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Induction of retinal degeneration in a crab by light and okadaic acid in vitro: Comparison with the Drosophila light-dependent retinal degeneration mutant w rdgBKS222

Published online by Cambridge University Press:  02 June 2009

A. D. Blest ,
M. Carter ,
J. A. Clausen ,
S. Stowe ,
S. C. Trowell  and
Y. Tsukitani
A. D. Blest
Affiliation:
Developmental Neurobiology Group, Research School of Biological Sciences, Australian National University, Australia
M. Carter
Affiliation:
Developmental Neurobiology Group, Research School of Biological Sciences, Australian National University, Australia
J. A. Clausen
Affiliation:
Developmental Neurobiology Group, Research School of Biological Sciences, Australian National University, Australia
S. Stowe
Affiliation:
Developmental Neurobiology Group, Research School of Biological Sciences, Australian National University, Australia
S. C. Trowell
Affiliation:
Developmental Neurobiology Group, Research School of Biological Sciences, Australian National University, Australia Entomology Division, CSIRO, Canberra, Australia
Y. Tsukitani
Affiliation:
Fujisawa Pharmaceutical Co., Ltd., Tokyo, Japan
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Abstract

Retinae of the crab Leptograpsus which had been maintained on a 12-h light/12-h dark cycle were cultured in vitro and exposed to 1 μM okadaic acid (OKA) at 0.75 h before light onset. Control retinae were subjected to the same routine and sampled at the same times without OKA treatment. At the concentration used, OKA totally inhibits types 1 and 2A protein phosphatases, minimally inhibits type 2B, and does not affect type 2C. 1 μM OKA provoked a diminution of rhabdom diameter measured at the level of the photoreceptor nuclei in the dark, some ommatidial cartridges being stripped of rhabdomeral microvilli altogether. After 1-h illumination (225–320 lux), further reduction of rhabdom diameter was modest in control retinae but precipitate in those treated with OKA. After 2 h, control rhabdom diameters showed a further, not significant, decline, but OKA had induced a resynthesis of massive structures with the light-microscopic appearance of rhabdoms. Electron microscopy revealed that they were heterogeneous and of the following kinds: (1) a minority of rhabdoms with normally disposed but distorted microvilli; (2) rhabdoms in the throes of events that parody normal assembly; and (3) rhabdomal volumes occupied by saccular organelles or by pleats or ruffles of irregular architecture. The cytoplasm of all such receptors was packed with free and bound ribosomes and endomembranes. The sequence of events parallels that seen during light-induced degeneration of photoreceptors of the Drosophila mutant w rdgBKS222. Preliminary experiments show that a protein kinase activator SC-9 mimics many of these effects in the dark in the presence of 1 μM OKA. As a working hypothesis, it is proposed that light activates protein kinases via diacylglycerols generated by the phototransduction cascade, and that in both crab retinas challenged with OKA and retinas of rdgBKS222 activation of a nuclear regulatory protein by hyperphosphorylation provokes a runaway transcription whose selectivity and extent remain to be determined.

Keywords

Protein phosphatasesOkadaic AcidArthropod rhabdomsPhotoreceptor membrane turnoverDrosophila w rdgBKS222 retinal degeneration mutant
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 1-2 , August 1991 , pp. 35 - 48
Copyright
Copyright © Cambridge University Press 1991

