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Light-regulated proteins in Limulus ventral photoreceptor cells

Published online by Cambridge University Press:  02 June 2009

Samuel C. Edwards ,
Anne C. Wishart ,
Eric M. Wiebe  and
Barbara-Anne Battelle
Samuel C. Edwards*
Affiliation:
The Whitney Laboratory and the Department of Neuroscience, University of Florida, St. Augustine
Anne C. Wishart
Affiliation:
The Whitney Laboratory and the Department of Neuroscience, University of Florida, St. Augustine
Eric M. Wiebe
Affiliation:
The Whitney Laboratory and the Department of Neuroscience, University of Florida, St. Augustine
Barbara-Anne Battelle
Affiliation:
The Whitney Laboratory and the Department of Neuroscience, University of Florida, St. Augustine
*
Correspondence and reprint requests to: Samuel C. Edwards, The Department of Biology, The University of South Florida, 4202 E. Fowler Avenue, Tampa, FL 33620, USA.
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Abstract

The protein intermediates of the photoresponse and the modulation of this response in invertebrate photoreceptors are largely unknown. As a first step toward identifying these proteins, we have examined light-stimulated changes in protein phosphorylation in preparations of Limulus photoreceptors. Here we show that light modulates the level of phosphorylation of three proteins associated with Limulus ventral photoreceptors: the upper band of a 46-kD protein doublet (46A) and a 122-kD protein, which become more heavily phosphorylated in response to light, and the lower component of the 46-kD doublet (46B), which is phosphorylated in dark-adapted cells, but not in cells maintained in the light. In dark-adapted preparations, 46A is phosphorylated within 30 s after a flash of light and dephosphorylates over a period of many minutes. It is also a major substrate for calcium/calmodulin-dependent protein kinase (Wiebe et al., 1989); therefore, we speculate that 46A is involved in some aspect of dark adaptation. Interestingly, the level of phosphorylation of 46A is the same when measured from preparations maintained in complete darkness or ambient light for at least 1.5 h. The 122-kD phosphoprotein is the same protein which becomes phosphorylated in response to efferent innervation to Limulus eyes (Edwards et al., 1988) and the efferent neurotransmitter, octopamine (Edwards and Battelle, 1987). It may be involved in the increase in retinal sensitivity and the enhanced response of photoreceptors to light that is initiated by efferent innervation. Its role in light-stimulated processes is not clear. The level of phosphorylation of 46B may be most relevant to the long-term state of adaptation of the photoreceptor cell to light and dark.

Keywords

Limulus polyphemusPhotoreceptorsProtein phosphorylationPhototransductionAdaptation
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 2 , August 1989 , pp. 95 - 105
Copyright
Copyright © Cambridge University Press 1989

