Skip to main content
SpringerLink
Log in

Intracellular Ca2+ concentration and latency of light-induced Ca2+ changes in photoreceptors of the honeybee drone

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

We have measured Cai at rest and upon light stimulation in the photoreceptors of the honeybee drone microfluorometrically with the fluorescent Ca2+ indicator dyes fura-2, fluo-3 and Ca-green 5N.

In darkness, Cai was ∼ 90 nM after 5 min of dark adaptation. A saturating light step caused Cai to rise in the bulk cytoplasm to ∼ 750 nM within 1 s. Our measurements with the low affinity dye Ca-green 5N showed that bright 1-s light flashes cause a rapid increase in Cai which was graded with stimulus intensity. Ca-green 5N fluorescence reached a peak in about 200 ms, and then decayed to a slightly lower sustained plateau. The fluorescence signal peaked, when the receptor potential was repolarizing from its peak to the plateau. This observation is in agreement with the proposal that the peak-to-plateau transition of the receptor potential is caused by the rise in Cai

From our Fluo-3 measurements it appears that the latency of the Ca2+ increase is by 3–4 ms longer than the latency of the receptor potential elicited by bright 100-ms light flashes. This result provides no support for the proposal that Ca2+ mediates the opening of those membrane channels responsible for the upstroke of the receptor potential.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ER:

endoplasmic reticulum

IP3 :

Inositol 1,4,5-trisphosphate

SMC:

submicrovillar cisternae

References

  • Bader CR, Baumann F, Bertrand D (1976) Role of intracellular calcium and sodium in light adaptation in the retina of the honey bee drone (Apis mellifera L.) J Gen Physiol 67:475–491

    Google Scholar 

  • Baumann F (1968) Slow and spike potentials recorded from retinular cells of the honeybee drone in response to light. J Gen Physiol 52:855–875

    Google Scholar 

  • Baumann O, Takeyasu K (1993) Polarized distribution of Na,K-ATPase in honeybee photoreceptors is maintained by interaction with glial cells. J Cell Sci 105:287–301

    Google Scholar 

  • Baumann O, Walz B (1989a) Topography of Ca2+-sequestering endoplasmic reticulum in photoreceptors and pigmented glial cells in the compound eye of the honeybee drone. Cell Tissue Res 255:511–522

    Google Scholar 

  • Baumann O, Walz B (1989b) Calcium and inositol polyphosphatesensitivity of the calcium-sequestering endoplasmic reticulum in the photoreceptor cells of the honeybee drone. J Comp Physiol A 165:627–636

    Google Scholar 

  • Baumann O, Walz B, Somlyo AV, Somlyo AP (1991) Electron probe microanalysis of calcium release and magnesium uptake by endoplasmic reticulum in bee photoreceptors. Proc Natl Acad Sci USA 88:741–744

    Google Scholar 

  • Bertrand D, Fuortes G, Muri R (1979) Pigment transformation and electrical responses in retinula cells of drone, Apis mellifera. J Physiol (Lond) 296:431–441

    Google Scholar 

  • Bezprozvanni I, Watras J, Ehrlich BE (1991) Bell-shaped calciumresponse curves of Ins(1,4,5)P3 and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351:751–754

    Google Scholar 

  • Bolsover SR, Brown JE (1985) Calcium ion, an intracellular messenger of light adaptation, also participates in excitation of Limulus photoreceptors. J Physiol (Lond) 364:384–393

    Google Scholar 

  • Brown JE (1986) Calcium and light adaptation in invertebrate photoreceptors. In: Stieve H (ed) The molecular mechanism of photoreception. Springer, Berlin Heidelberg New York, pp 231–240

    Google Scholar 

  • Brown JE, Blinks JR (1974) Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors. Detection with aequorin. J Gen Physiol 64:643–665

    Google Scholar 

  • Brown JE, Brown PK, Pinto LH (1977) Detection of light-induced changes of intracellular ionized calcium concentration in Limulus ventral photoreceptors using arsenazo III. J Physiol (Lond) 267:299–320

