Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-25T14:04:55.744Z Has data issue: false hasContentIssue false
  • English
  • Français

Calcium/calmodulin-stimulated phosphorylation of photoreceptor proteins in Limulus

Published online by Cambridge University Press:  02 June 2009

Eric M. Wiebe ,
Anne C. Wishart ,
Samuel C. Edwards  and
Barbara-Anne Battelle
Eric M. Wiebe
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
Samuel C. Edwards
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: Barbara-Anne Battelle, The Whitney Laboratory and the Department of Neuroscience, University of Florida, 9505 Ocean Shore Boulevard, St. Augustine, FL 32086, USA.
Get access Rights & Permissions [Opens in a new window]

Abstract

Calcium (Ca2+) is thought to play a major role in the photoresponse of both vertebrates and invertebrates, but the mechanisms through which Ca2+ exerts its effects are unclear. In many systems, some effects of Ca2+ on cellular processes are thought to be mediated via activation of calcium/calmodulin protein kinase (CaCAM-PK) and the phosphorylation of specific proteins. Thus, protein substrates for CaCAM-PK in photoreceptor cells may be important in mediating the effects of Ca2+ on the photoresponse.

In this study, we identify eight substrates for CaCAM-PK found in both the ventral and lateral eyes of Limulus. We focus on a characterization of one of these, a 46-kD substrate. We show that its subcellular distribution in ventral photoreceptors and its isoelectric forms are identical to the 46-kD light-stimulated phosphoprotein (46A) described by Edwards et al. (1989). Furthermore, we present evidence that 46A is unique to photoreceptor cells, and that it is present throughout the cell. Based on the results of this study, and the previous study by Edwards et al. (1989), we propose that 46A is involved in mediating the effects of Ca2+ on Limulus photoreceptor cell function, and that it may be involved in dark adaptation.

Keywords

Limulus polyphemusPhotoreceptorsCalciumCalmodulinProtein phosphorylationAdaptation
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 2 , August 1989 , pp. 107 - 118
Copyright
Copyright © Cambridge University Press 1989

