Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-17T13:21:22.996Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization of a calcium/calmodulin-dependent protein phosphatase in the Limulus nervous tissue and its light regulation in the lateral eye

Published online by Cambridge University Press:  02 June 2009

D. Z. Ellis  and
S. C. Edwards
D. Z. Ellis
Affiliation:
Department of Biology, Institute for Biomolecular Sciences, University of South Florida, Tampa
S. C. Edwards
Affiliation:
Department of Biology, Institute for Biomolecular Sciences, University of South Florida, Tampa
Get access Rights & Permissions [Opens in a new window]

Abstract

Calcium (Ca2+) plays an integral role in the light response of the photoreceptors in both vertebrate and invertebrate organisms. In the ventral eye of the horseshoe crab, Limulus polyphemus, a flash of light delivered to a dark-adapted photoreceptor stimulates a rapid rise in intracellular free calcium concentration ([Ca2+]i), which in turn mediates light adaptation. It has previously been demonstrated that in Limulus photoreceptors light, via Ca2+, activate s a calcium/calmodulin (Ca2+/CaM)-dependent protein kinase which increases the phosphorylation of arrestin. We now have identifie d biochemically, a calcium/calmodulin-dependent protein phosphatase (Ca2+/CaM PP ) in homogenates of the Limulus lateral and ventral eye, brain, and lateral optic nerve using as a substrate, a 32P-labeled peptide fragment of the regulatory subunit of cAMP-dependent protein kinase (RII). This protein phosphatase shares biochemical properties with calcineurin, a Ca2+/CaM-dependent protein phosphatase (type-2B). Its activity is enhanced by Ca2+, calmodulin and Mn2+; and is inhibited by mastoparan, a calmodulin antagonist, and a synthetic peptide corresponding to the autoinhibitory domain of mammalian calcineurin. Most importantly, light regulates the Ca2+/CaM PP activity in the lateral eye. While there is no difference in basal activity in long-term dark- or light-adapted preparations, Ca2+ enhances Ca2+/CaM PP activity only in long-term light-adapted eyes.

Keywords

Limulus polyphemusPhotoreceptorLight regulationCalciumCalmodulinProtein phosphataseCalcineurin
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 5 , September 1994 , pp. 851 - 860
Copyright
Copyright © Cambridge University Press 1994

