Skip to main content
SpringerLink
Log in

Photoreceptors of the retina and pinealocytes of the pineal gland share common components of signal transduction

  • Original Articles
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

Light absorbed by retinal photoreceptors triggers a cascade of reactions that initiate cGMP hydrolysis, cation channel closure and membrane hyperpolarization. Down-regulation of the cascade involves additional proteins that interfere with amplification along the cascade. Pinealocytes are activated by norepinephrine during the dark phase of the day/night cycle. Mature pinealocytes of the mammalian pineal express the known photoreceptor proteins that are implicated in down-regulation of the visual cascade, but the cascade components that produce cGMP hydrolysis and membrane hyperpolarization are absent. Pinealocytes accumulate cyclic AMP minimally when norepinephrine activates their beta adrenergic receptors alone, but the response is potentiated by the simultaneous activation of their alpha-1 adrenergic receptors. A model is proposed whereby phosducin, a phosphoprotein that binds the beta, gamma subunit of G-proteins, could modulate the synthesis of cyclic AMP by buffering the amount of beta, gamma G-protein subunits that are available for activating adenylate cyclase.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Klein, D. C., and Moore, R. Y. 1979. Pineal N-acetyltransferase and hydroxyindole-O-methyltransferase control by the retinohypothalmic tract and the suprachiasmatic nucleus. Brain Res. 174:245–262.

    Google Scholar 

  2. Reiter, R. J. 1988. Intrinsic rhythms of the pineal gland and associated hormone cycles in body fluids. Pages 5–10,in Reinberg, A., Smolenshky, M. and Labrecque, G. (eds.), Annual Review of Chronopharmacology, Pergamon Press, Oxford.

    Google Scholar 

  3. Lolley, R. N., and Lee, R. H. 1990. Cyclic GMP and Photoreceptor Function. The FASEB Journal 4:3001–3008.

    Google Scholar 

  4. Hagins, W. A., Penn, R. D. and Yoshikami, S. 1970. Dark current and photocurrent in retinal rods. Biophys. J. 10:380–412.

    Google Scholar 

  5. Yau, K.-W., and Nakatani, K. 1985. Light-induced reduction of cytoplasmic free calcium in retinal rod outer segment. Nature. Lond. 313:579–581.

    Google Scholar 

  6. Applebury, M. L. and Hargrave, P. A. 1986. Molecular Biology of the visual pigments. Vision Res. 26:1881–1895.

    Google Scholar 

  7. Fung, B., Hurley, J., and Stryer, L. 1981. Flow of information in the light-triggered cyclic nucleotide cascade of vision. Proc. Natl. Acad. Sci. USA, 78:152–56.

    Google Scholar 

  8. Baehr, W., Devlin, M. J., and Applebury, M. L. 1979. Isolation and characterization of cGMP phosphodiesterase from bovine rod outer segments. J. Biol. Chem. 254:11669–11677.

    Google Scholar 

  9. Hurley, J. B. and Stryer, L. 1982. Purification and characterization of gamma regulatory subunit of the cyclic GMP phosphodiesterase from retinal rod outer segments. J. Biol. Chem. 257:11094–11099.

    Google Scholar 

  10. Wensel, T. G., and Stryer, L. 1990. Activation mechanism of retinal rod cyclic GMP phosphodiesterase from bovine rod outer segments. Biochemistry 29:2155–2161.

    Google Scholar 

  11. Liebman, P. A., and Pugh, E. N., Jr. 1979. The control of phosphodiesterase in rod disk membranes: kinetics, possible mechanism and significance for vision. Vision Res. 19:37–38.

    Google Scholar 

  12. Cook, N. J., Molday, L. L., Reid, D., Kaupp, B., and Molday, R. S. 1989. The cGMP-gated channel of bovine rod photoreceptor is localized exclusively in the plasma membrane. J. Biol. Chem. 264:6996–6999.

    Google Scholar 

  13. Hurwitz, R. L. 1991. Affinity purification of the photoreceptor cGMP-gated cation channel. J. Biol. Chem. 266:7975–7977.

    Google Scholar 

  14. Stryer, L. 1986. Cyclic GMP cascade of vision. Ann. Rev. Neurosci. 9:87–110.

    Google Scholar 

  15. Kuhn, H. 1978. Light-regulated binding of rhodopsin kinase and other proteins to cattle photoreceptor membranes. Biochemistry 17:4389–4395.