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References

Battelle, B-A. (1980). Neurotransmitter candidate in the visual system of Limuluspolyphemus: synthesis and distribution of octopamine. Vision Research 20, 911–922.CrossRefGoogle ScholarPubMed
Battelle, B-A. & Evans, J.A. (1984). Octopamine release from centrifugal fibers of the Limulus peripheral visual system. Journal of Neu-rochemistry 42, 71–79.Google ScholarPubMed
Battelle, B-A., Evans, J.A. & Chamberlain, S.C. (1982). Efferent Fibers to Limulus eyes synthesize and release octopamine. Science 216, 1250–1252.CrossRefGoogle Scholar
Bayer, D.S. & Barlow, R.B. Jr, (1978). Limulus ventral eye: physiological properties of photoreceptor cells in organ culture medium. Journal of General Physiology 72, 539–564.CrossRefGoogle ScholarPubMed
Bownds, M.D., Dawes, J., Miller, J. & Stahlman, M. (1972). Phosphorylation of frog photoreceptor membranes induced by light. Nature 237, 125–127.Google ScholarPubMed
Brown, J.E. & Blinks, J.R. (1974). Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Journal of General Physiology 64, 643–665.CrossRefGoogle ScholarPubMed
Classen-Link, I. & Stieve, H. (1981). Time course of dark adaptation in the Limulus ventral nerve photoreceptor–measured as constant response amplitude curve–and its dependence upon extracellular calcium. Biophysics of Structure and Mechanism 7, 336–337.Google Scholar
Edwards, S.C. & Battelle, B-A. (1987). Octpamine- and cyclic AMP-stimulated phosphorylation of a protein in Limulus ventral and lateral eyes. Journal of Neuroscience 7, 2811–2820.CrossRefGoogle ScholarPubMed
Edwards, S.C, Wishart, A.C. & Battelle, B-A. (1987). Light-stimulated phosphorylation of proteins in the Limulus ventral and lateral eyes. Society for Neuroscience Abstracts 13, 1397.Google Scholar
Edwards, S.C., Wishart, A.C., Renninger, G.H., Weibe, E.M. & Battelle, B-A. (1988). Phosphorylation of the 122-kD protein in vivo in Limulus lateral eyes by efferent stimulation. Society for Neuroscience Abstracts 14, 386.Google Scholar
Fein, A. & DeVoe, R.D. (1973). Adaptation in the ventral eye of Limulus is functionally independent of the photochemical cycle, membrane potential, and membrane resistance. Journal of General Physiology 61, 273–289.CrossRefGoogle ScholarPubMed
Fein, A. & Tsacopoulos, M. (1988 a). Light-induced oxygen consumption in Limulus ventral photoreceptors does not result from a rise in intracellular sodium concentration. Journal of General Physiology 91, 515–527.CrossRefGoogle Scholar
Fein, A. & Tsacopoulos, M. (1988 b). Activation of mitochondrial oxidative metabolism by calcium ions in Limulus ventral photoreceptors. Nature 331, 437–440.CrossRefGoogle Scholar
Frank, R.N., Cavanagh, H.D. & Kenyon, K.R. (1973). Light-stimulated phosphorylation of bovine visual pigments by adenosine tri-phosphate. Journal of Biological Chemistry 248, 596–609.CrossRefGoogle Scholar
Gnegy, M.E., Muirhead, N. & Harrison, J.K. (1984). Regulation of calmodulin- and dopamine-stimulated adenylate cyclase activities by light in bovine retina. Journal of Neurochemistry 42, 1632–1640.CrossRefGoogle ScholarPubMed
Heukeshoven, J. & Dernick, R. (1985). Simplified method of silver staining of proteins in polyacrylamide gels and the mechanism of silver staining. Electrophoresis 6, 103–112.CrossRefGoogle Scholar
Kass, L. & Barlow, R.B. Jr, (1984). Efferent neurotransmission of circadian rhythms in Limulus lateral eye, I: Octopamine-induced increases in retinal sensitivity. Journal of Neuroscience 4, 908–917.CrossRefGoogle ScholarPubMed
Kass, L. & Renninger, G.H. (1988). Circadian change in function of Limulus ventral photoreceptors. Visual Neuroscience 1, 3–11.CrossRefGoogle ScholarPubMed
Kass, L., Pelletier, J.L., Renninger, G.H. & Barlow, R.B. Jr, (1988). Efferent neurotransmission of circadian rhythms in Limulus lateral eye, II: Intracellular recordings in vitro. Journal of Comparative Physiology A 164, 95–105.CrossRefGoogle ScholarPubMed