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

Aitken, A., Klee, C.B. & Cohen, P. (1984). The structure of the B subunit of calcineurin. European Journal of Biochemistry 139, 663–671.Google Scholar
Blumenthal, D.K., Takio, K., Hensen, R.S. & Krebs, E.G. (1986). Dephosphorylation of cAMP-dependent protein kinase regulatory subunit (type II) by calmodulin-dependent protein phosphatase. Journal of Biological Chemistry 261, 8140–8145.Google Scholar
Bolsover, S.R. & Brown, J.E. (1985). Calcium ion, an intracellular messenger of light-adaptation, also participates in excitation of Limulus photoreceptor. Journal of Physiology 364, 381–391.Google Scholar
Bradford, M.M. (1976). A rapid and sensitive method for the quanti-tation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 131, 248–254.Google Scholar
Brown, J.E. & Blinks, J.R. (1974). Changes in intracellular free calcium concentrations during illumination of invertebrate photoreceptors. Detection with aequorin. Journal of General Physiology 73, 219–243.Google Scholar
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.Google Scholar
Busse, R. & Mulsch, A. (1990). Calcium-dependent nitric oxide synthesis in endothelial cytosol is mediated by calmodulin. FEBS Letters 4, 133–134.Google Scholar
Calman, B.C., Andrews, A.W. & Battelle, B.A. (1992). The 46 kD protein in Limulus photoreceptors is phosphorylated by a calcium/calmodulin-dependent protein kinase. Investigative Ophthalmology and Visual Science 34, 807.Google Scholar
Cohen, P. (1991). Classification of protein-serine-threonine phosphatases: Identification and quantitation in cell extracts. Methods in Enzymology 201, 389–398.Google Scholar
Edwards, S.E., Wishart, A.C., Wiebe, E.M. & Battelle, B.A. (1989). Light-regulated proteins in Limulus ventral photoreceptor cells. Visual Neuroscience 3, 95–105.Google Scholar
Edwards, S.C. & Herrera, D.C. (1991). Protein phosphatases in the photoresponse in Limulus photoreceptor. Investigative Ophthalmology and Visual Science 32, 1008.Google Scholar
Edwards, S.E. (1993). Involvement of serine/threonine protein phosphatases in the photoresponse in Limulus photoreceptor. Advances in Protein Phosphatases 7, 529–542.Google Scholar
Goto, S., Matsukado, Y. & Mihara, Y. (1986). The distribution of calcineurin in rat brain and its relation to extrapyramidal system. Brain Research 397, 161–172.Google Scholar
Harrison, S.M. & Bers, D.M. (1987). The effects of temperature and ionic strength on the apparent Ca-affinity of EGTA and the analogous Ca-chelators BAPTA and dibromo-BAPTA. Biochimica et Biophysica Acta 925, 133–143.Google Scholar
Hashimoto, Y. & Soderling, T. (1988). Regulation of calcineurin by phosphorylation. Identification of the regulatory site phosphorylated by a Ca+/CaM-dependent protein kinase II and protein kinase C. The Journal of Biological Chemistry 264, 16524–16529.Google Scholar
Hashimoto, Y., Perrino, B.A. & Soderling, T.R. (1990). Identification of an autoinhibitory domain in calcineurin. Journal of Biological Chemistry 265, 1924–1927.Google Scholar
Hemmings, H.C. Jr., & Greengard, P. (1986). DARP-32, a dopamine-regulated phosphoprotein. Brain Research 69, 149–158.Google Scholar
Hendey, B., Klee, C. & Maxfield, F. (1992). Inhibition of neutro-phil chemokinesis on vitronectin by inhibitors of calcineurin. Science 258, 296–299.Google Scholar
Ingebritsen, T.S., Stewart, A.A. & Cohen, P. (1983). The protein phosphatases involved in cellular regulation 6. Measurement of type-I and type II protein phosphatases in extracts of mammalian tissue: An assessment of their physiological role. European Journal of Biochemistry 132, 297–304.Google Scholar
Kincaid, R.L., Vaughn, M., Osborne, J.C. Jr., & Tkachuk, V.A. (1982). Calcium-dependent interaction of 5-dimethylamino naphthalene-1-sulfonyl-calmodulin with cyclic nucleotide phospho-diesterase, calcineurin, and troponin-1. Journal of Biological Chemistry 257, 10638–10643.Google Scholar
Kincaid, R., Nightingale, M.S. & Martin, B. (1988). Characterization of a cDNA clone encoding the calmodulin-binding domain of mouse brain calcineurin. Proceedings of the National Academy of Sciences of the U.S.A. 85, 8983–8987.Google Scholar
