

Photoreceptor membranes phospholipid metabolism phosphorylation-dephosphorylation light modulation 


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  1. 1.
    Fesenko, E. E., Kolesnikov, S. S., and Lyubarsky, A. L. 1985. Induction by cyclic GMP of cationic conductance in plasma membranes of retinal rod outer segments. Nature 313:310–313.Google Scholar
  2. 2.
    Nakatani, K., and Yau, K. W. 1985. cGMP opens the light-sensitive conductance in retinal rods. Biophys. J. 47:356–360.Google Scholar
  3. 3.
    Kawamura, S., and Bownds, M. D. 1981. Light adaptation of the cyclic GMP phosphodiesterase of frog photoreceptor membranes mediated by ATP and calcium ions. J. Gen. Physiol. 77:571–591.Google Scholar
  4. 4.
    Troyer, E. W., Hall, L. A., and Ferrendelli, J. A. 1978. Guanylate cyclase in CNS: enzymatic characteristics of soluble and particulate enzymes from mouse cerebellum and retina. J. Neurochem. 31:825–833.Google Scholar
  5. 5.
    Kapoor, C. L., and Chader, G. J. 1984. Endogenous phosphorylation of retinal photoreceptor outer segment proteins by calcium phospholipid-dependent protein kinase. Biochem. Biophys. Res. Commun. 122:1397–1403.Google Scholar
  6. 6.
    Hayashi, F., and Amakawa, T. 1985. Light-mediated breakdown of phosphatidylinositol 4,5 bisphosphate in isolated rod outer segments of frog photoreceptor. Biochem. Biophys. Res. Commun. 128:954–959.Google Scholar
  7. 7.
    Ghalayini, A. J., and Anderson, R. E. 1984. Phosphatidylinositol 4,5 bisphosphate light-mediated breakdown in the vertebrate retina. Biochem. Biophys. Res. Commun. 124:503–506.Google Scholar
  8. 8.
    Fung, B. K., Hurley, J. B., and Stryer, L. 1981. Flow of information in the light-triggered cyclic nucleotide cascade of vision. Proc. Natl. Acad. Sci. USA 78:152–156.Google Scholar
  9. 9.
    Vandenberg, C. A., and Montal, M. 1984. Light-regulated biochemical events in invertebrate photoreceptors. 2. Light-regulated phosphorylation of rhodopsin and phosphoinositides in squid photoreceptor membranes. Biochemistry 23:2347–2352.Google Scholar
  10. 10.
    Kelleher, D. J., and Johnson, G. L. 1986. Phosphorylation of rhodopsin by protein kinase C in vitro. J. Biol. Chem. 261:4749–4757.Google Scholar
  11. 11.
    Bazán, N. G., Di Fazio, S. E. de, Careaga, M. M., Bazán, H. E. P., and Giusto, N. M. 1982. Phosphatidic acid of photoreceptor membranes: high content of docosahexaenoate and active [2-3H]glycerol metabolism. Biochim. Biophys. Acta 712:702–706.Google Scholar
  12. 12.
    Fliesler, S. J., and Anderson, R. E. 1983. Chemistry and metabolism of lipids in the vertebrate retina. Prog. Lipid Res. 22:79–131.Google Scholar
  13. 13.
    Giusto, N. M., and Ilincheta de Boschero, M. G. 1986. Synthesis of polyphosphoinositides in vertebrate photoreceptor membranes. Biochim. Biophys. Acta 877:440–446.Google Scholar
  14. 14.
    Ilincheta de Boschero, M., and Giusto, N. M. 1992. Phosphatidic acid and polyphosphoinositide metabolism in rod outer segments. Differential role of soluble and peripheral proteins. Biochim. Biophys. Acta 1127:105–115.Google Scholar
  15. 15.
    Seelig, J., Macdonald, P. M., and Scherer, P. G. 1987. Phospholipid head groups as sensors of electric charge in membranes. Biochemistry 26:7535–7541.Google Scholar
  16. 16.
    Pasquaré de Garcia, S. J., and Giusto, N. M. 1986. Phosphatidate phosphatase activity in isolated rod outer segments from bovine retina. Biochim. Biophys. Acta 875:195–202.Google Scholar
  17. 17.
    Pasquaré, S. J., and Giusto, N. M. 1993. Differential properties of phosphatidate phosphohydrolase and diacylglyceride lipase activities in retinal subcellular fractions and rod outer segments. Comp. Biochem. Physiol. 104B:141–148.Google Scholar
  18. 18.
    Moller, F., Wong, K. H., and Green, P. 1981. Control of fat cell phosphatidate phosphohydrolase by lipolytic agents. Can. J. Biochem. 59:9–15.Google Scholar
  19. 19.
    Berglund, R., Bjorkhem, I., and Einarsson, K. 1982. Apparent phosphorylation-dephosphorylation of soluble phosphatidic acid phosphatase in rat liver. Biochem. Biophys. Res. Commun. 105:288–295.Google Scholar
  20. 20.
    Ide, H., Koyama, S., and Nakazawa, Y. 1990. DAG generated in the PL vesicles by PLC is effectively utilized by DAG lipase in rat liver cytosol. Biochim. Biophys. Acta 1044:179–186.Google Scholar