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References

Amster-Choder, O., Houman, F. & Wright, A. (1989). Protein phosphorylation regulates transcription of the β-glucoside utilization operon in Escherichia coli. Cell 58, 847–855.Google Scholar
Arikawa, K., Hicks, J.L. & Williams, D.S. (1990). Identification of actin filaments in the rhabdomeralmicrovilli of Drosophila photo-receptors. Journal of Cell Biology 110, 1992–1998.Google Scholar
Arndt, K.T., Styles, C.A. & Fink, G.R. (1989). A suppressor of a HIS4 transcriptional defect encodes a protein with homology to the catalytic subunit of protein phosphatases. Cell 56, 527–537.CrossRefGoogle Scholar
Biaolojan, C. & Takai, A. (1988). Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases: specificity and kinetics. Biochemical Journal 256, 283–290.Google Scholar
Blest, A.D. (1988a). The turnover of phototransductive membranes in compound eyes and ocelli. Advances in Insect Physiology 20, 1–53.CrossRefGoogle Scholar
Blest, A.D. (1988b). Post-embryonic development of the principal retina of a jumping spider, I: The establishment of receptor tiering by conformational changes. Philosophical Transactions of the Royal Society B (London) 320, 489–504.Google Scholar
Blest, A.D. & Stowe, S. (1990). Dynamic microvillar cytoskeletons in arthropod and squid photoreceptors. Cell Motility and the Cytoskeleton 17, 1–5.CrossRefGoogle Scholar
Blest, A.D., Stowe, S. & Price, G.D. (1980). The sources of acid hydrolases for photoreceptor membrane degradation in a grapsid crab. Cell and Tissue Research 205, 229–244.CrossRefGoogle Scholar
Blest, A.D., Stowe, S., Eddey, W. & Williams, D.S. (1982). The local deletion of a microvillar cytoskeleton from photoreceptors of tipulid flies during membrane turnover. Proceedings of the Royal Society B (London) 215, 469–479.Google Scholar
Cherry, J.R., Johnson, T.R., Dollard, C., Shuster, J.R. & Denis, C.L. (1989). Cyclic-AMP-dependent protein kinase phosphorylates and inactivates the yeast transcriptional activator ARDI. Cell 56, 409–419.CrossRefGoogle Scholar
Cohen, P. (1989). The structure and regulation of protein phosphatases. Annual Reviews of Biochemistry 58, 453–508.Google Scholar
Decouet, H.G. & Tanimura, T. (1987). Monoclonal antibodies provide evidence that rhodopsin in the outer rhabdomeres of Drosophila melanogaster is not glycosylated. European Journal of Cell Biology 44, 50–56.Google Scholar
Dent, P., Lavoinne, A., Nakielny, S., Caudwell, F.B., Watt, P. & Cohen, P. (1990). The molecular mechanism by which insulin stimulates glycogen synthesis in mammalian skeletal muscle. Nature 348, 302–308.Google Scholar
Harris, W.A. & Stark, W.S. (1977). Hereditary retinal degeneration in Drosophila melanogaster: a mutant defect associated with the phototransduction process. Journal of General Physiology 69, 261–291.Google Scholar
Haystead, T.A.J., Sim, A.T.R., Carlino, D., Honnor, R.C., Tsukitani, Y., Cohen, P. & Hardie, D.G. (1989). Effects of the tumour promoter okadaic acid on intracellular protein phosphorylation and metabolism. Nature 337, 28–31.Google Scholar
Hotta, Y. & Benzer, S. (1970). Genetic dissection of the Drosophila nervous system by means of mosaics. Proceedings of the National Academy of Sciences of the U.S.A. 67, 1156–1163.CrossRefGoogle ScholarPubMed
June, C.H., Fletcher, M.C., Ledbetter, J.A., Schieven, G.L., Siegel, J.N., Phillips, A.F. & Samelson, L.E. (1990). Inhibition of tyrosine phosphorylation prevents T-cell receptor-mediated signal transduction, Proceedings of the National Academy of Sciences of the U.S.A. 87, 7722–7726.CrossRefGoogle ScholarPubMed
