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Accumulation of calcium in degenerating photoreceptors of several Drosophila mutants

Published online by Cambridge University Press:  02 June 2009

Iman Sahly ,
Walter H. Schröder ,
Karl Zierold  and
Baruch Minke
Iman Sahly
Affiliation:
Institut für Biologische Informationsverarbeitung, KFA Jülich, Germany Department of Physiology and the Minerva Center for Studies of Visual Transduction, the Hebrew University–Hadassah Medical School, Jerusalem 91120, Israel
Walter H. Schröder
Affiliation:
Institut für Biologische Informationsverarbeitung, KFA Jülich, Germany
Karl Zierold
Affiliation:
Max-Planck-lnstitut für molekulare Physiologie, 4600 Dortmund, Germany
Baruch Minke
Affiliation:
Department of Physiology and the Minerva Center for Studies of Visual Transduction, the Hebrew University–Hadassah Medical School, Jerusalem 91120, Israel
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Abstract

The hypothesis that a large, possibly toxic, increase in cellular calcium accompanies photoreceptor cell degeneration in several different Drosophila mutants was tested. The calcium content of wild type and mutant photoreceptors of Drosophila was measured using rapid freezing of the eyes and energy-dispersive x-ray analysis (e.d.x.) of cryosections and semithin sections of cryosubstituted material. Light- and dark-raised mutants of the following strains were studied: retinal degeneration B (rdgB); retinal degeneration C (rdgC); neither inactivation nor afterpotential C (ninaC), and no receptor potential A (norpA). These are light-dependent retinal degeneration mutants in which the affected gene products had been previously shown as myosin-kinase (ninaC), calcium-dependent phosphoprotein phosphatase (rdgC), phosphoinositide transfer protein (rdgB), and phospholipase C (norpA). In light-raised mutants, ommatidia of variable degrees of degeneration were observed. Mass-dense globular bodies of 200–500 nm diameter in relatively large quantities were found in the degenerating photoreceptor of all the mutants tested. These subcellular globules were found to have a very high calcium content, which was not found in wild type or in nondegenerating photoreceptors of the mutants. Nondegenerating photoreceptors were found not only in dark-raised mutants, but in smaller quantities also in light-raised mutants. Usually these globular structures contained high levels of phosphorus, indicating that at least part of the calcium in the mutant photoreceptors is precipitated as calcium phosphate. The results indicate that a large increase in cellular calcium accompanies light-induced photoreceptor degeneration in degenerating Drosophila mutants even when induced by very different mutations, suggesting that the calcium accumulation is a secondary rather than a primary effect in the degeneration process.

Keywords

Energy-dispersive X-ray analysisCryosectionCryosubstitutionRetinal degeneration
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 4 , July 1994 , pp. 763 - 772
Copyright
Copyright © Cambridge University Press 1994

