Significance of Changes in Intracellular Ca2+ for the Mechanism of Signal Transduction in Vertebrate Rod Cells

  • U. B. Kaupp
  • K.-W. Koch
Part of the Dahlem Workshop Reports book series (DAHLEM, volume 34)


Light and cyclic GMP stimulate the flux of Ca2+ ions across the plasma and disk membrane in rod cells of the vertebrate retina. Ca2+ enters the cytosol through the light-sensitive channels in the plasma membrane and a cyclic GMP-regulated conductance in the disk membrane. Ca2+ is extruded from the cell by an Na+/Ca2+ exchange mechanism. The existence of an active, ATP-dependent uptake of Ca2+ into disks is likely; a Ca2+-transport ATPase in the plasma membrane, however, has not yet been identified. Some of these transport systems may be directly or indirectly regulated by light. The individual contributions of each transport system to the maintenance of the cytosolic Ca2+ concentration in the dark and its change by light have not yet been delineated. In particular, attempts to detect the rapid injection of Ca2+ (<100 ms) from inside disks into the cytosol — a crucial component of the “Ca2+ hypothesis” — have been unsuccessful. A final decision on the relevance of changes in Ca2+ i for the generation of the electrical signal must be postponed until the much needed measurements of intracellular Ca2+ in these cells are available.


