Skip to main content
SpringerLink
Log in

Changes in Protein Phosphorylation and Nucleoside Triphosphates during Phototransduction — Physiological Correlates

  • Conference paper
The Molecular Mechanism of Photoreception

Part of the book series: Dahlem Workshop Reports ((DAHLEM LIFE,volume 34))

Abstract

Illumination of vertebrate rods causes the phosphorylation of the visual pigment rhodopsin, the dephosphorylation of two small proteins, and can also change nucleoside triphosphate levels. Light-induced phosphorylation of invertebrate rhodopsin has also been observed. The physiological roles of these reactions are not understood. Vertebrate rhodopsin is phosphorylated at multiple sites nears its C-terminal end located at the surface of the disc membrane, and it seems likely that this influences its interaction with other proteins regulating the transduction pathway. Both the protein phosphorylation reactions and nucleoside triphosphate changes induced by illumination are slower than conductance changes, and they occur mainly at light levels higher than those required to saturate the conductance. This suggests that they may be more important in regulating adaptation and recovery processes than in triggering the initial conductance changes. After a bright flash rhodopsin phosphorylation occurs over the same time period as the recovery of conductance in the dark, and a GTP decrease is reversed as light sensitivity returns. The correspondence between the measured chemistry and physiology is not obligatory, however, because lowering calcium concentration in the medium accelerates the return of both conductance and sensitivity without influencing the kinetics of either rhodopsin phosphorylation or the GTP return.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aton, B., and Litman, B.J. 1984. Activation of rod outer segment phosphodiesterase by enzymatically altered rhodopsin: A regulatory role for the carboxyl terminus of rhodopsin. Exp. Eye Res. 38: 547–559.

    Article  PubMed  CAS  Google Scholar 

  2. Baylor, D.A.; Lamb, T.D.; and Yau, K.-W. 1979. The membrane current of single rod outer segments. J. Physiol. 288: 589–611.

    PubMed  CAS  Google Scholar 

  3. Berger, S.J.; Devries, G.W.; Carter, J.G.; Schulz, D.W.; Passonneau, P.N.; Lowry, O.H.; and Ferrendelli, J.A. 1980. The distribution of the components of the cyclic GMP cycle in retina. J. Biol. Chem. 255: 3128–3133.

    PubMed  CAS  Google Scholar 

  4. Biernbaum, M.S., and Bownds, M.D. 1979. Influence of light and calcium on guanosine 5′-triphosphate in isolated frog rod outer segments. J. Gen. Physiol. 74: 649–669.

    Article  PubMed  CAS  Google Scholar 

  5. Biernbaum, M.S., and Bownds, M.D. 1985. Frog rod outer segments with attached inner segment ellipsoids as an in vitro model for photoreceptors on the retina. J. Gen. Physiol. 85: 83–105.

    Article  PubMed  CAS  Google Scholar 

  6. Biernbaum, M.D., and Bownds, M.S. 1985. Light-induced changes in GTP and ATP in frog rod photoreceptors: Comparison with recovery of dark current and light sensitivity during dark adaptation. J. Gen. Physiol. 85: 107–121.

    Article  PubMed  CAS  Google Scholar 

  7. Bownds, M.D.; Dawes, J.; Miller, J.; and Stahlman, M. 1972. Phosphorylation of frog photoreceptor membranes induced by light. Nature 237: 125–127.

    CAS  Google Scholar 

  8. Cohen, P. 1982. The role of protein phosphorylation in neural and hormonal control of cellular activity. Nature 296: 613–620.

    Article  PubMed  CAS  Google Scholar 

  9. de Azeredo, F.A.M.; Lust, W.D.; and Passonneau, J.V. 1981. Light-induced changes in energy metabolites, guanine nucleotides, and guanylate cyclase within frog retinal layers. J. Biol. Chem. 256: 2731–2735.

    PubMed  Google Scholar 

  10. De Vries, G.W., and Ferrendelli, J.A. 1983. Localization of an endogenous substrate for cyclic AMP-stimulated protein phosphorylation in retina. Exp. Eye Res. 36: 505–516.

    Article  PubMed  Google Scholar 

  11. Fung, B.K.-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.

    Article  PubMed  CAS  Google Scholar 

  12. Goldberg, N.D.; Ames, A. III; Gander, J.E.; and Walseth, T.F. 1983. Magnitude of increase in retinal cGMP metabolic flux determined by 18O incorporation into nucleotide alpha-phosphoryls corresponds with intensity of photic stimulation. J. Biol. Chem. 258: 9213–9219.

    PubMed  CAS  Google Scholar 

  13. Hamm, H.E., and Bownds, M.D. 1984. A monoclonal antibody to guanine nucleotide binding protein inhibits the light-activated cyclic GMP pathway in frog rod outer segments. J. Gen. Physiol. 84: 265–280.

