Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-23T05:35:53.942Z Has data issue: false hasContentIssue false

Gap-junctional properties of electrically coupled skate horizontal cells in culture

Published online by Cambridge University Press:  02 June 2009

Haohua Qian
Affiliation:
Department of Ophthalmology and Visual Sciences, Lions of Illinois Eye Research Institute, University of Illinois College of Medicine, Chicago Department of Anatomy and Cell Biology, University of Illinois College of Medicine, Chicago
Robert Paul Malchow
Affiliation:
Department of Ophthalmology and Visual Sciences, Lions of Illinois Eye Research Institute, University of Illinois College of Medicine, Chicago
Harris Ripps
Affiliation:
Department of Ophthalmology and Visual Sciences, Lions of Illinois Eye Research Institute, University of Illinois College of Medicine, Chicago Department of Anatomy and Cell Biology, University of Illinois College of Medicine, Chicago

Abstract

Whole-cell voltage-clamp recordings were used to examine the unusual pharmacological properties of the electrical coupling between rod-driven horizontal cells in skate retina as revealed previously by receptive-field measurements (Qian & Ripps, 1992). The junctional resistance was measured in electrically coupled cell pairs that had been enzymatically isolated and maintained in culture; the typical value was about 19.92 MΩ(n = 45), more than an order of magnitude lower than the nonjunctional membrane resistance. These data and the intercellular spread of the fluorescent dye Lucifer Yellow provide a good indication that skate horizontal cells are well coupled. The junctional conductance between cells was not modulated by the neurotransmitters dopamine (200 μM) or GABA (1 mM), nor was it affected by the membrane-permeable analogues of cAMP or cGMP, or the adenylate cyclase activator, forskolin. Although resistant to agents that have been reported to alter horizontal-cell coupling in cone-driven horizontal cells, the junctional conductance between paired horizontal cells of skate was greatly reduced by the application of 20 mM acetate, which is known to effectively reduce intracellular pH. Together with the results obtained in situ on the receptive-field properties of skate horizontal cells, these findings indicate that the gap-junctional properties of rod-driven horizontal cells of the skate are fundamentally different from those of cone-driven horizontal cells in other species. This raises the possibility that there is more than one class of electrical synapse on vertebrate horizontal cells.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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

