Hostname: page-component-848d4c4894-8kt4b Total loading time: 0 Render date: 2024-06-17T18:17:50.387Z Has data issue: false hasContentIssue false
  • English
  • Français

Localization of phototransduction in Limulus ventral photoreceptors: A demonstration using cell-free rhabdomeric vesicles

Published online by Cambridge University Press:  02 June 2009

Juan Bacigalupo  and
Edwin C. Johnson
Juan Bacigalupo
Affiliation:
Department of Physiology, Marshall University School of Medicine, Huntington
Edwin C. Johnson
Affiliation:
Department of Physiology, Marshall University School of Medicine, Huntington
Get access Rights & Permissions [Opens in a new window]

Abstract

Second messengers are involved in a number of cellular responses to a variety of stimuli. Diffusion of these second messengers likely will determine the speed and efficiency of such responses. Localization, particularly in large cells, would enhance the efficiency of such transduction systems by restricting the volume in which this diffusion takes place and thereby limiting the diffusion of soluble messengers. Phototransduction in Limulus ventral photoreceptors involves second-messenger systems; the volume of this cell is quite large, but the effect of a single photoexcited rhodopsin molecule is exerted over light-dependent channels localized within a very small area of the plasma membrane. In order to investigate localization of phototransduction in these photoreceptors, we have compared the light responses of small vesicles (photoballs) excised from these cells with those of the intact photoreceptors. We found that the basic kinetics of excitation and adaptation of the photoballs are essentially identical to those of the intact cell. This indicates that all of the necessary machinery for phototransduction is present and intact in the photoball and that any diffusion of second messengers that affect the normal light response of the cell must occur within a region at least as small as our photoballs (on the order of 1 μm3).

Keywords

LocalizationPhotoballPhototransductionReceptor potentialSecond messengersPhotoreceptor
Type
Research Articles
Information
Visual Neuroscience , Volume 8 , Issue 1 , January 1992 , pp. 41 - 47
Copyright
Copyright © Cambridge University Press 1992

