Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-13T07:04:47.620Z Has data issue: false hasContentIssue false
  • English
  • Français

Calcium homeostasis in photoreceptor cells of Drosophila mutants inaC and trp studied with the pupil mechanism

Published online by Cambridge University Press:  02 June 2009

Cornelia A. Hofstee  and
Doekele G. Stavenga
Cornelia A. Hofstee
Affiliation:
Department of Biophysics, University of Groningen, Nijenborgh 4, NL-9747 AG, Groningen, The Netherlands
Doekele G. Stavenga
Affiliation:
Department of Biophysics, University of Groningen, Nijenborgh 4, NL-9747 AG, Groningen, The Netherlands
Get access Rights & Permissions [Opens in a new window]

Abstract

The light-driven pupil mechanism, consisting of an assembly of mobile pigment granules inside the photoreceptor cells, has been investigated by in vivo reflection microspectrophotometry in wild type (WT) Drosophila and in the photoreceptor mutants inaC and trp. The pupillary response of a dark-adapted WT eye to a step in light is a monophasic reflectance increase reaching a plateau after ca. 15-s light adaptation. This reflectance change is due to photoreceptor pigment granules that accumulate near the tips of the rhabdomeres under light adaptation and that are withdrawn towards the periphery in the dark (Franceschini & Kirschfeld, 1976). The step response of the pupil mechanism of inaC is triphasic. Strikingly, the reflectance level at light onset is distinctly higher than that in WT, due to a partly aggregated state of the photoreceptor pigment granules near the rhabdomere tips that persists in the dark-adapted state, in line with direct calcium measurements of Peretz et al. (1994b). The step response of the pupil mechanism of inaC is slightly elevated compared to that of WT. The step response in trp is a transient, biphasic reflectance change, approximating a log normal function. This function is also a good approximation of the pulse response in WT and inaC. The intensity range of pupillary sensitivity is about 4 log unit. The range of inaC compared to that of WT is slightly (≈0.5 log unit) shifted towards lower intensities, but that in trp is strongly shifted to higher intensities (≈2.5 log unit). The results can be interpreted with the present knowledge of the primary steps in fly phototransduction and the hypothesis that the local intracellular calcium concentration determines the position of the pigment granules, and hence are in line with the notion that the pupil can be used as a qualitative Ca2+ probe.

Keywords

FruitflyPhotoreceptorAdaptationCalcium
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 2 , March 1996 , pp. 257 - 263
Copyright
Copyright © Cambridge University Press 1996