    Google Scholar 

  16. Wilden, U., Hall, S. W., and Kuhn, H. 1986. Phosphodiesterase activation by photoexcited rhodopsin is quenched when rhodopsin is phosphorylated and binds the intrinsic 48-kDa protein of rod outer segments. Proc. Natl. Acad. Sci. U.S.A. 83:1174–1178.

    Google Scholar 

  17. Lee, R., Lieberman, B. and Lolley, R. 1987. A novel complex from bovine visual cells of a 33,000-dalton phosphoprotein with β- and τ-Transducin: purification and subunit structure. Biochemistry, 26:3983–3989.

    Google Scholar 

  18. Ho, Y.-K., Ting, T. D., Lolley, R. N., and Lee, R. H., 1990. Interaction of the 33kDa phosphoprotein (phosducin) and transducin of rod photoreceptor cells. Invest. Ophthalmol. Vis. Res. (Suppl) 31:215.

    Google Scholar 

  19. Vanecek, J., Sugden, D., Weller, J., and Klein, D. C. 1985. Atypical synergistic alpha and beta-adrenergic regulation of adenosine 3′,5′ monophosphate and guanosine 3′,5′ monophosphate in cultured rat pinealocytes. Endocrinology 116:2167–2173.

    Google Scholar 

  20. Reig, J. A., Yu, L., and Klein, D. C. 1990. Pineal transduction: adrenergic-cyclic-AMP-dependent phosphorylation of cytuplasmic 33 kDa protein (MEKA) which binds beta, gamma-complex of transducin. J. Biol. Chem. 265:5816–5824.

    Google Scholar 

  21. Adamus, G., Palcqewski, K., Carruth, M., McDowell, J. H., and Hargrave, P. A. 1989. Visual transduction system in the rat pineal gland: Evidence for rhodopsin and rhodopsin kinase. Invest. Ophthalmol. Vis. Sci. (Suppl) 30:284.

    Google Scholar 

  22. Sommers, R. L., and Klein, D. C. 1984. Rhodopsin kinase activity in the mammalian pineal gland and other tissues. Science 226:182–184.

    Google Scholar 

  23. Craft, C. M., Whitmore, D. H., and Donoso, L. A. 1990. Differential expression of mRNA and protein encoding retinal and pineal S-antigen during the light/dark cycle. J. Neurochem. 55:1461–1473.

    Google Scholar 

  24. Craft, C. M., Lolley, R. N., Seldin, M. F., and Lee, R. H. 1991. Rat pineal gland phosducin: cDNA isolation, nucleotide sequence and chromosomal assignment in the mouse. Genomics 10:400–409.

    Google Scholar 

  25. Lohse, M. J., Benovic, J. L., Codina, J., Caron, M. G., and Lefkowitz, R. J. 1990. B-Arrestin: A protein that regulates B-adrenergic receptor function. Science 248:1547–1550.

    Google Scholar 

  26. Lee, R. H., Brown, B. M., and Lolley, R. N. 1990. Protein kinase A phosphorylates retinal phosducin on serine 73in situ. J. Biol. Chem. 265:15860–15866.

    Google Scholar 

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

    Google Scholar 

  28. Lee, R. H., Lieberman, B. S., and Lolley, R. N. 1990. Retinal accumulation of the phosducin/Tβτ and transducin complexes in developing normal mice and in mice and dogs with inherited retinal degeneration. Exp. Eye Res. 51:325–333.

    Google Scholar 

  29. Lee, R. H., Fowler, A., McGinnis, J. F., Lolley, R. N., and Craft, C. M. 1990. Amino acid and cDNA sequence of bovine phosducin, a soluble phosphoprotein from photoreceptor cells. J. Biol. Chem. 265:15867–15873.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Cell Biology and Jules Stein Eye Institute, UCLA School of Medicine, 90024, Los Angeles, California

    Richard N. Lolley & Rehwa H. Lee

  2. the Developmental Neurology Laboratory, Veterans Administration Medical Center, 91343, Sepulveda, California

    Richard N. Lolley & Rehwa H. Lee

  3. Laboratory of Molecular Neurogenetics, Department of Psychiatry, University of Texas Southwestern Medical Center and Veterans Administration Medical Center, 75238, Dallas, Texas

    Cheryl M. Craft

Authors
  1. Richard N. Lolley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cheryl M. Craft
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rehwa H. Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Special issue dedicated to Dr. Frederick E. Samson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lolley, R.N., Craft, C.M. & Lee, R.H. Photoreceptors of the retina and pinealocytes of the pineal gland share common components of signal transduction. Neurochem Res 17, 81–89 (1992). https://doi.org/10.1007/BF00966868

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00966868

Key Words

Search

Navigation