    Google Scholar 

  • Brown JE, Rubin LJ, Ghalayini AJ, Tarver AL, Irvine RF, Berridge MJ, Anderson RE (1984) myo-Inositol polyphosphate may be a messenger for visual excitation in Limulus photoreceptors. Nature 311:160–162

    Google Scholar 

  • Calman B, Chamberlain S (1982) Distinct lobes of Limulus ventral photoreceptors. II. Structure and ultrastructure. J Gen Physiol 80:839–862

    Google Scholar 

  • Coles JA, Orkand RK (1983) Modification of potassium movement through the retina of the drone (Apis mellifera) by glial uptake. J Physiol (Lond) 340:157–174

    Google Scholar 

  • Coles JA, Vallet AM (1991) Signal-to-noise ratio at high light intensities in drone photoreceptors. Neurosci Res Suppl 15:81–11

    Google Scholar 

  • Coles JA, Orkand RK, Yamate CL, Tsacopoulos M (1986) Free concentrations of Na, K, and Cl in the retina of the honey bee drone: stimulus-induced redistribution and homeostasis. Ann NY Acad Sci 481:303–317

    Google Scholar 

  • Eberhard M, Erne P (1989) Kinetics of calcium binding to fluo-3 determined by stopped-flow fluorescence. Biochem Biophys Res Commun 163:309–314

    Google Scholar 

  • Fabiato A (1988) Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Meth Enzymol 157:378–417

    Google Scholar 

  • Faddis MN, Brown JE (1992) Flash photolysis of caged compounds in Limulus ventral photoreceptors. J Gen Physiol 100:547–570

    Google Scholar 

  • Fein A, Payne R, Corson DW, Berridge MJ, Irvine RF (1984) Photoreceptor excitation and adaptation by inositol 1,4,5 trisphosphate. Nature 311:157–160

    Google Scholar 

  • Finch EA, Turner TJ, Goldin SM (1991) Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science 252:443–446

    Google Scholar 

  • Grynkiewicz G, Poeni M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440–3450

    Google Scholar 

  • Hardie RC (1991) Whole-cell recordings of the light induced current in dissociated Drosophila photoreceptors: evidence for feedback by calcium permeating the light-sensitive channels. Proc R Soc Lond B 245:203–210

    Google Scholar 

  • Hardie RC, Minke B (1992) The trp gene is essential for a light activated Ca2+ channel in Drosophila photoreceptors. Neuron 8:643–651

    Google Scholar 

  • Kao JPY, Tsien RY (1988) Ca2+ binding kinetics of fura-2 and azo-1 from temperature-jump relaxation measurements. Biophys J 53:635–640

    Google Scholar 

  • Konishi M, Hollingworth S, Baylor SM (1988) Myoplasmic binding of fura-2 investigated by steady-state fluorescence and absorbance measurements. Biophys J 54:1089–1104

    Google Scholar 

  • Levy S, Fein A (1985) Relationship between light sensitivity and intracellular free calcium in Limulus ventral photoreceptors. J Gen Physiol 85:805–841

    Google Scholar 

  • Levy S, Payne R (1993) A lingering elevation of Cai accompanies inhibition of inositol 1,4,5-trisphosphate-induced Ca release in Limulus ventral photoreceptors. J Gen Physiol 101:67–84

    Google Scholar 

  • Lisman JE, Brown JE (1975) Effects of intracellular injection of calcium buffers in Limulus ventral photoreceptors. J Gen Physiol 66:489–506

    Google Scholar 

  • Maaz G, Stieve H (1980) The correlation of the receptor potentials with the light-induced transient increase in intracellular Ca concentration measured by absorption change of A III injected into Limulus ventral nerve photoreceptor cells. Biophys Struct Mech 9:207–223

    Google Scholar 

  • Minke B, Selinger Z (1992) Inositol lipid pathway in fly photoreceptors: excitation, calcium mobilization and retinal degeneration. In: Osborne NN, Chader GJ (eds) Progress in retinal research, vol 11. Pergamon Press, Oxford, pp 99–124

    Google Scholar 

  • Minke B, Tsacopoulos M (1986) Light induced sodium dependent accumulation of calcium and potassium in the extracellular space of bee retina. Vision Res 26:679–690