Outer Segment Disk Membrane Vertebrate Retina Cytosolic Concentration Proton Uptake 
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  1. (1).
    Ashley, C.C. 1967. The role of cell calcium in the contraction of single cannulated muscle fibers. Am. Zool. 7: 647.PubMedGoogle Scholar
  2. (2).
    Bastian, B.L., and Fain, G.L. 1982. The effects of sodium replacement on the responses of toad rods. J. Physiol. 330: 331–347.PubMedGoogle Scholar
  3. (3).
    Baylor, D.A., and Fuortes, M.G.F. 1970. Electrical responses of single cones in the retina of the turtle. J. Physiol. 207: 77–92.PubMedGoogle Scholar
  4. (4).
    Berridge, M.J., and Irvine, R.F. 1984. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312: 315–321.PubMedCrossRefGoogle Scholar
  5. (5).
    Brown, J.E., and Rubin, L.J. 1984. A direct demonstration that inositol trisphosphate induces an increase in intracellular calcium in Limulus photoreceptors. Biohem. Biophys. Res. Commun. 125: 1137–1142.CrossRefGoogle Scholar
  6. (6).
    Brown, J.E.; Rubin, L.J.; Ghalayini, A.J.; Tarver, A.P.; Irvine, R.F.; Berridge, M.J.; and Anderson, R.E. 1984. Evidence that myo-inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature 311: 160–163.PubMedCrossRefGoogle Scholar
  7. (7).
    Campbell, A.K. 1983. Intracellular Calcium. Chichester: John Wiley.Google Scholar
  8. (8).
    Caretta, A., and Cavaggioni, A. 1983. Fast ionic flux activated by cyclic GMP in the membrane of cattle rod outer segment. Eur. J. Biochem. 132: 1–8.PubMedCrossRefGoogle Scholar
  9. (9).
    Cavaggioni, A., and Sorbi, R.T. 1981. Cyclic GMP releases calcium from disk membranes of vertebrate photoreceptors. Proc. Natl. Acad. Sci. USA 78: 3964–3968.PubMedCrossRefGoogle Scholar
  10. (10).
    Cohen, A.I. 1981. The use of incubated retinas in investigating the effects of calcium and other ions on cyclic-nucleotide levels in photoreceptors. Curr. Top. Membr. Trans. 15: 215–229.Google Scholar
  11. (11).
    Cone, R.A. 1972. Rotational diffusion of rhodopsin in the visual receptor membrane. Nat. New Biol. 236: 39–43.PubMedGoogle Scholar
  12. (12).
    Corson, D.W.; Fein, A.; and Payne, R. 1985. Detection of an inositol 1, 4, 5-triphosphate-induced rise in intracellular free Ca2+ with aequorin in Limulus ventral photoreceptors. Biol. Bull., in press.Google Scholar
  13. (13).
    Cote, R.H.; Biernbaum, M.S.; Nicol, G.D.; and Bownds, M.D. 1984. Light-induced decreases in cGMP concentration precede changes in membrane permeability in frog rod photoreceptors. J. Biol. Chem. 259: 9635–9641.PubMedGoogle Scholar
  14. (14).
    Detwiler, P.B.; Conner, J.A.; and Bodoia, R.D. 1982. Gigaseal patchclamp recordings from outer segments of intact retinal rods. Nature 300: 59–62.PubMedCrossRefGoogle Scholar
  15. (15).
    Di Virgilio, F.; Lew, D.P.; and Pozzan, T. 1984. Protein kinase C activation of physiological processes in human neutrophils at vanishingly small cytosolic concentrations. Nature 310: 691–693.PubMedCrossRefGoogle Scholar
  16. (16).
    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.PubMedCrossRefGoogle Scholar
  17. (17).
    Fesenko, E.E.; Kolesnikov, S.S.; and Lyubarsky, A.L. 1985. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313: 310–313.PubMedCrossRefGoogle Scholar
  18. (18).
    George, J.S., and Hagins, W.A. 1983. Control of Ca2+ in rod outer segment disks by light and cyclic GMP. Nature 303: 344–348.PubMedCrossRefGoogle Scholar
  19. (19).
    Gold, G.H., and Korenbrot, J.I. 1980. Light-induced calcium release by intact retinal rods. Proc. Natl. Acad. Sci. USA 77: 5557–5561.PubMedCrossRefGoogle Scholar
  20. (20).
    Gold, G.H., and Korenbrot, J.I. 1981. The regulation of calcium in the intact retinal rod: A study of light-induced calcium release by outer segment. Curr. Top. Membr. Trans. 15: 307–330.Google Scholar
  21. (21).