Akopain, A., McReynolds, J., Ammermuller, J. & Weiler, R. (1991). Activation of PKC modulates light responses in turtle horizontal cells. Investigative Ophthalmology and Visual Science (Suppl.) 32, 991.Google Scholar
Bennett, M.V.L., Barrio, L.C., Bargiello, T.A., Spray, D.C., Hertzberg, E. & SAEZ, J.C. (1991). Gap junctions: New tools, new answers, new questions. Neuron 6, 305320CrossRefGoogle ScholarPubMed
Beyer, E.C., Paul, D.L. & Goodenough, D.A. (1990). Connexin family of gap junction proteins. Journal of Membrane Biology 116, 187194CrossRefGoogle ScholarPubMed
Chanson, M., Bruzzone, R.D., Spray, D.C., Regazzi, R. & Meda, P. (1988). Cell uncoupling and protein kinase C: Correlation in a cell line but not in a differentiated tissue. American Journal of Physiology 255, C699C704CrossRefGoogle Scholar
Devries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopa-mine and second messengers. Journal of Physiology 414, 351375CrossRefGoogle Scholar
Devries, S.H. & Schwartz, E.A. (1992). Hemi-gap-junction channels in solitary horizontal cells of the catfish retina. Journal of Physiology 445, 201230CrossRefGoogle ScholarPubMed
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981). Improved patch-clamping techniques for high-resolution current recording form cells and cell-free membrane patches. Pflugers Archives 391, 85100CrossRefGoogle Scholar
Harris, A.L., Spray, D.C. & Bennett, M.V.L. (1981). Kinetic properties of a voltage-dependent junctional conductance. Journal of General Physiology 77, 95117CrossRefGoogle ScholarPubMed
Hestrin, S. & Korenbrot, J.I. (1987). Voltage-activated potassium channels in the plasma membrane of rod outer segments: A possible effect of enzymatic dissociation. Journal of Neuroscience 7, 30723080CrossRefGoogle Scholar
Hidaka, S., Shingai, R., Dowling, J.E. & Naka, K. (1989). Junctions form between catfish horizontal cells in culture. Brain Research 498, 5363CrossRefGoogle ScholarPubMed
Ishida, A.T. & Fain, G.L. (1981). D-aspartate potentiates the effects of L-glutamate on horizontal cells in goldfish retina. Proceedings of the National Academy of Sciences of the U.S.A. 78, 58905894CrossRefGoogle ScholarPubMed
Kaneko, A. (1971), Electrical connexions between horizontal cells in the dogfish retina. Journal of Physiology 213, 95105CrossRefGoogle ScholarPubMed
Kaneko, A. & Stuart, A.E. (1984). Coupling between horizontal cells in the carp retina revealed by diffusion of Lucifer yellow. Neuroscience Letters 47, 17CrossRefGoogle ScholarPubMed
Lamb, T.D. (1976). Spatial properties of horizontal cell responses in the turtle retina. Journal of Physiology 263, 239255CrossRefGoogle ScholarPubMed
Lasater, E.M. (1987). Retinal horizontal cell gap junctional conductance is modulated by dopamine through a cyclic AMP-dependent protein kinase. Proceedings of the National Academy of Sciences of the U.S.A. 84, 73197323CrossRefGoogle ScholarPubMed
Lasater, E.M. & Dowling, J.E. (1982). Carp horizontal cells in culture respond selectively to L-glutamate and its agonists. Proceedings of the National Academy of Sciences of the U.S.A. 79, 936940CrossRefGoogle ScholarPubMed
Lasater, E.M. & Dowling, J.E. (1985). Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 82, 30253029CrossRefGoogle ScholarPubMed
Lasater, E.M., Dowling, J.E. & Ripps, H. (1984). Pharmacological properties of isolated horizontal and bipolar cells from the skate retina. Journal of Neuroscience 4, 19661975CrossRefGoogle ScholarPubMed
MacDonald, J.F. & Worrowicz, J.M. (1980). Two conductance mechanisms activated by applications of L-glutamic, L-aspartic, DL-homocysteic, N-methyl-D-aspartic, and DL-kainic acids to cultured mammalian central neurons. Canadian Journal of Physiology and Pharmacology 58, 13931397CrossRefGoogle Scholar
Majerus, P.W., Connolly, T.M., Deckmyn, H., Ross, T.S., Bross, T.E., Ishii, H., Bansal, V.S. & Wilson, D.B. (1986). The metabolism of phosphoinositide-derived messenger molecules. Science 234, 15191526CrossRefGoogle Scholar
Malchow, R.P., Qian, H. & Ripps, H. (1992). The slowly developing outward current of skate horizontal cells: A reflection of the opening of hemi-gap junctional channels? Investigative Ophthalmology and Visual Science (Suppl.) 33, 906.Google Scholar
Malchow, R.P., Qian, H., Ripps, H. & Dowling, J.E. (1990). Structural and functional properties of two types of horizontal cell in the skate retina. Journal of General Physiology 95, 177198CrossRefGoogle ScholarPubMed
Malchow, R.P. & Ripps, H. (1990). Effects of 7-aminobutyric acid on skate retinal horizontal cells: Evidence for an electrogenic uptake mechanism. Proceedings of the National Academy of Sciences of the U.S.A. 87, 89458949CrossRefGoogle Scholar