    Google Scholar 

  • Mojet MH, Hardie RC (1993) Multiple light-induced conductances in invertebrate phototransduction. In: Elsner N, Heisenberg M (eds) Gene — Brain — Behaviour. Thieme, Stuttgart New York, p 343

    Google Scholar 

  • Payne R (1986) Phototransduction by microvillar photoreceptors of invertebrates: mediation of a visual cascade by inositol trisphosphate. Photobiochem Photobiophys 13:373–397

    Google Scholar 

  • Payne R (1990) Dynamics of the release of calcium by light and inositol 1,4,5-trisphosphate in Limulus ventral photoreceptors. In: Hidalgo C, Bacigalupo J, Jaimovich E, Vergara J (eds) Transduction in biological systems. Plenum Press, New York London, pp 9–25

    Google Scholar 

  • Payne R, Fein A (1987) Inositol 1,4,5-trisphosphate releases calcium from specialized sites within Limulus photoreceptors. J Cell Biol 104:933–937

    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 by negative feedback. Phil Trans R Soc Lond B 320:359–379

    Google Scholar 

  • Poeni M (1990) Alteration of intracellular fura-2 fluorescence by viscosity: a simple correction. Cell Calcium 11:85–91

    Google Scholar 

  • Ranganathan R, Harris GL, Steven CF, Zuker CS (1991) A Drosophila mutant defective in extracellular calcium-dependent photoreceptor deactivation and desensitization. Nature 354:230–232

    Google Scholar 

  • Roe MW, Lemasters JJ, Herman B (1990) Assessment of fura-2 for measurements of cytosolic free calcium. Cell Calcium 11:63–73

    Google Scholar 

  • Sandler C, Kirschfeld K (1988) Light intensity controls extracellular Ca2+ concentration in the blowfly retina. Naturwissenschaften 75:256–258

    Google Scholar 

  • Shaw SR (1969) Interreceptor coupling in ommatidia of drone honeybee and locust compound eyes. Vision Res 9:999–1029

    Google Scholar 

  • Stieve H, Benner S (1992) The light-induced rise in cytosolic calcium starts later than the receptor current of the Limulus ventral photoreceptor. Vision Res 32:403–416

    Google Scholar 

  • Vergara J, Escobar A (1993) Detection of Ca2+ transients in skeletal muscle fibers using the low-affinity dye Calcium-Green-5N. Biophys J 64:A37

    Google Scholar 

  • Walz B (1982) Ca2+-sequestering smooth endoplasmic reticulum in an invertebrate photoreceptor. II. Its properties as revealed by microphotometric measurements. J Cell Biol 93:849–859

    Google Scholar 

  • Walz B (1992) Enhancement of sensitivity in photoreceptors of the honeybee drone by light and by Ca2+. J Comp Physiol A 170:605–613

    Google Scholar 

  • Williams DA, Fay FS (1990) Intracellular calibration of the fluorescent calcium indicator fura-2. Cell Calcium 11:75–83

    Google Scholar 

  • Williamson ED, Adams LH (1919) Temperature distribution in solids during heating or cooling. Physical Rev 14:99–114

    Google Scholar 

  • Zhao H, Muallem S (1990) Inhibition of InsP3-mediated Ca release by Ca in cells from peripheral tissues. J Biol Chem 265:21419–21422

    Google Scholar 

  • Ziegler A, Walz B (1989) Analysis of extracellular calcium and volume changes in the compound eye of the honeybee drone, Apis mellifera. J Comp Physiol A 165:697–709

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Zoologie, Universität Regensburg, Universitätsstrasse 31, D-93040, Regensburg, Germany

    B. Walz, B. Zimmermann & S. Seidl

Authors
  1. B. Walz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Zimmermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Seidl
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Walz, B., Zimmermann, B. & Seidl, S. Intracellular Ca2+ concentration and latency of light-induced Ca2+ changes in photoreceptors of the honeybee drone. J Comp Physiol A 174, 421–431 (1994). https://doi.org/10.1007/BF00191708

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00191708

Key words

Search

Navigation