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

Bacigalupo, J., Johnson, E.C., Robinson, P.R. & Lisman, J.E. (1990). Second messengers in invertebrate phototransduction. In Transduction in Biological Systems, ed. Hidalgo, C., Bacigalupo, J., Jaimovich, E. & Vergara, J., pp. 27–45. New York: Plenum Press.CrossRefGoogle Scholar
Bacigalupo, J., Johnson, E.C., Vergara, C. & Lisman, J.E. (1991). Light-dependent channels from excised patches of Limulus ventral photoreceptors are opened by cGMP. Proceedings of the National Academy of Sciences of the U.S.A. 88, 7938–7942.CrossRefGoogle ScholarPubMed
Bacigalupo, J. & Johnson, E.C. (1989). Localización del mecanismo de fototransducción en fotorreceptores de Limulus. Archivos de Biologiay Medicina Experimental 22, R230.Google Scholar
Bacigalupo, J. & Lisman, J.E. (1983). Single-channel currents activated by light in Limulus ventral photoreceptors. Nature 304, 268–270.CrossRefGoogle ScholarPubMed
Baumann, O. & Walz, B. (1989). Calcium and inositol polyphosphate-sensitivity of the calcium sequestering endoplasmic reticulum in the photoreceptor cells of the honey bee drone. Journal of Comparative Physiololy A 165, 627–636.CrossRefGoogle Scholar
Bloomquist, B.T., Shortridge, R.D., Schneuwly, W., Perdew, M., Montell, C., Steller, H., Rubin, G. & Pak, W.L. (1988). Isolation of a putative phospholipase-C gene of Drosophila, norpA, and its role in phototransduction. Cell 54, 723–733.CrossRefGoogle ScholarPubMed
Bolsover, S.R. & Brown, J.E. (1985). Calcium ion, an intracellular messenger of light adaptation, also participates in excitation of Limulus photoreceptors. Journal of Physiology 364, 381–393.CrossRefGoogle ScholarPubMed
Brown, J.E. & Coles, J.A. (1979). Saturation of the response to light in Limulus ventral photoreceptors. Journal of Physiology (London) 296, 373–392.Google Scholar
Brown, J.E. & Lisman, J.E. (1975). Intracellular Ca modulates sensitivity and time scale in Limulus ventral photoreceptors. Nature 228, 252–253.CrossRefGoogle Scholar
Brown, J.E., Watkins, D.C. & Malbon, C.C. (1987). Light-induced changes in the content of inositol phosphates in squid Loligo pealei retinas. Biochemical Journal 247, 293–297.CrossRefGoogle Scholar
Calman, B.G. & Chamberlain, S.C. (1982). Distinct lobes of Limulus photoreceptors. II. Structure and ultrastructure. Journal of General Physiology 80, 839–862.CrossRefGoogle ScholarPubMed
Devary, O., Heichal, O., Blumenfeld, A., Cassel, D., Suss, E., Barash, S., Rubinstein, C.T., Minke, B. & Selinger, Z. (1987). Coupling of photoexcited rhodopsin to inositol phospholipid hydrolysis in fly photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 84, 6939–6943.CrossRefGoogle ScholarPubMed
Ertel, E.A. (1990). Excised patches of plasma membrane from vertebrate rod outer segments retain a functional phototransduction enzymatic cascade. Proceedings of the National Academy of Sciences of the U.S.A. 87, 4226–4230.CrossRefGoogle ScholarPubMed
Fein, A. & Lisman, J.E. (1975). Localized desensitization of Limulus photoreceptors by light or intracellular calcium ion injections. Science 187, 1094–1096.CrossRefGoogle ScholarPubMed
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sioworth, F.J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Archives 391, 85–100.CrossRefGoogle ScholarPubMed
Johnson, E.C. & Pak, W.L. (1986). Electrophysiological study of Drosophila rhodopsin mutants. Journal of General Physiology 88, 651–673.CrossRefGoogle ScholarPubMed
Johnson, E.C., Robinson, P.R. & Lisman, J.E. (1986). Cyclic GMP is involved in the excitation of invertebrate photoreceptors. Nature 324, 468–470.CrossRefGoogle ScholarPubMed
Lamb, T.D., McNaughton, P.A. & Yau, K.-W. (1981). Spatial spread of activation and background desensitization in toad rod outer segments. Journal of Physiology (London) 319, 463–496.Google Scholar
Millecchia, R. & Mauro, A. (1969). The ventral photoreceptor cells of Limulus. III. A voltage-clamp study. Journal of General Physiology 54, 331–351.CrossRefGoogle Scholar
Payne, R., Corson, D.W., Fein, A. & Berridge, M.J. (1986). Excitation and adaptation of Limulus ventral photoreceptors by inositol 1,4,5-trisphosphate result from a rise in intracellular calcium. Journal of General Physiology 88, 127–142.CrossRefGoogle ScholarPubMed
Payne, R. & Fein, A. (1983). Localized adaptation within the rhabdomeral lobe of ventral photoreceptors. Journal of General Physiology 81, 767–796.CrossRefGoogle ScholarPubMed
Payne, R. & Fein, A. (1984). Localization of the photocurrent of Limulus ventral photoreceptors using a vibrating probe. Biophysical Journal 50, 193–196.CrossRefGoogle Scholar
Payne, P. & Fein, A. (1986). The initial response of Limulus ventral photoreceptors to bright flashes: released calcium as a synergist to excitation. Journal of General Physiology 87, 243–269.CrossRefGoogle ScholarPubMed
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. Philosophical Transactions of the Royal Society B (London) 320, 359–379.Google Scholar
Robinson, P.R., Wood, S.F., Szuts, E.Z., Fein, A., Hamm, H.E. & Lisman, J.E. (1990). Light-dependent GTP-binding proteins in squid photoreceptors. Biochemical Journal 272, 79–85.CrossRefGoogle ScholarPubMed
Rubin, L.J., Womble, M., Brown, J.E. & Finger, T.E. (1989). Accessibility of colloidal gold and horseradish peroxidase to cytosolic spaces in Limulus ventral photoreceptors. Visual Neuroscience 2, 89–96.CrossRefGoogle ScholarPubMed
Schneider, B.G., Shyjan, A.W. & Levenson, R. (1991). Co-localization and polarized distribution of Na+, K+-ATPase α3 and β2-subunits in photoreceptor cells. Journal of Histochemistry and Cytochemistry 39, 507–517.CrossRefGoogle Scholar
Stern, J., Chinn, K., Bacigalupo, J. & Lisman, J.E. (1982). Distinct lobes of Limulus ventral photoreceptors. I. Functional and anatomical properties of lobes revealed by removal of glial cells. Journal of General Physiology 80, 825–837.CrossRefGoogle ScholarPubMed
Szuts, E.Z., Wood, S.F., Reid, M.S. & Fein, A. (1986). Light stimulates the rapid formation of inositol trisphosphate in squid retinas. Biochemical Journal 240, 929–932.CrossRefGoogle ScholarPubMed
Ziegler, A. & Walz, B. (1990). Evidence for light-induced release of Ca2+ from intracellular stores in bee photoreceptors. Neuroscience Letters 111, 87–91.CrossRefGoogle ScholarPubMed
Zimmermann, A.L., Karpen, J.W. & Baylor, D.A. (1988). Hindered diffusion in excised membrane patches from retinal rod outer segments. Biophysical Journal 54, 351–355.CrossRefGoogle Scholar