Manjunath, C.K., Nicholson, B.J., Teplow, D., Hood, L., Page, E. & Revel, J.-P. (1987). The cardiac gap junction protein (Mr 47,000) has a tissue-specific cytoplasmic domain of Mr 17,000 at its carboxy-terminals. Biochemical and Biophysical Research Communications 142, 228234CrossRefGoogle Scholar
McMahon, D.G., Knapp, A.G. & Dowling, J.E. (1989). Horizontal cell gap junctions: Single channel conductance and modulation by dopamine. Proceedings of the National Academy of Sciences of the U.S.A. 86, 76397643CrossRefGoogle ScholarPubMed
Murray, A.W. & Gainer, H.S.T.C. (1989). Regulation of gap junctional communication by protein kinases. In Cell Interactions and Gap Junctions, Vol. 1, ed. Sperelakis, N. & Cole, W.C., pp. 97106. Florida: CRC Press, Inc.Google Scholar
Naka, K.I. & Rushton, W.A.H. (1967). The generation and spread of s-potentials in fish (cyprinidae). Journal of Physiology 192, 437461CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T. & Kato, S. (1985). Dopaminergic interplex-iform cells and their regulatory function for spatial properties of horizontal cells in the fish retina. In Neurocircuitry of the retina: A Cajal Memorial, ed. Gallego, A. & Gouras, P., pp. 7788. New York: Elsevier.Google Scholar
Neyton, J. & Trautmann, A. (1985). Single-channel currents of an intercellular junction. Nature 317, 331335CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1986). Studies and perspectives of protein kinase C. Science 233, 305312CrossRefGoogle ScholarPubMed
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1984). Decrease of gap junctional permeability induced by dopamine and cyclic aden-osine 3’:5’-monophosphate in horizontal cells of turtle retina. Journal of Neuroscience 4, 24772488CrossRefGoogle Scholar
Piccolino, M., Witkovsky, P. & Trimarchi, C. (1987). Dopaminergic mechanisms underlying the reduction of electrical coupling between horizontal cells of the turtle retina induced by d-amphetamine, bicuculline, and veratridine. Journal of Neuroscience 7, 22732284Google ScholarPubMed
Qian, H. & Ripps, H. (1992). The receptive-field properties of rod-driven horizontal cells in the skate retina. Journal of General Physiology 100, 457478CrossRefGoogle ScholarPubMed
Revel, J.-P., Nicholson, B.J. & Yancey, S.B. (1985). Chemistry of gap junctions. Annual Review of Physiology 47, 263279CrossRefGoogle ScholarPubMed
Ripps, H. & Witkovsky, P. (1985). Neuron-glia interaction in the brain and retina. In Progress in Retinal Research, ed. Osborne, N. & Chader, G., pp. 181220. New York: Pergamon Press.Google Scholar
Rodrigues, P.S. & Dowling, J.E. (1990). Dopamine induces neurite retraction in retinal horizontal cells via diacylglycerol and protein kinase C. Proceedings of the National Academy of Sciences of the U.S.A. 87, 96939697CrossRefGoogle ScholarPubMed
Rook, M.B., Jongsma, H.J. & Van Ginneken, A.C.G. (1988). Properties of single gap junctional channels between isolated neonatal rat heart cells. American Journal of Physiology 255, H770–H782.Google ScholarPubMed
Saez, J.C., Nairn, A.C., Czernik, A.J., Spray, D.C., Hertzberg, E.L., Greengard, P. & Bennett, M.V.L. (1990). Phosphorylation of connexin 32, the hepatocyte gap junction protein, by cAMP-dependent protein kinase, protein kinase C and Ca2+/calmodulin-dependent protein kinase II. European Journal of Biochemistry 192, 263273CrossRefGoogle ScholarPubMed
Spray, D.C. & Bennett, M.V.L. (1985). Physiology and pharmacology of gap junctions. Annual Review of Physiology 47, 281303CrossRefGoogle ScholarPubMed
Spray, D.C., Saez, J.C., Bunt, J.M., Watanabe, T., Reid, L.M., Hertzberg, E.L. & Bennett, M.V.L. (1988). Gap junction conductance: Multiple sites of regulation. In Gap Junctions, ed. Hertzberg, E.L. & Johnson, R.G., pp. 227244. New York: Alan R. Liss.Google Scholar
Takeda, A., Hashimoto, E., Yamamura, H. & Shimazu, T. (1987). Phosphorylation of liver gap junction protein by protein kinase C. FEBS Letters 210, 169172CrossRefGoogle ScholarPubMed
Tornqvist, K., Yang, X.-L. & Dowling, J.E. (1988). Modulation of cone horizontal cell activity in the teleost fish retina. III. Effects of prolonged darkness and dopamine on electrical coupling between horizontal cells. Journal of Neuroscience 8, 22792288CrossRefGoogle ScholarPubMed
Van Buskirk, R. & Dowling, J.E. (1981). Isolated horizontal cells from carp retina demonstrate dopamine-dependent accumulation of cyclic AMP. Proceedings of the National Academy of Sciences of the U.S.A. 78, 78257829CrossRefGoogle ScholarPubMed