Kuhn, H. & Dreyer, W.J. (1972). Light-dependent phosphorylation of rhodopsin by ATP. FEBS Letters 20, 1–6.CrossRefGoogle ScholarPubMed
Laemmli, U.K. (1970). Cleavage of structural proteins during assembly of the head of the bacteriophage T4. Nature 277, 680–685.CrossRefGoogle Scholar
Lee, R.H., Brown, B.M. & Lolly, R.N. (1984). Light-induced dephosphorylation of a 33 K protein in rod outer segments of rat retina. Biochemistry 23, 1972–1977.CrossRefGoogle Scholar
Levy, S. & Fein, A. (1985). Relationship between light sensitivity and intracellular free calcium concentration in Limulus ventral photoreceptors. Journal of General Physiology 85, 805–841.CrossRefGoogle ScholarPubMed
Lisman, J.E. & Brown, J.E. (1972). The effects of intracellular ionto-phoretic injection of calcium and sodium ions on the light response of Limulus ventral photoreceptors. Journal of General Physiology 59, 701–719.CrossRefGoogle ScholarPubMed
Lisman, J.E. & Brown, J.E. (1975). Effects of intracellular injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. Journal of General Physiology 66, 489–506.CrossRefGoogle ScholarPubMed
Matsumoto, H. & Pak, W.L. (1984). Light-induced phosphorylation of retina-specific polypeptides on Drosophila in vivo. Science 223, 184–186.CrossRefGoogle ScholarPubMed
Nestler, E.J. & Greengard, P. (1984). Protein Phosphorylation in the Nervous System. New York: John Wiley and Sons.Google Scholar
O'Day, P.M. & Gray-Keller, M.P. (1989). Evidence for electrogenic Na+/Ca2+ exchange in Limulus ventral photoreceptors. Journal of General Physiology 93, 473–494.CrossRefGoogle ScholarPubMed
O'Day, P.M. & Lisman, J.E. (1985). Octopamine enhances dark adaptation in Limulus ventral photoreceptors. Journal of Neuroscience 5, 1490–1496.CrossRefGoogle ScholarPubMed
Paulsen, R. & Bentrop, J. (1984). Reversible phosphorylation of opsin induced by irradiation of blowfly retinae. Journal of Comparative Physiology 155, 39–45.CrossRefGoogle Scholar
Paulsen, R. & Bentrop, J. (1986). Light-modulated biochemical events in fly photoreceptors. Fortschritte der Zoologie 33, 299–319.Google Scholar
Payne, R. (1986). Phototransduction by microvillar photoreceptors of invertebrates: mediation of a visual cascade by inositol triphosphate. Photobiology and Photobiophysics 13, 373–397.Google Scholar
Polans, A.S., Hermolin, J. & Bownds, D. (1979). Light-induced dephosphorylation of two proteins in frog rod outer segments. Journal of General Physiology 74, 595–613.CrossRefGoogle ScholarPubMed
Stieve, H. & Andre, E. (1984). Octopamine modulates the sensitivity of Limulus ventral photoreceptors. Zeitschrift fur Naturforschungen 39, 981–985.CrossRefGoogle Scholar
Szuts, E.Z. (1985). Light stimulates phosphorylation of two large membrane proteins in frog photoreceptors. Biochemistry 24, 4176–4184.CrossRefGoogle ScholarPubMed
Takeuchi, Y., Komori, N., Hanley, J.P., Tobin, S.L., Takuma, Y. & Matsumoto, H. (1989). The light-induced phosphorylation of Drosophila photoreceptor-specific protein, 49K, is regulated by calcium ions. Investigative Ophthalmology and Visual Science (Suppl.) 30, 114.Google Scholar
Warren, M.K. & Pierce, S.K. (1982). Two cell volume regulatory systems in the Limulus myocardium: an interaction of ions and quaternary ammonium compounds. Biological Bulletin 163, 504–516.CrossRefGoogle Scholar
Weber, K. & Osborn, M. (1969). The reliability of molecular-weight determination by dodecyl-sulfate-polyacrylamide electrophoresis. Journal of Biological Chemistry 244, 4406–4412.CrossRefGoogle Scholar
Wiebe, E.M., Wishart, A.C., Edwards, S.C. & Battelle, B-A. (1988). Light- and Ca2+/calmodulin-stimulated phosphorylation of photo-receptor proteins in Limulus. Investigative Ophthalmology and Visual Science (Suppl.) 29, 351.Google Scholar
Wiebe, E.M., Wishart, A.C., Edwards, S.C. & Battelle, B-A. (1989). Calcium/calmodulin-stimulated phosphorylation of photoreceptor proteins in Limulus. Visual Neuroscience 3, 107–118.CrossRefGoogle ScholarPubMed