Kirschfeld, K. & Vogt, K. (1980). Calcium ions and pigment migration in fly photoreceptors. Naturwissenschaften 67, 516–517.CrossRefGoogle Scholar
Lapetina, E.G., Reep, B., Ganong, B.R. & Bell, R.M. (1985). Exogenous sn-1,2-diacylglycerols containing saturated fatty acids function as bioregulators of protein kinase C in human platelets. Journal of Biological Chemistry 260, 1358–1361.CrossRefGoogle ScholarPubMed
Ludolph, C., Pagnanelli, D. & Mote, M.I. (1973). Neural control of proximal screening pigment migration by retinula cells of the swimming crab (Callinectes sapidus). Biological Bulletin 145, 159–170.CrossRefGoogle Scholar
Minke, B., Rubinstein, C.T., Sahly, I., Bar-Nachum, S., Timberg, R. & Selinger, Z. (1990). Phorbol ester induces photoreceptor-specific degeneration in a Drosophila mutant. Proceedings of the National Academy of Sciences of the U.S.A. 87, 113–117.CrossRefGoogle Scholar
Montell, C. & Rubin, G.M. (1988). The Drosophila ninaC locus encodes two photoreceptor cell-specific proteins with domains homologous to protein kinases and the myosin heavy chain head. Cell 52, 755–772.Google Scholar
Montell, C., Jones, K., Zuker, C. & Rubin, G. (1987). A second opsin gene expressed in the ultraviolet sensitive R7 photoreceptor cells of Drosophila melanogaster. Journal of Neuroscience 7, 1558–1566.Google Scholar
Orgad, S., Dudai, Y. & Cohen, P. (1987). The protein phosphatases of Drosophila melanogaster and their inhibitors. European Journal of Biochemistry 164, 31–38.Google Scholar
O'Tousa, J., Baehr, W., Martin, R.L., Hirsch, J., Pak, W.L. & Applebury, M. (1985). The Drosophila ninaE gene encodes an opsin. Cell 40, 839–850.CrossRefGoogle ScholarPubMed
Piekos, W.B. (1987). Multivesicular body formation and function in the light-adapted crayfish retina: a new interpretation. Cell and Tissue Research 249, 541–546.Google Scholar
Piekos, W.B. (1989). Temporal separation of rhabdom shrinkage and MVB formation in the light-adapting crayfish retina. Journal of Experimental Zoology 250, 17–21.Google Scholar
Rubinstein, C.T., Bar-Nachum, S., Selinger, Z. & Minke, B. (1989a). Light-induced retinal degeneration in rdgB (retinal degeneration B) mutant of Drosophila: electrophysiological and morphological manifestations of degeneration. Visual Neuroscience 2, 529–539.CrossRefGoogle ScholarPubMed
Rubinstein, C.T., Bar-Nachum, S., Selinger, Z. & Minke, B. (1989b). Chemically induced retinal degeneration in the rdgB (retinal degeneration B) mutant of Drosophila. Visual Neuroscience 2, 541–551.CrossRefGoogle ScholarPubMed
Schwemer, J. (1984). Renewal of visual pigment in photoreceptors of the blowfly. Journal of Comparative Physiology 154, 535–547.Google Scholar
Schwemer, J. (1986). Turnover of photoreceptor membranes and visual pigment in invertebrates. In The Molecular Mechanism of Photoreception, ed. Stieve, H., Dahlem, Konferenzen, pp. 303–326. Berlin: Springer-Verlag.Google Scholar
Stark, W.S. & Carlson, S.D. (1982). Ultrastructural pathology of the compound eye and optic neuropiles of the retinal degeneration mutant (w rdgBKs222) Drosophila melanogaster. Cell and Tissue Research 225, 11–22.CrossRefGoogle Scholar
Stark, W.S. & Sapp, R. (1987). Ultrastructure of the retina of Drosophila melanogaster: the mutant ora (outer rhabdomeres absent) and its inhibition of degeneration in rdgB (retinal degeneration-B). Journal of Neurogenetics 4, 227–240.Google ScholarPubMed
Stark, W.S., Chen, D.-M., Johnson, M.A. & Frayer, K.L. (1983). The rdgB gene in Drosophila: retinal degeneration in different mutant alleles and inhibition of degeneration by norpA. Journal of Insect Physiology 29, 123–131.Google Scholar
