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Gap junction channel gating at bass retinal electrical synapses

Published online by Cambridge University Press:  02 June 2009

Chengbiao Lu  and
Douglas G. McMahon
Chengbiao Lu
Affiliation:
Department of Physiology, University of Kentucky, Lexington
Douglas G. McMahon
Affiliation:
Department of Physiology, University of Kentucky, Lexington
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Abstract

To further characterize the properties of retinal horizontal cell electrical synapses, we have studied the gating characteristics of gap junctions between cone-driven horizontal cells from the hybrid striped bass retina using double whole-cell voltage-clamp techniques. In a total of 105 cell pairs, the macroscopic conductance ranged from 0.4–100 nS with most cell pairs exhibiting junctional conductances between 10 and 30 nS. The junctional current-voltage relationship showed that peak or instantaneous currents (Iinst) were linear within the Vj range of ±100 mV and that steady-state junctional currents (Iss) exhibited rectification with increasing voltage beginning around ±30–40 mV Vj. The normalized junctional current-voltage relationship was well fit by a two-state Boltzmann distribution, with an effective gating charge of 1.9 charges/channel, a half-maximal voltage of approximately ±55 mV, and a normalized residual conductance of 0.28. The decay of junctional current followed a single exponential time course with the time constant decreasing with increasing Vj. Recovery of junctional current from voltage-dependent inactivation takes about 1 s following a pulse of 80 mV, and is about five times slower than the inactivation time course at the same Vj. Single-channel analysis showed that the unitary conductance of junctional channels is 50–70 pS. The overall open probability decreased in a voltage-dependent manner. Both the mean channel open time and the frequency of channel opening decreased, while the channel closure time increased. The ratio of closed time/total recording time significantly increased as Vj increased. Increased Vj reduced the number of events at all levels and shifted the unitary conductance to a lower level. Kinetic analysis of channel open duration showed that the distribution of channel open times was best fit by two exponentials and increased Vj significantly reduced the slower time constant. These results indicate that bass retina horizontal cells exhibit voltage-dependent inactivation of macroscopic junctional current. The inactivation occurs at the single-channel level mainly by increasing the rate of closure of voltage-sensitive channels.

Keywords

Gap junctionHorizontal cellsVoltage dependenceConnexinSingle channel
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 6 , November 1996 , pp. 1049 - 1057
Copyright
Copyright © Cambridge University Press 1996