    Goldberg, N.D.; Ames, A. III; Gander, J.E.; and Walseth, T.F. 1983. Magnitude of increase in retinal cGMP metabolic flux determined by 18 O incorporation into nucleotide-phosphoryls corresponds with intensity of photic stimulation. J. Biol. Chem. 258: 9213–9219.PubMedGoogle Scholar
  22. (22).
    Hanke, W., and Kaupp, U.B. 1984. Incorporation of ion channels from bovine rod outer segments into planar lipid bilayers. Biophys. J. 46: 587–595.PubMedCrossRefGoogle Scholar
  23. (23).
    Hawthorne, J.N. 1983. Polyphosphoinositide metabolism in excitable membranes. Biosci. Rep. 3: 887–904.PubMedCrossRefGoogle Scholar
  24. (24).
    Hodgkin, A.L.; McNaughton, P.A.; Nunn, B.J.; and Yau, K.-W. 1984. Effect of ions on retinal rods from Bufo marinus. J. Physiol. 350: 649–680.PubMedGoogle Scholar
  25. (25).
    Kaupp, U.B. 1984. The role of calcium in visual transduction. In Information and Energy Transduction in Biological Membranes, eds. E.J. Helmreich, pp. 325–339. New York: A.R. Riss.Google Scholar
  26. (26).
    Kaupp, U.B., and Koch, K.-W. 1984. Cyclic GMP releases calcium from leaky rod outer segments. Vision Res. 24: 1477–1479.PubMedCrossRefGoogle Scholar
  27. (27).
    Kaupp, U.B., and Schnetkamp, P.P.M. 1982. Calcium metabolism in vertebrate photoreceptors. Cell Calcium 3: 83–112.PubMedCrossRefGoogle Scholar
  28. (28).
    Kaupp, U.B.; Schnetkamp, P.P.M.; and Junge, W. 1979. Light-induced calcium release in intact rod outer segments upon photoexcitation of rhodopsin. Biochim. Biophys. Acta 552: 390–403.PubMedCrossRefGoogle Scholar
  29. (29).
    Kaupp, U.B.; Schnetkamp, P.P.M.; and Junge, W. 1981a. Rapid calcium release and proton uptake at the disk membrane of isolated cattle rod outer segments. 1. Stoichiometry of light-stimulated calcium release and proton uptake. Biochemistry 20: 5500–5510.PubMedCrossRefGoogle Scholar
  30. (30).
    Kaupp, U.B.; Schnetkamp, P.P.M.; and Junge, W. 1981b. Rapid calcium release and proton uptake at the disk membrane of isolated cattle rod outer segments. 2. Kinetics of light-stimulated calcium release and proton uptake. Biochemistry 20: 5511–5516.PubMedCrossRefGoogle Scholar
  31. (31).
    Koch, K.-W., and Kaupp, U.B. 1985. Cyclic GMP directly regulates a cation conductance in membranes of bovine rods by a cooperative mechanism. J. Biol. Chem. 260: 6788–6800.PubMedGoogle Scholar
  32. (32).
    Lamb, T.D. 1984. Effects of temperature changes on toad rod photocurrents. J. Physiol. 346: 557–578.PubMedGoogle Scholar
  33. (33).
    Lamb, T.D.; McNaughton, P.A.; and Yau, K.-W. 1981. Spatial spread of activation and background desensitization in toad rod outer segments. J. Physiol. 319: 463–496.PubMedGoogle Scholar
  34. (34).
    Liebman, P.A., and Pugh, E.N., Jr. 1981. Control of rod disk membrane phosphodiesterase and a model for visual transduction. Curr. Top. Membr. Trans. 15: 157–170.Google Scholar
  35. (35).
    Lipton, S.A. 1983. cGMP and EGTA increase the light-sensitive current of retinal rods. Brain Res. 265: 41–48.PubMedCrossRefGoogle Scholar
  36. (36).
    Lisman, J.E.. and Brown, J.E. 1975. Effects of intracellular injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. J. Gen. Physiol. 66: 489–506.PubMedCrossRefGoogle Scholar
  37. (37).
    Lolley, R.N., and Racz, E. 1982. Calcium modulation of cyclic GMP synthesis in rat visual cells. Vision Res. 22: 1481–1486.PubMedCrossRefGoogle Scholar
  38. (38).
    MacLeish, P.R.; Schwartz, E.A.; and Tachibana, M. 1984. Control of the generator current in solitary rods of the Ambystoma tigrinum retina. J. Physiol. 348: 645–664.PubMedGoogle Scholar
  39. (39).
    McLaughlin, S., and Brown, J.E. 1981. Diffusion of calcium ions in retinal rods. J. Gen. Physiol. 77: 475–487.PubMedCrossRefGoogle Scholar
  40. (40).
    Michell, R.H. 1975. Inositol phospholipids and cell surface receptor function. Biochim. Biophys. Acta 415: 81–147.PubMedGoogle Scholar
  41. (41).
    Mullins, L.J. 1981. Ion Transport in Heart. New York: Raven Press.Google Scholar