Stowe, S. (1980a). Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk. Cell and Tissue Research 211, 419–440.Google Scholar
Stowe, S. (1980b). Spectral sensitivity and retinal pigment movements in the crab (Leptograpsus variegatus) (Fabricius). Journal of Experimental Biology 87, 73–98.Google Scholar
Stowe, S. (1981). Effects of illumination changes on rhabdom synthesis in a crab. Journal of Comparative Physiology 142, 19–25.CrossRefGoogle Scholar
Stowe, S. (1982). Rhabdom synthesis in isolated eye stalks and retinae of the crab (Leptograpsus variegatus). Journal of Comparative Physiology 148, 313–321.Google Scholar
Stowe, S. (1983a). Light-induced and spontaneous breakdown of the rhabdom of a crab at dawn: depolarization versus calcium levels. Journal of Comparative Physiology 153, 365–375.Google Scholar
Stowe, S. (1983b). Phagocytosis of photoreceptor membrane at dawn in a crab. Cell and Tissue Research 234, 463–467.Google Scholar
Tachibana, Y., Scheur, P.J., Tsukitani, Y., Kncucm, H., Van Engen, D., Clardy, J., Gopichand, Y. & Schmitz, F.J. (1981). Okadaic acid, a cytotoxic polyether from two marine sponges of the genus Halichondria. Journal of the American Chemical Society 103, 2469–2471.CrossRefGoogle Scholar
Trowell, S.C. (1985). Cytochemical distribution and biochemistry of a novel phosphatase in the photoreceptive microvilli of a crab. European Journal of Cell Biology 36, 277–285.Google Scholar
Trowell, S.C. (1988). Partialx purification and characterization of the 4-nitro-phenylphosphatase activity of invertebrate photoreceptor microvilli. Absence of in vitro rhodopsin phosphatase activity. Comparative Biochemistry and Physiology 89, 285–297.Google Scholar
Trowell, S.C. & Carter, M. (1988). The polypeptide composition of the 4-nitro-phenylphosphatase (4-Nppase) of invertebrate photoreceptive microvilli. In Molecular Physiology of Retinal Proteins, ed. Hara, T., Yamada Conference XXI, pp. 415–416. Osaka, Japan: Yamada Science Foundation.Google Scholar
Trowell, S.C., McClean, A., Carter, M. & Davis, D.T. (1989). A phosphatase of undefined function is common to the photoreceptive microvilli of several arthropod species. Cell and Tissue Research 258, 83–90.Google Scholar
Williams, D.S. (1982). Rhabdom size and photoreceptor membrane turnover in a muscoid fly. Cell and Tissue Research 226, 629–639.Google Scholar
Williams, D.S. (1983). Changes of photoreceptor performance associated with the daily turnover of photoreceptor membrane in locusts. Journal of Comparative Physiology 105, 509–519.Google Scholar
Williams, D.S. & Blest, A.D. (1980). Extracellular shedding of photoreceptor membrane in a tipulid fly. Cell and Tissue Research 205, 423–438.CrossRefGoogle Scholar
Wion, D., MacGrogan, D., Houlgatte, R. & Brachet, P. (1990). Phorbol 12-myristate 13-acetate (PMA) increases the expression of the nerve growth factor (NGF) gene in mouse L-929 fibroblasts. FEBS Letters 262, 42–44.CrossRefGoogle ScholarPubMed
Yamada, T., Takeuchi, Y., Komori, N., Kobayashi, H., Sakai, Y., Hotta, Y. & Matsumoto, H. (1990). A 59-kilodalton phosphoprotein in the Drosophila photoreceptor is an arrestin homolog. Science 248, 483–486.Google Scholar
Zuker, C.S., Cowman, A.F. & Rubin, G.M. (1985). Isolation and structure of a rhodopsin gene from Drosophilia melanogaster. Cell 40, 851–858.CrossRefGoogle Scholar
Zwiller, J., Honkanen, R.E. & Boynton, A.L. (1990). Stimulation of DNA synthesis by an inositol polyphosphate-activated protein phosphatase in calcium-deprived rat liver cells. Experimental Cell Research 187, 193–196.CrossRefGoogle ScholarPubMed