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

REFERENCES

Barash, S., Suss, E., Stavenga, D.G., Rubinstein, C.T., Selinger, Z. & Minke, B. (1988). Light reduces the excitation efficiency in the nss mutant of the sheep blowfly Lucilia. Journal of General Physiology 92, 307–330.CrossRefGoogle ScholarPubMed
Calman, B.G. & Chamberlain, S.C. (1992). Localization of actin filaments and microtubules in the cells of the Limulus lateral and ventral eyes. Visual Neuroscience 9, 365–375.CrossRefGoogle ScholarPubMed
Connolly, T.M., Lawing, W.J. Jr. & Majerus, P.W. (1988). Protein kinase C phosphorylates human platelet inositol trisphosphate 5′-phosphomonoesterase, increasing the phosphatase activity. Cell 46, 951–958.CrossRefGoogle Scholar
Dolph, P.J., Man-Son-Hing, H., Yarfitz, S., Colley, N.J., Running, Deer J., Spencer, M., Hurley, J.B. & Zuker, C.S. (1994). An eye-specific Gβ subunit essential for termination of the phototransduction cascade. Nature 370, 59–61.CrossRefGoogle Scholar
Franceschini, N. (1972). Pupil and pseudopupil in the compound eye of Drosophila. In Information Processing in the Visual System of Arthropods, ed. Wehner, R., pp. 75–82. Berlin-Heidelberg-New York: Springer.Google Scholar
Franceschini, N. (1975). Sampling of the visual environment by the compound eye of the fly: Fundamentals and applications. In Photoreceptor Optics, ed. Snyder, A.W. & Menzel, R., pp. 98–125. Berlin-Heidelberg-New York: Springer.CrossRefGoogle Scholar
Franceschini, N. & Kirschfeld, K. (1971). Les phénomènes de pseudopupille dans l'oeil composé de Drosophila. Kybernetik 9, 159–182.CrossRefGoogle ScholarPubMed
Franceschini, N. & Kirschfeld, K. (1976). Le contrôle automatique du flux lumineux dans l'oeil composé des Diptéres. Propriétés spectrales, statiques et dynamiques du mécanisme. Biological Cybernetics 21, 181–203.CrossRefGoogle Scholar
Hamdorf, K. & Kirschfeld, K. (1980). Reversible events in the transduction process of photoreceptors. Nature 283, 859–860.CrossRefGoogle ScholarPubMed
Hardie, R.C. & Minke, B. (1992). The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8, 643–651.CrossRefGoogle ScholarPubMed
Hardie, R.C. & Minke, B. (1993). Novel Ca2+ channels underlying transduction in Drosophila photoreceptors: Implications for phosphoinositide-mediated Ca2+ mobilization. Trends in Neuroscience 16, 371–376.CrossRefGoogle ScholarPubMed
Hardie, R.C., Peretz, A., Suss-Toby, E., Rom-Glas, A., Bishop, S.A., Selinger, Z. & Minke, B. (1993). Protein kinase C is required for light adaptation in Drosophila photoreceptors. Nature 363, 634–637.CrossRefGoogle ScholarPubMed
Howard, J. (1984). Calcium enables photoreceptor migration in a mutant fly. Journal of Experimental Biology 113, 471–475.CrossRefGoogle Scholar
Howard, J., Dubs, A. & Payne, R. (1984). The dynamics of phototransduction in insects. Journal of Comparative Physiology A154, 707–718.CrossRefGoogle Scholar
Järemo, Jonson A.-C. & Nilsson, D.-E. (1994). Effects of energy deprivation on the fly pupil mechanism: evidence for a rigor state. Journal of Comparative Physiology A174, 701–706.Google Scholar
King, C.A. & Cronin, T.W. (1993). Cytoskeleton of retinular cells from the stomatopod, Gonodactylus oerstedii: Possible roles in pigment granule migration. Cell Tissue Research 274, 315–328.CrossRefGoogle Scholar
Kirschfeld, K. & Franceschini, N. (1969). Ein Mechanismus zur Steuerung des Lichtflusses in den Rhabdomeren des Komplexauges von Musca. Kybernetik 6, 13–22.CrossRefGoogle ScholarPubMed
Kirschfeld, K. & Vogt, K. (1980). Calcium ions and pigment migration in fly photoreceptors. Naturwissenschaften 67, 516–517.CrossRefGoogle Scholar
Laughlin, S.B. (1980). Neural principles in the visual system. In Handbook of Sensory Physiology, Vol VII/6B, ed. Autrum, H., pp. 196–208. Berlin-Heidelberg-New York: Springer.Google Scholar
LO, M.-V.C. & Pak, W.L. (1981). Light-induced pigment migration in the retinula cells of Drosophila melanogaster. Comparison of wild type with ERG-defective mutants. Journal of General Physiology 77, 155–175.CrossRefGoogle Scholar
Minke, B. (1982). Light-induced reduction in excitation efficiency in the trp mutant of Drosophila. Journal of General Physiology 79, 361–385.CrossRefGoogle ScholarPubMed
Montell, C. & Rubin, G.M. (1989). Molecular characterization of the Drosophila trp locus: A putative integral membrane protein required for phototransduction. Neuron 2, 1313–1323.CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1988). The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334, 661–665.CrossRefGoogle ScholarPubMed
Peretz, A., Suss-Toby, E., Rom-Glas, A., Arnon, A., Payne, R. & Minke, B. (1994 a). The light response of Drosophila photoreceptors is accompanied by an increase in cellular calcium: Effects of specific mutants. Neuron 12, 1257–1267.CrossRefGoogle Scholar
Peretz, A., Sandler, C., Kirschfeld, K., Hardie, R.C. & Minke, B. (1994 b). Genetic dissection of light-induced Ca2+ influx into Drosophila photoreceptors. Journal of General Physiology 104, 1057–1077.CrossRefGoogle ScholarPubMed
Ranganathan, R., Harris, G.L., Stevens, C.F. & Zuker, C.S. (1991 a). A Drosophila mutant defective in extracellular calcium-dependent photoreceptor deactivation and rapid desensitization. Nature 354, 230–232.CrossRefGoogle ScholarPubMed
Ranganathan, R., Harris, W.A. & Zuker, C.S. (1991 b). The molecular genetics of invertebrate phototransduction. Trends in Neurosciences 14, 486–493.CrossRefGoogle ScholarPubMed
Ranganathan, R., Bacskai, B.J., Tsien, R.Y. & Zuker, C.S. (1994). Cytosolic calcium transients: spatial localization and role in Drosophila photoreceptor cell function. Neuron 13, 837–848.CrossRefGoogle ScholarPubMed
Roebroek, J.G.H. & Stavenga, D.G. (1990). On the effective density of the pupil mechanism in fly photoreceptors. Vision Research 8, 1235–1242.CrossRefGoogle Scholar
Ron, D., Chen, C.-H., Caldwell, J., Jamieson, L., Orr, E. & Mochly-Rosen, D. (1994). Cloning of an intracellular receptor for protein kinase C: A homolog of the β subunit of G proteins. Proceedings of the National Academy of Sciences of the U.S.A. 91, 839–843.CrossRefGoogle ScholarPubMed
Selinger, Z., Doza, Y.N. & Minke, B. (1993). Mechanisms and genetics of photoreceptors desensitization in Drosophila flies. Biochimica Biophysica Acta 1179, 283–299.CrossRefGoogle ScholarPubMed
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
Stavenga, D.G. (1975). Optical qualities of the fly eye—an approach from the side of geometrical, physical and waveguide optics. In Photoreceptor Optics, ed. Snyder, A.W. & Menzel, R., pp. 126–144. Berlin-Heidelberg-New York: Springer.CrossRefGoogle Scholar
Stavenga, D.G. (1979). Pseudopupils of compound eyes. In Handbook of Sensory Physiology, Vol VII/6A, ed. Autrum, H., pp. 357–439. Berlin-Heidelberg-New York: Springer.Google Scholar
Stavenga, D.G. (1983). Fluorescence of blowfly metarhodopsin. Biophysics of Structure and Mechanism 9, 309–317.CrossRefGoogle Scholar
Stavenga, D.G. (1989). Pigments in compound eyes. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 152–172. Berlin-Heidelberg-New York-London-Paris-Tokyo: Springer.CrossRefGoogle Scholar
Wilcox, M. & Franceschini, N. (1984). Stimulated drug uptake in a photoreceptor cell. Neuroscience Letters 50, 187–192.CrossRefGoogle Scholar