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bass, M., Pant, H.C., Gainer, H. & Soderling, T.R. (1987). Calcium/calmodulin-dependent protein kinase II in squid synaptosomes. Journal of Neurochemistry 49, 1116–1123.CrossRefGoogle Scholar
Battelle, B-A. (1980). Neurotransmitter candidates in the visual system of Limulus polyphemus: synthesis and distribution of octopamine. Vision Research 20, 911–922.CrossRefGoogle ScholarPubMed
Bennett, M.K., Erondu, N.E. & Kennedy, M.B. (1983). Purification and characterization of a calmodulin-dependent protein kinase that is highly enriched in the brain. Journal of Biological Chemistry 258, 12735–12744.CrossRefGoogle Scholar
Bolsover, S.R. & Brown, J.E. (1985). Calcium ion, and intracellular messenger of light-adaptation, also participates in excitation of Limulus photoreceptors. Journal of Physiology 364, 381–393.CrossRefGoogle ScholarPubMed
Bornstein, J.M., Wasterlain, C.G. & Farber, D.B. (1988). A retinal calmodulin-dependent kinase: calcium/calmodulin-stimulated and -inhibited sites. Journal of Neurochemistry 50, 1438–1446.CrossRefGoogle Scholar
Brown, J.E. (1986). Calcium and light adaptation in invertebrate photoreceptors. In The Molecular Mechanisms of Photoreception, ed. Stieve, H., pp. 231–240. New York: Springer-Verlag.CrossRefGoogle Scholar
Brown, J.E. & Blinks, J.R. (1974). Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. Journal of General Physiology 64, 643–665.CrossRefGoogle ScholarPubMed
Brown, J.E., Brown, P.K. & Pinto, L.H. (1977). Detection of light-induced changes of intracellular ionized calcium concentration in Limulus ventral photoreceptors using arsenazo III. Journal of Physiology 267, 299–320.CrossRefGoogle ScholarPubMed
Brown, J.E. & Lisman, J.E. (1975). Intracellular calcium modulates sensitivity and time scale in Limulus ventral photoreceptors. Nature 258, 252–254.CrossRefGoogle ScholarPubMed
Brown, J.E. & Rubin, L.J. (1984). A direct demonstration that inositol-triphosphate induces an increase in intracellular calcium in Limulus photoreceptors. Biochemical and Biophysical Research Communications 125, 1137–1142.CrossRefGoogle Scholar
Brown, J.E., Rubin, L.J., Ghalayini, A.J., Tarver, A.P., Irvine, R.F., Berridge, M.J. & Anderson, R.E. (1984). Myo-inositol poly-phosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature 311, 100–103.CrossRefGoogle Scholar
Chamberlain, S.C. & Barlow, R.B. Jr, (1980). Neuroanatomy of the visual afferents in the horseshoe crab (Limulus polyphemus). Journal of Comparative Neurology 192, 387–400.CrossRefGoogle ScholarPubMed
DeCouet, H.G., Jablonski, P.P. & Perkin, J.L. (1986). Calmodulin associated with rhabdomeral photoreceptor microvilli of arthropods and squid. Cell and Tissue Research 244, 315–319.CrossRefGoogle Scholar
DeRiemer, S.A., Kaczmareck, L.K., Lai, Y., McGuinness, T.L. & Greengard, P. (1984). Calcium/calmodulin-dependent protein phosphorylation in the nervous system of Aplysia. Journal of Neuroscience 4, 1618–1625.CrossRefGoogle ScholarPubMed
Edwards, S.C. & Battelle, B-A. (1987). Octopamine- 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., Wiebe, E.M. & Battelle, B-A. (1989). Light-stimulated phosphorylation and dephosphorylation of proteins in Limulus ventral eye. Visual Neuroscience (submitted).CrossRefGoogle Scholar
Fabiato, A. & Fabiato, F. (1979). Calculator programs for computing the composition of the solutions containing multiple metals and li-gands used for experiments in skinned muscle cells. Journal of Physiology (Paris), 75, 463–505.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). Activation of mitochondrial oxidative metabolism by calcium ions in Limulus ventral photoreceptor. Nature 331, 437–440.CrossRefGoogle ScholarPubMed
Fein, A. & Tsacopoulos, M. (1988 b). Light-induced oxygen consumption in Limulus ventral photoreceptors does not result from a rise in the intracellular sodium concentration. Journal of General Physiology 91, 515–527.CrossRefGoogle Scholar
Gietzen, K., Wuthrich, A. & Bader, H. (1981). R 24571: a new powerful inhibitor of red blood cell Ca2+-transport ATPase and of calmodulin-regulated functions. Biochemical and Biophysical Research Communications 101, 418–425.CrossRefGoogle Scholar
Goldring, J.R., Gonzalez, B., McGuire, J.S. Jr, & DeLorenzo, R.J. (1983). Purification and characterization of a calmodulin-dependent protein kinase from brain cytosol able to phosphorylate tubulin and microtubule-associated protein. Journal of Biological Chemistry 258, 12632–12640.CrossRefGoogle Scholar
Gorman, A.L.F., Levy, S., Nasi, E. & Tillotson, D. (1984). Intracellular calcium measured with calcium-sensitive micro-electrodes and Arsenazo III in voltage-clamped Aplysia neurons. Journal of Physiology 353, 127–142.CrossRefGoogle Scholar
Heukeshoven, J. & Dernick, R. (1985). Simplified method for silver staining of proteins in polyacrylamide gels and the mechanism of silver staining. Electrophoresis 6, 103–112.CrossRefGoogle Scholar