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References

Barrio, L.C., Suchyna, T., Bargiello, T., Xu, L.X., Roginski, R.S., Bennett, M.V.L. & Nicholson, B.J. (1991). Gap junctions formed by connexins 26 and 32 alone and in combination are differently affected by applied voltage. Proceedings of the National Academy of Sciences of the U.S.A. 88, 8410–8414.CrossRefGoogle ScholarPubMed
Bruzzone, R., White, T.W., Yoshizaki, G., Patino, R. & Paul, D.L. (1995). Intercellular channels in teleosts: Functional characterization of two connexins from Atlantic croaker. FEBS Letters 358, 301–304.Google Scholar
Bukauskas, E.F., Kempf, C. & Weingart, R. (1992 a). Electrical coupling between cells of the insect Aedes albopictus. Journal of Physiology 448, 312–337.CrossRefGoogle ScholarPubMed
Bukauskas, E.F., Kempf, C. & Weingart, R. (1992 b). Cytoplasmic bridge and gap junctions in an insect cell line (Aedes albopictus). Experimental Physiology 77, 903–911.CrossRefGoogle Scholar
Chanson, M., Chandross, K.J., Rook, M.B., Kessler, J.A. & Spray, D.C. (1993). Gating characteristics of a steeply voltage-dependent gap junction channel in rat Schwann cells. Journal of General Physiology 102, 925–946.CrossRefGoogle ScholarPubMed
Darrow, B.J., Laing, J.G., Lampe, P.D., Saffitz, J.E., Beyer, B.C. (1995). Expression of multiple connexins in cultured neonatal rat ventricular myocytes. Circulation Research 76, 381–387.CrossRefGoogle ScholarPubMed
DeVries, S.H. & Schwartz, E.A. (1992). Hemi-gap-junction channels in solitary horizontal cells of the catfish retina. Journal of Physiology 445, 201–230.CrossRefGoogle ScholarPubMed
Dowling, J.E., Pak, M.W. & Lasater, E.M. (1982). White perch horizontal cells in culture: Methods, morphology and process growth. Brain Research 360, 331–338.CrossRefGoogle Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: The Belknap Press of Harvard University Press.Google Scholar
Edgerton, T.L. & McMahon, D.O. (1995). Partial sequence of a gap junction channel gene from the giant danio retina. Investigative Ophthalmology and Visual Science (Suppl.) 36, S929.Google Scholar
Gho, M. (1994). Voltage-clamp analysis of gap junctions between embryonic muscles in Drosophila. Journal of Physiology 481, 371–383.CrossRefGoogle ScholarPubMed
Giaume, C., Kado, R.T. & Korn, H. (1987). Voltage-clamp analysis of a crayfish rectifying synapse. Journal of Physiology 386, 91–112.CrossRefGoogle ScholarPubMed
Harris, A.L., Spray, D.C. & Bennett, M.V. (1981). Kinetic properties of a voltage-dependent junctional conductance. Journal of General Physiology 77, 95–117.CrossRefGoogle ScholarPubMed
Lal, R. & Arnsdorf, M.F. (1992). Voltage-dependent gating and single-channel conductance of adult mammalian atrial gap junctions. Circulation Research 71, 737–743.CrossRefGoogle 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, 3025–3029.CrossRefGoogle ScholarPubMed
McMahon, D.G. & Brown, D.R. (1994). Modulation of gap junction channel gatting at zebrafish retinal electrical synapses. Journal of Neurophysiology 72, 2257–2268.Google Scholar
McMahon, D.G. (1994). Modulation of electrical synaptic transmission in zebrafish retinal horizontal cells. Journal of Neuroscience 14, 1722–1743.CrossRefGoogle ScholarPubMed
Moreno, A.P., Fishman, G.I. & Spray, D.C. (1992). Phosphorylation shifts unitary conductance and modifies voltage-dependent kinetics of human connex43 gap junction channels. Biophysical Journal 62, 51–53.CrossRefGoogle ScholarPubMed
Moreno, A.P., Rook, M.B., Fishman, G.I. & Spray, D.C. (1994). Gap junction channels: Distinct voltage-sensitive and -insensitive conductance states. Biophysical Journal 67, 113–119.CrossRefGoogle ScholarPubMed
Moreno, A.P., Laing, J.G., Beyer, E.C. & Spray, D.C. (1995). Properties of gap junction channels formed of connexin 45 endogenously expressed in human hepatoma (SKHepl) cells. American Journal of Physiology 268, C356–C365.CrossRefGoogle Scholar
Neyton, J. & Trautmann, A. (1985). Single-channel currents of an intercellular junction. Nature 317, 331–335.CrossRefGoogle ScholarPubMed
Ringham, G.L. (1975). Localization and electrical characteristics of a giant synapse in the spinal cord of the lamprey. Journal of Physiology 251, 395–407.CrossRefGoogle ScholarPubMed
Rook, M.B., Jongsma, H.J. & Ginneken, A.C.G.V. (1988). Properties of single gap junctional channels between isolated neonatal rat heart cells. American Journal of Physiology 255, H770–H782.Google Scholar
Rup, D.M., Veenstra, R.D., Wang, H., Brink, P.R. & Beyer, B.C. (1993). Chick connexin-56, a novel lens gap junction protein. Journal of Biological Chemistry 268, 706–712.Google Scholar
Spray, D.C., Harris, A.L. & Bennett, M.V.L. (1981). Equilibrium properties of a voltage-dependent junctional conductance. Journal of General Physiology 77, 77–93.Google Scholar
Spray, D.C., Cherbas, L., Cherbas, P., Morales, E.A. & Carrow, G.M. (1989). Ionic coupling and mitoyic synchrony of siblings in a Drosophila cell line. Experimental Cell Research 184, 509–517.CrossRefGoogle Scholar
Sterling, P. (1989). Retina (Chapter 6). In The Synaptic Organization of the Brain, 3rd edition, ed. Shepherd, G.M., pp. 170–213. New York: Oxford University Press, Inc.Google Scholar
Verselis, V.K., Ginter, C.S. & Bargiello, T.A. (1994). Opposite voltage gating polarities of two closely related connexins. Nature 368, 348–351.CrossRefGoogle ScholarPubMed
Veenstra, R.D. (1990). Voltage-dependent gating of gap junction channels in embryonic chick ventricular cell pairs. American Journal of Physiology 258, C662–C672.Google Scholar
Veenstra, R.D., Wang, H.Z., Westphale, E.M. & Beyer, B.C. (1992). Multiple connexins confer distinct regulatory and conductance properties of gap junctions in developing heart. Circulation Research 71, 1277–1283.CrossRefGoogle ScholarPubMed
Wang, H., Li, J., Lemanski, L.F. & Veenstra, R.D. (1992). Gating of mammalian cardiac gap junction channels by transjunctional voltage. Biophysical Journal 63, 139–152.CrossRefGoogle ScholarPubMed
White, R.L., Spray, D.C., De Carvalho, A.C.C., Wittenberg, B.A. & Bennett, M.V.L. (1985). Some electrical and pharmacological properties of gap junctions between adult ventricular myocytes. American Journal of Physiology 249, C447–455.Google Scholar