  21. 21.
    Pagano, R. E., and Longmuir, K. J. 1985. Phosphorylation, transbilayer movement and facilitated intracellular transport of diacylglycerol are involved in the uptake of a fluorescent analog of phosphatidic acid by cultured fibroblasts. J. Biol. Chem. 260:1909–1916.Google Scholar
  22. 22.
    Seyfred, M. A., Kohnken, R. E., Collins, C. A., and McConnel, D. G. 1984. Rapid diglyceride phosphorylation in isolated rod outer segments. Biochem. Biophys. Res. Commun. 123:121–127.Google Scholar
  23. 23.
    Roque, M. E., and Giusto, N. M. 1995. Phosphatidylethanolamine N-methyltransferase activity in isolated rod outer segments from bovine retina. Exp. Eye Res. 60:631–643.Google Scholar
  24. 24.
    Hille, B. 1984. Ionic channels of excitable membranes. Chapter 13, Synauer Associates, Sunderland, MA.Google Scholar
  25. 25.
    Barber, J. R., and Clark, S. 1984. Inhibition of protein carboxyl methylation by S-adenosyl-L-homocysteine in intact erytrocytes. J. Biol. Chem. 259:7115–7122.Google Scholar
  26. 26.
    Pérez-Sala, D., Tan, E. W., Cañada, F. J., and Rando, R. 1991. Methylation and demethylation reactions of guanine nucleotide-binding proteins of retinal rod outer segments. Proc. Natl. Acad. Sci. USA 88:3043–3046.Google Scholar
  27. 27.
    Samborski, R. W., Ridgway, N. D., and Vance, D. E. 1990. Evidence that only newly made phosphatidylethanolamine is methylated to phosphatidylcholine and that phosphatidylethanolamine is not significantly deacylated-reacylated in rat hepatocytes. J. Biol. Chem. 265:18322–18329.Google Scholar
  28. 28.
    Tacconi, M. T., and Wurtman, R. J. 1985. Phosphatidylcholine produced in rat synaptosomes by N-methylation is enriched in polyunsaturated fatty acids. Proc. Natl. Acad. Sci. 82:4828–4831.Google Scholar
  29. 29.
    Aveldaño de Caldironi, M. I., Giusto, N. M., and Bazán, N. G. 1981. Polyunsaturated fatty acids of the retina. Prog. Lipid Res. 20:49–57.Google Scholar
  30. 30.
    Dennis, E. A., Rhee, S. G., Billah, M. M., and Hannun, Y. A. 1991. Role of phospholipases in generating lipid 2nd messengers in signal tranduction. FASEB J. 5:2068–2078.Google Scholar
  31. 31.
    El Touny, S., Khan, W., and Hannun, Y. 1990. Regulation of platelet protein kinase C by oleic acid. J. Biol. Chem. 265:16437–16443.Google Scholar
  32. 32.
    Alam, S. Q., Alam, B. S., and Ren, Y-F. 1987. Adenylate cyclase activity, membrane fluidity and fatty acid composition of rat heart in essential fatty acid deficiency. J. Mol. Cell Cardiol. 19:465–475.Google Scholar
  33. 33.
    Hook, G. E. R., Spalding, J. W., Ortner, M. J., Tombropoulos, E. G., and Chignell, C. F. 1984. Investigation of phospholipids of the pulmonary extracellular lining by electron paramagnetic resonance. Biochem. J. 223:533–542.Google Scholar
  34. 34.
    Futterman, S., Downes, J. L., and Hendrickson, A. 1971. Effect of fatty acid deficiency on the fatty acid composition, morphology and electroretinographic response of the retina. Invest. Ophtalmol. 10:151–156.Google Scholar
  35. 35.
    Vemuri, R., and Philipson, K. D. 1990. Influence of phospholipid fatty acyl composition in sarcolemmal and sarcoplasmic reticular cation transporter. Biochem. Biophys. Res. Commun. 168:917–922.Google Scholar
  36. 36.
    van Kuijk, F. J. G. M., Sevanian, A., Handelman, G. J., and Dratz, E. A. 1987. A new role for phospholipase A2: protection of membranes from lipid peroxidation damage. Trends Biochem. Sci. 12:31–34.Google Scholar
  37. 37.
    Irvine, R. F. 1982. How is the level of free arachidonic acid controlled in mammalian cells? Biochem. J. 204:3–16.Google Scholar
  38. 38.
    Giusto, N. M., Ilincheta de Boschero, M. G., Sprecher, H., and Aveldaño, M. I. 1986. Active labeling of phosphatidylcholines by [1-14C]docosahexaenoate in isolated photoreceptor membranes. Biochim. Biophys. Acta 860:137–148.Google Scholar
  39. 39.
    Zimmerman, W. F., and Keys, S. 1986. Acyltransferase and fatty acid coenzyme A synthetase activities within bovine rod outer segments. Biochem. Biophys. Res. Commun. 138:988–994.Google Scholar
  40. 40.
    Zimmerman, W. F., and Keys, S. 1988. Acylation and deacylation of phospholipids in isolated bovine rod outer segments. Exp. Eye Res. 47:247–260.Google Scholar