Ivens, I. & Stieve, H. (1984). Influence of the membrane potential on the intracellular light induced Ca2+-concentration change of the Limulus ventral photoreceptor monitored by Arsenazo III under voltage-clamp conditions. Zeitschrift fur Naturforschung 39c, 986–992.CrossRefGoogle Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during assembly of the head of the bacteriophage T4. Nature 277, 680–685.CrossRefGoogle Scholar
Lai, Y., Nairn, A.C., Gorelick, F.S. & Greengard, P. (1987). Ca2+/calmodulin-dependent protein kinase II: identification of autophosphorylation sites responsible for generation of Ca2+/calmodulin-independence. Proceedings of the National Academy of Sciences of the U.S.A. 84, 5710–5714.CrossRefGoogle ScholarPubMed
Levy, S. & Fein, A. (1985). Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. Journal of General Physiology 85, 805–841.CrossRefGoogle Scholar
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 a). Light-induced changes of sensitivity in Limulus ventral photoreceptors. Journal of General Physiology 66, 473–488.CrossRefGoogle ScholarPubMed
Lisman, J.E. & Brown, J.E. (1975 b). Effects of intracellular iontophoretic injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. Journal of General Physiology 66, 489–506.CrossRefGoogle ScholarPubMed
Lisman, J.E., Fain, G.L. & O'Day, P.M. (1982). Voltage-dependent conductances in Limulus ventral photoreceptor. Journal of General Physiology 79, 187–209.CrossRefGoogle Scholar
Lisman, J.E. & Strong, J.A. (1979). The initiation of excitation and light adaptation in Limulus ventral photoreceptors. Journal of General Physiology 73, 219–243.CrossRefGoogle ScholarPubMed
Miller, S.C. & Kennedy, M.B. (1986). Regulation of type II calcium/calmodulin-dependent protein kinase by autophosphorylation. A calcium-triggered switch. Cell 44, 861–870.CrossRefGoogle ScholarPubMed
Nagy, K. & Stieve, H. (1983). Changes in intracellular calcium ion concentration, in the course of dark adaptation measured by Arsenazo III in the Limulus photoreceptor. Biophysics of Structure and Mechanism 9, 207–223.CrossRefGoogle Scholar
Nestler, E.J. & Greengard, P. (1984). Protein Phosphorylation in the Nervous System. New York: Wiley.Google Scholar
Novak-Hofer, I., Lemos, J.R., Villermain, M. & Levttan, I.B. (1985). Calcium- and cyclic nucleotide-dependent protein kinases and their substrates in Aplysia nervous system. Journal of Biological Chemistry 269, 10283–10287.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, 473–495.CrossRefGoogle ScholarPubMed
O'Day, P.M., Lisman, J.E. & Goldring, M. (1982). Functional significance of voltage-dependent conductances in Limulus ventral photoreceptors. Journal of General Physiology 79, 211–232.CrossRefGoogle ScholarPubMed
O'Farrell, P.H. (1975). High resolution two-dimensional electropho-resis of proteins. Journal of Biological Chemistry 250, 4007–4021.CrossRefGoogle Scholar
Owen, J.D. (1981). The effect of external calcium on the light-induced increase in intracellular Ca2+ in Limulus ventral photoreceptors. Biophysical Journal 33, 205a.Google Scholar
Payne, R. (1986). Phototransduction by microvillar photoreceptors of invertebrates: mediation of a visual cascade by inositol trisphosphate. Photobiochemistry and Photobiophysics 13, 373–397.Google Scholar
Payne, R., Corsen, D.W. & Fein, A. (1986). Pressure injection of calcium both excites and adapts Limulus ventral photoreceptors. Journal of General Physiology 88, 107–126.CrossRefGoogle ScholarPubMed
Payne, R. & Fein, A. (1987). Inositol 1,4,5 trisphosphate releases calcium from specialized sites within Limulus photoreceptors. Journal of Cell Biology 104, 933–937.CrossRefGoogle ScholarPubMed
Peterson, G.L. (1977). A simplification of the protein assay method of Lowry et al., which is more applicable. Analytical Biochemistry 83, 346–356.CrossRefGoogle Scholar
Saitoh, T. & Schwartz, J.H. (1985). Phosphorylation-dependent sub-cellular translocation of a Ca2+/calmodulin-dependent protein kinase produces an autonomous enzyme in Aplysia neurons. Journal of Cell Biology 100, 835–842.CrossRefGoogle Scholar
Semple-Roland, S.L. & Ulshafer, R.J. (1989). Analysis of proteins in developing rd (retinal degeneration) chick retina using two-dimensional gel electrophoresis. Experimental Eye Research (in press).CrossRefGoogle Scholar
Waloga, G., Brown, J.E. & Pinto, L.H. (1975). Detection of changes in [Ca2+], from Limulus ventral photoreceptors using Arsenazo III. Biological Bulletin 149, 449–450.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
Wiebe, E.W., Wishart, A.C., Edwards, E.C. & Battelle, B-A. (1988). Light- and Ca2+/calmodulin-stimulated phosphorylation of photoreceptor proteins in Limulus. Investigative Ophthalmology and Visual Science (Suppl.) 29, 351.Google Scholar