  42. (42).
    Palade, P., and Vergara, J. 1982. Arsenazo III and Antipyrilazo III calcium transients in single skeletal muscle fibers. J. Gen. Physiol. 79: 679–707.PubMedCrossRefGoogle Scholar
  43. (43).
    Payne, R.; Fein, A.; and Corson, D.W. 1985. A rise in intracellular Ca2+is necessary and perhaps sufficient for photoreceptor excitation and adaptation by inositol 1, 4, 5-triphosphate. Biol. Bull., in press.Google Scholar
  44. (44).
    Pinto, L.H., and Brown, J.E. 1984. Pressure injection of 3′, 5′-cyclic GMP into solitary rod photoreceptors of the tiger salamander. Brain Res. 304: 197–200.PubMedCrossRefGoogle Scholar
  45. (45).
    Poo, M.-M., and Cone, R.A. 1974. Lateral diffusion of rhodopsin in the photoreceptor membrane. Nature 247: 438–441.PubMedCrossRefGoogle Scholar
  46. (46).
    Puckett, K.L.; Aronson, E.T.; and Goldin, S.M. 1985. ATP-dependent calcium uptake activity associated with a disk membrane traction isolated from bovine retinal rod outer segments. Biochemistry 24: 390–400.PubMedCrossRefGoogle Scholar
  47. (47).
    Reuter, H. 1983. Calcium channel modulation by neurotransmitters, enzymes and drugs. Nature 301: 569–574.PubMedCrossRefGoogle Scholar
  48. (48).
    Robinson, P.R.; Kawamura, S.; Abramson, B.; and Bownds, M.D. 1980. Control of the cyclic GMP phosphodiesterase of frog photoreceptor membranes. J. Gen. Physiol. 76: 631–645.PubMedCrossRefGoogle Scholar
  49. (49).
    Schnetkamp, P.P.M. 1979. Calcium translocation and storage of isolated intact cattle rod outer segments. Biochim. Biophys. Acta 554: 441–459.PubMedCrossRefGoogle Scholar
  50. (50).
    Schröder, W.H., and Fain, G.L. 1984. Light-dependent calcium release from photoreceptors measured by laser micro-mass analysis. Nature 309: 268–270.PubMedCrossRefGoogle Scholar
  51. (51).
    Smith, H.G., Jr.; Fager, R.S.; and Litman, B.J. 1977. Light-activated calcium release from sonicated bovine retinal rod outer segment disks. Biochemistry 16: 1399–1405.PubMedCrossRefGoogle Scholar
  52. (52).
    Sorbi, R.A. 1981. Modulation of sodium conductance in photoreceptor membranes by calcium ions and cGMP. Curr. Top. Membr. Trans. 15: 331–338.Google Scholar
  53. (53).
    Streb, H.; Irvine, R.F.; Berridge, M.J.; and Schulz, I. 1983. Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1, 4, 5-trisphosphate. Nature 306: 67–69.PubMedCrossRefGoogle Scholar
  54. (54).
    Szuts, E. 1981. Calcium tracer exchange in the rods of excised retina. Curr. Top. Membr. Trans. 15: 291–305.Google Scholar
  55. (55).
    Wey, C.-L.; Cone, R.A.; and Edidin, M.A. 1981. Lateral diffusion of rhodopsin in photoreceptor cells measured by fluorescence photobleaching and recovery. Biophys. J. 33: 225–232.PubMedCrossRefGoogle Scholar
  56. (56).
    Yau, K.-W., and Nakatani, K. 1984. Cation selectivity of light-sensitive conductance in retinal rods. Nature 309: 352–354.PubMedCrossRefGoogle Scholar
  57. (57).
    Yau, K.-W., and Nakatani, K. 1984. Electrogenic Na-Ca exchange in retinal rod outer segment. Nature 311: 661–663.PubMedCrossRefGoogle Scholar
  58. (58).
    Yoshikami, S.; George, J.S.; Hagins, W.A. 1980. Light-induced calcium fluxes from rod outer segment layer of vertebrate retina. Nature 286: 395–398.PubMedCrossRefGoogle Scholar
  59. (59).
    Yoshikami, S., and Hagins, W.A. 1971. Ionic basis of dark current and photocurrent of retinal rods. Biophys. J. 10: 60a.Google Scholar
  60. (60).
    Yoshikami, S., and Hagins, W.A. 1973. Control of the dark current in vertebrate rods and cones. In Biochemistry and Physiology of Visual Pigments, ed. H. Langer, pp. 245–255. Berlin: Springer-Verlag.Google Scholar

Copyright information

© Dr. S. Bernhard, Dahlem Konferenzen, Berlin 1986

Authors and Affiliations

  • U. B. Kaupp
    • 1
  • K.-W. Koch
    • 1
  1. 1.Abteilung BiophysikUniversität OsnabrückOsnabrückF.R. Germany

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