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References

Blest, A.D., Stowe, S., Carter, M., O'Gara, E. & Delaney, A. (1992). Light-dependent endocytosis of crab rhabdomeral membrane potentiated by okadaic acid is reduced by either of two inhibitors of protein kinase C, or by a calcium-channel blocking agent, diltiazem. Journal of Comparative Physiology A 171, 523–532.CrossRefGoogle Scholar
Bloomquist, B.T., Shortridge, R.D., Schneuwly, S., Pedrew, M., Montell, C, Steller, H., Rubin, G. & Pak, W.L. (1988). Isolation of a putative phospholipase C gene of the Drosophila norpA and its role in phototransduction. Cell 54, 723–733.CrossRefGoogle ScholarPubMed
Byk, T., Bar-Yaacov, M., Doza, Y.N., Minke, B. & Selinger, Z. (1993). Regulatory arrestin cycle secures the fidelity and maintenance of the fly photoreceptor cell. Proceedings of the National Academy Sciences of the U.S.A. 90, 1907–1911.CrossRefGoogle ScholarPubMed
Fain, L. & Schroder, W. (1985). Calcium content and calcium exchange in dark-adapted toad rods. Journal of Physiology 368, 641–665.CrossRefGoogle ScholarPubMed
Farber, L. (1981). The role of calcium in cell death. Life Sciences 29, 1289–1295.CrossRefGoogle ScholarPubMed
Hardie, R.C. & Minke, B. (1992). The trp gene is essential for a light-activated calcium channel in Drosophila photoreceptors. Neuron 8, 643–651.Google Scholar
Hardie, R.C. & Minke, B. (1993). Novel Ca2+ channel underlying transduction in Drosophila photoreceptors: Implications for phosphoinositide-mediated Ca2+ mobilization. Trends in Neuroscience 16, 371–376.CrossRefGoogle ScholarPubMed
Harris, W.A. & Stark, W.L. (1977). Hereditary retinal degeneration in Drosophila melanogaster. A mutant defect associated with the phototransduction process. Journal of General Physiology 69, 261–291.CrossRefGoogle ScholarPubMed
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
Joy, D.C., Bunn, R.D. & Joy, C.S. (1992). Mac X-ray: The NIST “DTSA’ program and the 4Pi analysis boards. Scanning 14, 233–240.CrossRefGoogle Scholar
Matsumoto, H., Isono, K., Pye, Q. & Pak, W.L. (1987). Gene encoding cytoskeletal proteins in Drosophila rhabdomeres. Proceedings of the National Academy of Sciences of the U.S.A. 84, 985–989.CrossRefGoogle ScholarPubMed
Meyertholen, E.P., Stein, P.J., Williams, M.A. & Ostroy, S.E. (1987). Studies of the Drosophila norpA phototransduction mutant. II. Photoreceptor degeneration and rhodopsin maintenance. Journal of Comparative Physiology A 161, 793–798.CrossRefGoogle ScholarPubMed
Minke, B., Rubinstein, C, 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
Minke, B. & Selinger, Z. (1992). The inositol-lipid pathway is necessary for light excitation in fly photoreceptors. In Sensory Transduction, ed. Corey, D. & Roper, S.D., pp. 201–217. New York: Rockefeller University Press.Google Scholar
Minke, B. & Selinger, Z. (1991). Inositol lipid pathway in fly photoreceptors, excitation, calcium mobilization and retinal degeneration. In Progress in Retinal Research, Vol. II, ed. Osborne, N.N., & Chader, G.J., pp. 99–124. Oxford: Pergamon Press.Google 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, 757–772.CrossRefGoogle ScholarPubMed
Ostroy, S.E. (1978). Characteristics of Drosophila rhodopsin in wild-type and norpA vision transduction mutants. Journal of General Physiology 72, 717–732.CrossRefGoogle ScholarPubMed
Pak, W.L. (1975). Mutations affecting the vision of Drosophila melanogaster. In Handbook of Genetics, Vol. 3. ed. King, R.C, pp. 703–733. New York: Plenum Publishing Corp.Google Scholar
Pak, W.L. (1979). Study of photoreceptor function using Drosophila mutants. In Neurogenetics: Genetic Approach to the Nervous System, ed. Breakefield, X., pp. 67–99. New York: Elsevier North-Holland.Google Scholar
Porter, J.A., Hicks, J.L., Williams, D.S. & Montell, C. (1992). Differential localizations of and requirements for the two Drosophila ninaC kinase/myosins in photoreceptor cells. Journal of Cell Biology 116, 683–693.CrossRefGoogle ScholarPubMed
Porter, J.A. & Montell, C. (1993). Distinct roles of the Drosophila nina C kinase and myosin domains revealed by systematic mutagenesis. Journal of Cell Biology 122, 601–612.CrossRefGoogle Scholar
