The Calcium Gradient Along The Rod Outer Segment

  • K. Nicholas Leibovic
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 514)

Abstract

Vertebrate photoreceptor outer segments renew themselves by growing new membrane near the base and shedding old membrane at the tip. Parallel to the resulting age gradient along the outer segment there have also been observed gradients of membrane composition, rhodopsin phosphorylation, cGMP regeneration, responsiveness to light and others. This chapter describes the calcium gradient which has been found to exist along the outer segment. The concentration of calcium which increases towards the tip is due to an increase in buffered calcium. Since calcium is involved in a network of regulatory processes this gradient has implications for the transduction cascade as it affects the light response, as well as on disc shedding and other functions of the outer segments.

Keywords

Cholesterol Hydrolysis Magnesium Retina Pyruvate 

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References

  1. 1.
    Young RW. The renewal of photoreceptor cell outer segments. J Cell Biol 1967; 33:61–72.PubMedCrossRefGoogle Scholar
  2. 2.
    Young RW. Visual cells and the concept of renewal. Invest Ophthalmol Vis Sci 1976; 15:700–25.PubMedGoogle Scholar
  3. 3.
    Besharse JC. The daily light-dark cycle and rhythmic metabolism in the photorecptor-pigment epithelial complex. Progr in Retinal Res 1982; 1982:81–124.CrossRefGoogle Scholar
  4. 4.
    Bok D. Retinal photoreceptor-pigment epithelium interactions. Friedenwald lecture. Invest Ophthalmol Vis Sci 1985; 26:1659–94.PubMedGoogle Scholar
  5. 5.
    Boesze-Battaglia K, Albert AD. Cholesterol modulation of photoreceptor function in bovine retinal rod outer segments. J Biol Chem 1990; 265:20727–30.PubMedGoogle Scholar
  6. 6.
    Shichi HWilliams TC. Rhodopsin phosphorylation suggests biochemical heterogeneities of retinal rod disks. J Supramol Struct 1979; 12:419–24.PubMedCrossRefGoogle Scholar
  7. 7.
    Schnapf JL. Dependence of the single photon response on longitudinal position of absorption in toad rod outer segments. J Physiol 1983; 343:147–59.PubMedGoogle Scholar
  8. 8.
    Baylor DA, Lamb TD. Local effects of bleaching in retinal rods of the toad. J Physiol 1982; 328:49–71.PubMedGoogle Scholar
  9. 9.
    Leibovic KN, Pan KY. The saturated response of vertebrate rods and its relation to cGMP metabolism. Brain Res 1994; 653:325–9.PubMedCrossRefGoogle Scholar
  10. 10.
    Leibovic KN, Bandarchi J. Phototransduction and calcium exchange along the length of the retinal rod outer segment. Neuroreport 1997; 8:1295–300.PubMedCrossRefGoogle Scholar
  11. 11.
    Leibovic KN, Bandarchi J. Effects of light and temperature on the response gradient of retinal rod outer segments. Brain Res 1997; 750:321–4.PubMedCrossRefGoogle Scholar
  12. 12.
    Cornwall MC, Fein A, MacNichol Jr EF. Spatial localization of bleaching adaptation in isolated vertebrate rod photoreceptors. Proc Natl Acad Sci USA 1983; 80:2785–8.PubMedCrossRefGoogle Scholar
  13. 13.
    Matthews G. Spread of the light response along the rod outer segment: an estimate from patch-clamp recordings. Vision Res 1986; 26:535–41.PubMedCrossRefGoogle Scholar
  14. 14.
    Leibovic KN. Response waveforms of vertebrate photoreceptors: what are the underlying mechanisms? Biol Cybem 1978; 31:125–35.CrossRefGoogle Scholar
  15. 15.
    Nakatani K, Yau KW. Calcium and magnesium fluxes across the plasma membrane of the toad rod outer segment. J Physiol 1988; 395:695–729.PubMedGoogle Scholar
  16. 16.
    Pepperberg DR, Cornwall MC, Kahlert M et al. Light-dependent delay in the falling phase of the retinal rod photoresponse. Vis Neurosci 1992; 8:9–18.PubMedCrossRefGoogle Scholar
  17. 17.
    Bandarchi J, Leibovic KN. Effects of animal age on the responses along the outer segment of retinal rod photoreceptors. Neuroreport 1997; 8:581–5.PubMedCrossRefGoogle Scholar
  18. 18.
    Cervetto L, Lagnado L, Perry RJ et al. Extrusion of calcium from rod outer segments is driven by both sodium and potassium gradients. Nature 1989; 337:740–3.PubMedCrossRefGoogle Scholar
  19. 19.
    Stryer L. Cyclic GMP cascade of vision. Ann Rev Neurosci 1986; 9:87–119.PubMedCrossRefGoogle Scholar
  20. 20.
    Pugh EN, Cobbs WH. Visual transduction in vertebrate rods and cones: a tale of two transmitters, calcium and cGMP. Vision REs 1986; 26:1613–43.PubMedCrossRefGoogle Scholar
  21. 21.
    Yau KW, Baylor DA. Cyclic GMP-activated conductance of retinal photoreceptor cells. Annu Rev Neurosci 1989; 12:289–327.PubMedCrossRefGoogle Scholar
  22. 22.
    Leibovic KN. Vertebrate Photoreceptors. In: Leibovic KN, ed. Science of Vision. New York: 1990.CrossRefGoogle Scholar