King, M.M., Huang, C.Y., Chock, B.P., Nairn, A.C., Hemmings, H.C. Jr., Chan, K. & Greengard, P. (1984). Mammalian brain phosphoproteins as substrates for calcineurin. Journal of Biological Chemistry 259, 8080–8083.Google Scholar
Klee, C.B., Draetta, G.A. & Hubbard, M. (1988). Calcineurin. Advances in Enzymology 61, 149–200.Google Scholar
Klee, C.B. (1991). Concerted regulation of protein phosphorylation and dephosphorylation by calmodulin. Neurochemical Research 169, 1059–1065.Google Scholar
Levine, H. III, Smith, D.P., Whitney, M., Malicki, D.M., Dolph, P.J., Smith, G.F., Burkhart, W. & Zuker, C.S. (1991). Isolation of a novel visual-system-specific arrestin: An in vivo substrate for light-dependent phosphorylation. Mechanism for Development 33, 19–26.Google Scholar
Lisman, J.E. & Brown, J.E. (1975). Effects of intracellular ionophoretic injection of calcium buffers on light adaptation in Limulus ventral photoreceptors. Journal of General Physiology 66, 489–506.Google Scholar
Malinow, R., Schulman, H. & Tsien, R. (1989). Inhibition of post-synaptic PKC or CaM K II blocks induction but not expression of LTP. Science 245, 862–866.Google Scholar
Miller, J.L., Fox, D.A. & Litman, B.J. (1986). Amplification of phos-phodiesterase activation is greatly reduced by rhodopsin phosphorylation. Biochemistry 25, 4983–4988.Google Scholar
Novak-Hofer, I., Lemos, J.R., Villermain, M. & Levitan, 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
Payne, R., Walz, B., Levy, S. & Fein, A. (1988). The localization of calcium release by inositol trisphosphate in Limulus photoreceptors and its control in negative feedback. Philosophy Transfer Research Society (London) 320, 359–379.Google Scholar
Roskoski, R. (1983). Assays of protein kinase. Methods in Enzymology 99, 3–6.CrossRefGoogle ScholarPubMed
Shin, J., Richard, E.A. & Lisman, J.E. (1993). Ca2+ is an obligatory intermediate in the excitation cascade of Limulus photoreceptors. Neuron 11, 845–855.Google Scholar
Smith, W.C., Calman, B.G., Hutchinson, L., Greenberg, R.M., Donoso, L.A. & Battelle, B.A. (1993 a). Arrestin from Limulus lateral eyes: Cloning, expression, and localization. Investigative Ophthalmology and Visual Science 34, 807.Google Scholar
Smith, W.C., Eschweiler, A.W., Andrews, A., Greenberg, R.M. & Battelle, B.A. (1993 b). Circadian efferent input into Limulus retina stimulates the phosphorylation of a protein similar to the ninaC gene products of Drosophila. Society for Neuroscience Abstracts 19, 1199.Google Scholar
Steele, F.R., Washburn, T., Rieger, R. & O'Tousa, J. (1992). Drosophila retinal degeneration C (rdg C) encodes a novel serine/thre-onine protein phosphatase. Cell 69, 669–676.Google Scholar
Stewart, A.A., Ingebritsen, T.S., Manalan, A., Klee, C.D. & Cohen, P. (1982). Discovery of a calcium and calmodulin-dependent protein phosphatase. Probable identity with calcineurin (Cam-Bp80). FEBS Letters 137, 80–84.Google Scholar
Tallant, E.A. & Cheung, W.Y. (1983). Ontogeny of a CaM-dependent protein phosphatase. Biochemistry 22, 3630–3635.Google Scholar
Tallant, E.A. & Cheung, W.Y. (1984). Activation of bovine brain calmodulin-dependent protein phosphatase by limited trypsinization. Biochemistry 23, 973–979.Google Scholar
Warren, M.K. & Pierce, S.K. (1982). Two cell volume regulation systems in the Limulus myocardium: An interaction of ions and quaternary ammonium compounds. Biological Bulletin 163, 504–516.Google Scholar
Wlebe, E.M., Wishart, A.C., Edwards, S.C., & Battelle, B.A. (1989). Calcium/calmodulin stimulate phosphorylation of photo-receptor proteins in Limulus. Visual Neuroscience 3, 107–118.Google Scholar
Wolff, D.J. & Sved, D.W. (1985). The divalent cation dependence of bovine brain calmodulin-dependent phosphatase. Journal of Biological Chemistry 260, 4195–4202.Google Scholar
Wright, D., Noiman, E., Chock, P.B. & Chau, V. (1981). Fluoromet-ric assay for adenosine 3′ 5′-cyclic monophosphate-dependent protein kinaseand phosphoprotein phosphatase activities. Proceedings of the National Academy of Sciences of the U.S.A. 78, 6048–6050.Google Scholar
Yang, S.D., Tallant, E.A. & Cheung, W.Y. (1982). Calcineurin is a calmodulin-dependent protein phosphatase. Biochemical and Biophysical Research Communications 106, 1419–1425.Google Scholar