Rebhuhn, L.I. (1972). Freeze substitution and freeze drying. The Principles and Techniques of Electron Microscopy–Biological Applications, Vol. 2, ed. Hayat, M.A., pp. 3–42. New York: Van Nostrand Reinhold Co.Google Scholar
Rubinstein, C., Bar-Nachum, S., Selinger, Z. & Minke, B. (1989 a). Chemically-induced retinal degeneration in rdgB (retinal degeneration B) mutant of Drosophila. Visual Neuroscience 2, 541–551.CrossRefGoogle ScholarPubMed
Rubinstein, C, Bar-Nachum, S., Selinger, Z. & Minke, B. (1989 b). Light-induced retinal degeneration in rdgB (retinal degeneration B) mutant of Drosophila: Electrophysiological manifestations of degeneration. Visual Neuroscience 2, 529–539.CrossRefGoogle ScholarPubMed
Sahly, I., Bar-Nachum, S., Suss-Toby, E., Rom, A., Peretz, A., Kleiman, J., Byk, T., Selinger, Z. & Minke, B. (1992). Calcium channel blockers inhibit retinal degeneration in the rdgB mutant of Drosophila. Proceedings of the National Academy of Sciences of the U.S.A. 89, 435–439.CrossRefGoogle ScholarPubMed
Schroder, W.H. (1981). Quantitative LAMMA analysis of biological specimens. I. Standards II. Isotope Labeling. Fresenius Zeitschrift fur Analytische Chemie 308, 212–217.CrossRefGoogle Scholar
Schroder, W.H. & Fain, G.L. (1984). Light-dependent calcium release from photoreceptors measured by laser micro-mass analysis. Nature 309, 268–270.Google Scholar
Smith, D.P., Ranganathan, R., Hardy, R.W., Marx, J., Tsuchida, T. & Zuker, C.S. (1991). Photoreceptor deactivation and retinal degeneration mediated by a photoreceptor-specific protein kinase C. Science 254, 1478–1484.CrossRefGoogle ScholarPubMed
Spurr, A.R. (1969). A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructurat Research 26(1), 31–43.CrossRefGoogle ScholarPubMed
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., Sapp, R. & Schilly, D. (1988). Rhabdomere turnover and rhodopsin cycle: Maintenance of retinula cells in Drosophila melanogaster. Journal of Neurocytology 17, 499–509.CrossRefGoogle ScholarPubMed
Stark, W.S. & Carlson, S.D. (1982). Ultrastructure pathology of the compound eye and optic neuropile of retinal degenerative mutant (rdgBKS122) Drosophila melanogaster. Cell and Tissue Research 225, 11–22.CrossRefGoogle Scholar
Steele, F. & O'Tousa, J.E. (1990). Rhodopsin activation causes retinal degeneration in Drosophila rdgC mutant. Neuron 4, 883–890.CrossRefGoogle ScholarPubMed
Steele, F.R., Washburn, T., Rieger, R. & O'Tousa, J.E. (1992). Drosophila retinal degeneration C (rdgC) encodes a novel serine/threonine protein phosphatase. Cell 69, 669–676.CrossRefGoogle ScholarPubMed
Toyoshima, N., Matsumoto, P., Wang, P., Inoue, H., Yoshioka, T., Hotta, Y. & Osawa, T. (1990). Purification and partial amino acid sequences of phosphoinositide-specific phospholipase C of Drosophila eye. Journal of Biological Chemistry 265, 14842–14848.CrossRefGoogle ScholarPubMed
Vihtelic, T.S., Hyde, D.R. & O'Tousa, J.E. (1991). Isolation and characterization of the Drosophila retinal degeneration (rdgB) gene. Genetics 127, 761–768.CrossRefGoogle ScholarPubMed
Walz, B. & Baumann, O. (1989). Calcium-sequestering cell organelles: In situ localization, morphological, and functional characterization. In Progress in Histochemistry and Cytochemistry, Vol. 20, No. 2, ed., Grauman, W., Loioa, Z., Pearse, A.G.A., & Schtebler, T.H., pp. 1–47. Stuttgart, New York: Gustav Fischer Verlag.Google Scholar
Zierold, K. (1986). Preparation of cryosections for biological microanalysis. In The Science of Biological Specimen Preparation 1985. ed. Muller, M., Becker, R.P., Boyde, A. & Wolosewick, J.J., pp. 119–127. AMF O'Hare, Chicago, Illinois: Scanning Electron Microscopy Inc.Google Scholar
Zierold, K. (1988). X-ray microanalysis of freeze dried and frozen-hydrated cryosections. Journal of Electron Microscopic Techniques 9, 65–82.CrossRefGoogle ScholarPubMed
Zinkl, G.M., Mater, L., Studer, K., Sapp, R., Chen, D.-M. & Stark, W.S. (1990). Microphotometric, ultrastructural, and electrophysiological analyses of light-dependent processes on visual receptors in white-eyed wild-type and norpA (no receptor potential) mutant Drosophila. Visual Neuroscience 5, 429–439.CrossRefGoogle ScholarPubMed