  23. 23.
    McNaughton PA. Light response of vertebrate photoreceptors. Physiol Rev 1990; 70:847–84.PubMedGoogle Scholar
  24. 24.
    Yarfitz S, Hurley JB. Transduction mechanisms of vertebrate and invertebrate photoreceptors. J Biol Chem 1994; 269(20):14329–14332PubMedGoogle Scholar
  25. 25.
    Baehr W, Liebman PA. Visual Cascade. Encyclopedia of Life Sciences, MacMillan, 2000.Google Scholar
  26. 26.
    Yau KW, Nakatani K. Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment. Nature 1985; 313:579–82.PubMedCrossRefGoogle Scholar
  27. 27.
    Baylor DA, Lamb TD, Yau KW. The membrane current of single rod outer segments. J Physiol 1979; 288:589–611.PubMedGoogle Scholar
  28. 28.
    Leibovic KN. A new method of non-enzymatic dissociation of the Bufo retina. J Neurosci Methods 1986; 15:301–6.PubMedCrossRefGoogle Scholar
  29. 29.
    Leibovic KN, Dowling JE, Kim YY. Background and bleaching equivalence in steady-state adaptation of vertebrate rods. J Neurosci 1987; 7:1056–63.PubMedGoogle Scholar
  30. 30.
    Leibovic KN, Bandarchi J. Recovery from bleaching in photoreceptors promoted by biotin, pyruvate, and glucose. Vis Neurosci 1990; 4:489–92.PubMedCrossRefGoogle Scholar
  31. 31.
    Gray-Keller MP, Detwiler PB. The calcium feed back signal in the phototransduction cascade of vertebrate rods. Neuron 1994; 13:849–61.PubMedCrossRefGoogle Scholar
  32. 32.
    Korenbrot JI, Miller DL. Cytoplasmic free calcium concentration in dark-adapted retinal rod outer segments. Vision REs. 1989; 29:939–48.PubMedCrossRefGoogle Scholar
  33. 33.
    Lagnado L, Cervetto L, McNaughton PA. Calcium homeostasis in the outer segments of retinal rods from the tiger salamander. J Physiol 1992; 455:111–42.PubMedGoogle Scholar
  34. 34.
    McCarthy ST, Younger JP, Owen WG. Free calcium concentrations in bullfrog rods determined in the presence of multiple forms of Fura-2. Biophys J 1994; 67:2076–89.PubMedCrossRefGoogle Scholar
  35. 35.
    Younger JP, McCarthy ST, Owen WG. Light-dependent control of calcium in intact rods of the bullfrog Rana catesbeiana. J Neurophysiol 1996; 75:354–66.PubMedGoogle Scholar
  36. 36.
    Hagins WA, Yoshikami S. Proceedings: A role for Ca2+ in excitation of retinal rods and cones. Exp Eye Res 1974; 18:299–305.PubMedCrossRefGoogle Scholar
  37. 37.
    Waloga G. Effects of calcium and guanosine-3151-cyclic-monophosphoric acid on receptor potentials of toad rods. J Physiol 1983; 341:341–57.PubMedGoogle Scholar
  38. 38.
    Hsu Y-T, Molday RS. Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin. Nature 1993; 361:76–9.PubMedCrossRefGoogle Scholar
  39. 39.
    Koch K-W, Stryer L. Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 1988; 334:64–6.PubMedCrossRefGoogle Scholar
  40. 40.
    Boesze-Battaglia K, Fliesler SJ, Albert AD. Relationship of cholesterol content to spatial distribution and age of disc membranes in rod outer segments. J Biol Chem 1990; 265(31):18867–18870.PubMedGoogle Scholar
  41. 41.
    Papahadjopoulos D, Vail WJ, Newton C et al. Studies on membrane fusion. III. The role of calcium-induced phase changes. Biochim Biophys Acta 1977; 465:579–98.PubMedCrossRefGoogle Scholar
  42. 42.
    Koter M, de Kruijff B, van Deenen LL. Calcium-induced aggregation and fusion of mixed phosphatidylcholine-phosphatidic acid vesicles as studied by 31P NMR. Biochim Biophys Acta • 1978; 514:255–63.CrossRefGoogle Scholar
  43. 43.
    Zidovetzki R, Atiya AW, De Boeck H. Effect of divalent cations on the structure of dipalmitoylphosphatidyicholine and phosphatidylcholinelphosphatidylglycerol bilayers: an 2H-NMR study. Membr Biochem 1989; 8:177–86.PubMedCrossRefGoogle Scholar
  44. 44.
    Ohki S, Zschornig O. Ion-induced fusion of phosphatidic acid vesicles and correlation between surface hydrophobicity and membrane fusion. Chem Phys Lipids 1993; 65:193–204.PubMedCrossRefGoogle Scholar
  45. 45.
    Karpen JW, Loney DA, Baylor DA. Cyclic GMP-activated channels of salamander retinal rods: spatial distribution and variation of responsiveness. J Physiol 1992; 448:257–74.PubMedGoogle Scholar
  46. 46.
    Greenberger LM, Besharse JC. Photoreceptor disc shedding in eye cups. Inhibition by deletion of extracellular divalent cations. Invest Ophthalmol Vis Sci 1983; 24:1456–64.PubMedGoogle Scholar
  47. 47.
    LaVail MM. Rod outer segment disk shedding in rat retina: relationship to cyclic lighting. Science 1976; 194:1071–4.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • K. Nicholas Leibovic
    • 1
  1. 1.Department of Physiology and BiophysicsState University ofN.Y., at Buffalo, N.Y., and Medical College of Virginia, Virginia Commonwealth UniversityRichmond

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