    Article  PubMed  CAS  Google Scholar 

  14. Harris, H.W.; Levin, N.; and Lux, S.E. 1980. Comparison of the phosphorylation of human erythrocyte spectrin in the intact red cell and in various cell-free systems. J. Biol. Chem. 255: 11521–11525.

    PubMed  CAS  Google Scholar 

  15. Hermolin, J.H.; Karell, M.A.; Hamm, H.E.; and Bownds, M.D. 1982. Calcium and cyclic GMP regulation of light-sensitive protein phosphorylation in frog photoreceptor membranes. J. Gen. Physiol. 79: 633–655.

    Article  PubMed  CAS  Google Scholar 

  16. Hillman, P.; Hochstein, S.; and Minke, B. 1983. Transduction in invertebrate photoreceptors: Role of pigment bistability. Physiol. Rev. 63: 668–772.

    PubMed  CAS  Google Scholar 

  17. Kapoor, C.L., and Chader, G.J. 1984. Endogenous phosphorylation of retinal photoreceptor outer segment proteins by calcium phospholid-dependent protein kinase. Biochem. Biophys. Res. Comm. 3: 1397–1403.

    Article  Google Scholar 

  18. Koshland, D.E.; Goldbeter, A.; and Stock, J.B. 1982. Amplification and adaptation in regulatory and sensory systems. Science 217: 220–225.

    Article  PubMed  CAS  Google Scholar 

  19. Kühn, H. 1974. Light-dependent phosphorylation of rhodopsin in living frogs. Nature 230: 588–590.

    Article  Google Scholar 

  20. Kühn, H. 1981. Interactions of rod cell proteins with the disk membrane: Influences of light, ionic strength, and nucleotides. In Molecular Mechanisms of Photoreceptor Transduction, Current Topics in Membranes and Transport, ed. W.H. Miller, vol. 15, pp. 172–201. New York: Academic Press.

    Google Scholar 

  21. Kühn, H., and Bader, S. 1976. The rate of rhodopsin phosphorylation in isolated retinas of frog and cattle. Biochim. Biophys. Acta 428: 13–18.

    Article  PubMed  Google Scholar 

  22. Kühn, H., and Dreyer, W.J. 1972. Light dependent phosphorylation of rhodopsin by ATP. FEBS Lett. 20: 1–6.

    Article  PubMed  Google Scholar 

  23. Lamb, T.D. 1980. Spontaneous quantal events induced in toad rods by pigment bleaching. Nature 287: 349–351.

    Article  PubMed  CAS  Google Scholar 

  24. Lee, R.H.; Brown, B.M.; and Lolley, R.N. 1984. Light-induced dephosphorylation of a 33 K protein in rod outer segments of rat retina. Biochemistry 23: 1972–1977.

    Article  PubMed  CAS  Google Scholar 

  25. Liebman, P.A., and Pugh, E.N. 1980. ATP mediates rapid reversal of cyclic GMP phosphodiesterase activation in visual receptor membranes. Nature 287: 734–736.

    Article  PubMed  CAS  Google Scholar 

  26. Lisman, J. 1985. The role of metarhodopsin in the generation of quantum bumps in UV-receptors in Limulus media eye: Evidence for reverse-reactions into an active state. J. Gen. Physiol., in press.

    Google Scholar 

  27. Manning, D.R.; Disalvo, J.; and Stull, J.T. 1980. Protein phosphorylation: quantitative analysis in vivo and in intact cell systems. Molec. Cell Endocrin. 19: 1–19.

    Article  CAS  Google Scholar 

  28. Matsumoto, H., and Pak, W.L. 1984. Light-induced phosphorylation of retina-specific polypeptides of Drosophua in vivo. Science 223: 184–186.

    Article  PubMed  CAS  Google Scholar 

  29. Miller, J.A., and Paulsen, R. 1975. Phosphorylation and dephosphorylation of frog rod outer segment membranes as part of the visual process. J. Biol. Chem. 250: 4427–4432.

    PubMed  CAS  Google Scholar 

  30. Miller, J.A.; Paulsen, R.; and Bownds, M.D. 1977. Control of light-activated phosphorylation in frog photoreceptor membranes. Biochemistry 16: 2633–2639.

    Article  PubMed  CAS  Google Scholar 

  31. Nestler, E.J., and Greengard, P. 1983. Protein phosphorylation in the brain. Nature 305: 583–588.

    Article  PubMed  CAS  Google Scholar 

  32. Newsholme, E.A.; Challis, R.A.J.; and Crabtree, B. 1984. Substrate cycles: their role in improving sensitivity in metabolic control. Trends Biochem. Sci. 9: 277–280.

    Article  CAS  Google Scholar 

  33. Owens, C.O., and Ohad, I. 1982. Phosphorylation of Chlamydomonas reinhardi chloroplast membrane proteins in vivo and in vitro. J. Cell Biol. 93: 712–718.