  41. 41.
    Jelsema, C. L. 1987. Light activation of phospholipase A2 in rod outer segments of bovine retina and its modulation by GTP-binding proteins. J. Biol. Chem. 262:163–168.Google Scholar
  42. 42.
    Louie, K., Wiegand, R. D., and Anderson, R. E. 1988. Docosah-exaenoate-containing molecular species of glycerophospholipids from frog retinal rod outer segments show different rates of biosynthesis and turnover. Biochemistry 27:9014–9020.Google Scholar
  43. 43.
    Castagnet, P. I., and Giusto, N. M. 1993. Properties of phospholipase A2 activity from bovine retinal rod outer segments. Exp. Eye Res. 56:709–719.Google Scholar
  44. 44.
    Zimmerman, W. F., and Keys, S. 1991. Effect of the antioxidants dithiothreitol and vitamin E on phospholipid metabolism in isolated rod outer segments. Exp. Eye Res. 50:607–612.Google Scholar
  45. 45.
    Abdel-Latif, A. A. 1986. Calcium-mobilizing receptors, polyphosphoinositides and the generation of second messengers. Pharmacol. Rev. 38:227–272.Google Scholar
  46. 46.
    Gehm, B. D., and McConnell, D. G. 1990. Phosphoinositide synthesis in bovine rod outer segments. Biochemistry 29:5442–5446.Google Scholar
  47. 47.
    Millar, F. A., and Hawthorne, J. N. 1985. Polyphosphoinositide metabolism in response to light stimulation of retinal rod outer segments. Biochem. Soc. Trans. 13:185–186.Google Scholar
  48. 48.
    Brown, J. E., Blazynski, C., and Cohen, A. 1987. Light induces a rapid and transient increase in inositoltrisphosphate in toad rod outer segments. Biochem. Biophys. Res. Commun. 146:1392–1396.Google Scholar
  49. 49.
    Millar, F. A., Fisher, S. C., Muir, C. A., Edwards, E., and Hawthorne, J. N. 1988. Polyphosphoinositide hydrolysis in response to light stimulation of rat and chick retina and retinal rod outer segments. Biochim. Biophys. Acta 970:205–211.Google Scholar
  50. 50.
    Waloga, G., and Anderson, R. E. 1985. Effects of inositol-1,4,5-triphosphate injections into salamander rods. Biochim. Biophys. Res. Commun. 126:59–62.Google Scholar
  51. 51.
    Brown, J. E., Rubin, L. J., Ghalayini, A. J., Tarver, A. L., Irvine, R. F., Berridge, M. J., and Anderson, R. E. 1984. Myo-inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature 311:160–162.Google Scholar
  52. 52.
    Fein, A., Payne, R., Corson, D. W., Berridge, M. J., and Irvine, R. F. 1984. Photoreceptor excitation and adaptation by inositol 1,4,5-trisphosphate. Nature 311:157–160.Google Scholar
  53. 53.
    Parker, K. R., Briggs, J. A., and Dratz, E. A. 1986. Inositol trisphosphate stimulates Ca2+ release from toad retinal rod outer segment preparations. Biophys. J. 49:31a.Google Scholar
  54. 54.
    Hamm, H. 1990. Regulation by light of cyclic nucleotide-dependent protein kinases and their substrates in frog rod outer segments. J. Gen. Physiol. 95:545–567.Google Scholar
  55. 55.
    Lolley, R. N., Brown, B. M., and Farber, D. B. 1977. Protein phosphorylation in rod outer segments from bovine retina: cyclic nucleotide-activated protein kinase and its endogenous substrate. Biochem. Biophys. Res. Commun. 78:572–578.Google Scholar
  56. 56.
    Roque, M., Pasquaré, S., Castagnet, P., and Giusto, N. M. Can phosphorylation and dephosphorylation of rod outer segment membranes affect phosphatidate phosphohydrolase and diacylglycerol lipase activity? Comp. Biochem. Physiol. (accepted).Google Scholar
  57. 57.
    Boesze-Battaglia, K., Albert, A. D., and Yeagle, P. L. 1992. Fusion between disk membranes and plasma membrane of bovine photoreceptor cells is calcium dependent. Biochemistry 31:3733–3738.Google Scholar
  58. 58.
    Young, R. W., and Bok, D. 1969. Participation of the retinal pigment epithelium in the rod outer segment renewal process. J. Cell. Biol. 42:392–403.Google Scholar

Copyright information

© Plenum Publishing Corporation 1997

Authors and Affiliations

  • N. M. Giusto
    • 1
  • P. I. Castagnet
    • 1
  • M. G. Ilincheta
    • 1
  • M. E. Roque
    • 1
  • S. J. Pasquaré
    • 1
  1. 1.Instituto de Investigaciones BioquímicasUniversidad Nacional del Sur y Consejo Nacional de Investigaciones Científicas y TécnicasBahía BlancaArgentina

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