    Article  PubMed  CAS  Google Scholar 

  34. Paulsen, R., and Bentrop, J. 1984. Reversible phosphorylation of opsin induced by irradiation of blowfly retinae. J. Comp. Physiol. 155: 39–46.

    Article  CAS  Google Scholar 

  35. Paulsen, R., and Hoppe, I. 1978. Light-activated phosphorylation of cephalopod rhodopsin. FEBS Lett. 96: 55–58.

    Article  PubMed  CAS  Google Scholar 

  36. Pfister, C.; Kühn, H.; and Chabre, M. 1983. Interaction between photoexcited rhodopsin and peripheral enzymes in frog retinal rods. Influences on the postmetarhodopsin II decay and phosphorylation rate of rhodopsin. Eur. J. Biochem. 15: 489–499.

    Article  Google Scholar 

  37. Polans, A.S.; Hermolin, J.; and Bownds, M.D. 1979. Light-induced dephosphorylation of two proteins in frog rod outer segments. J. Gen. Physiol. 74: 595–613.

    Article  PubMed  CAS  Google Scholar 

  38. Robinson, W.E., and Hagins, W.A. 1979. GTP hydrolysis in intact rod outer segments and the transmitter cycle in visual excitation. Nature 280: 398–400.

    Article  PubMed  CAS  Google Scholar 

  39. Shacter-Norman, E.; Chock, P.B.; and Stadtman, E.R. 1983. Protein phosphorylation as a regulatory device. Phil. Trans. Roy. Soc. Lond. B 302: 157–166.

    Article  Google Scholar 

  40. Shichi, H.; Yamamoto, K.; and Somers, R.L. 1984. GTP binding protein: Properties and lack of activation by phosphorylated rhodopsin. Vision Res. 24: 1523–1531.

    Article  PubMed  CAS  Google Scholar 

  41. Shuster, T.A., and Farber, D.B. 1984. Phosphorylation in sealed rod outer segments: effects of cyclic nucleotides. Biochemistry 23: 515–521.

    Article  PubMed  CAS  Google Scholar 

  42. Sitaramayya, A., and Liebman, P.A. 1983. Phosphorylation of rhodopsin and quenching of cyclic GMP phosphodiesterase. Activation by ATP and weak bleaches. J. Biol. Chem. 258: 12106–12109.

    PubMed  CAS  Google Scholar 

  43. Stern, J.; Chinn, K.; Robinson, P.; and Lisman, J. 1985. The effect of nucleotides on the rate of spontaneous quantum bumps in Limulus ventral photoreceptors. J. Gen. Physiol., in press.

    Google Scholar 

  44. Vandenberg, C.A., and Montai, M. 1984. Light-regulated events in invertebrate photoreceptors. 2. Light-regulated phosphorylation of rhodopsin and phosphoinositides in squid photoreceptor membranes. Biochemistry 23: 2347–2352.

    Article  PubMed  CAS  Google Scholar 

  45. Walter, U. 1984. Cyclic-GMP-regulated enzymes and their possible physiological functions. In Advances in Cyclic Nucleotide and Protein Phosphorylation Research, ed. P. Greengard et al., vol. 17, pp. 249–257. New York: Raven Press.

    Google Scholar 

  46. Weller, M.; Virmaux, N.; and Mandel, P. 1975. Role of light and rhodopsin phosphorylation in control of permeability of retinal rod outer segment discs to Ca2+. Nature 256: 68–70.

    Article  PubMed  CAS  Google Scholar 

  47. Wilden, U., and Kühn, H. 1982. Light-dependent phosphorylation of rhodopsin: number of phosphorylation sites. Biochemistry 21: 3014–3022.

    Article  PubMed  CAS  Google Scholar 

  48. Zuckerman, R.; Buzdygon, B.; and Liebman, P. 1984. Characterization of the 48 kilodalton protein of retinal rod outer segments as a light-dependent ATP binding protein. Inv. Opthalmol. Vis. Sci. 25: 112.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Molecular Biology and Dept. of Zoology, University of Wisconsin, Madison, WI, 53706, USA

    M. D. Bownds & E. Brewer

Authors
  1. M. D. Bownds
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Brewer
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

H. Stieve

Rights and permissions

Reprints and permissions

Copyright information

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

About this paper

Cite this paper

Bownds, M.D., Brewer, E. (1986). Changes in Protein Phosphorylation and Nucleoside Triphosphates during Phototransduction — Physiological Correlates. In: Stieve, H. (eds) The Molecular Mechanism of Photoreception. Dahlem Workshop Reports, vol 34. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-70444-4_10

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-70444-4_10

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-70446-8

  • Online ISBN: 978-3-642-70444-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation