Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-26T13:19:11.361Z Has data issue: false hasContentIssue false
  • English
  • Français

A glutamate-elicited chloride current with transporter-like properties in rod photoreceptors of the tiger salamander

Published online by Cambridge University Press:  02 June 2009

George B. Grant  and
Frank S. Werblin
George B. Grant
Affiliation:
The Biological Laboratories, Harvard University, Cambridge
Frank S. Werblin
Affiliation:
Department of Molecular and Cell Biology, University of California, Berkeley
Get access Rights & Permissions [Opens in a new window]

Abstract

Glutamate, when puffed near the synaptic terminals, elicits a current in rod photoreceptors. The current is strongly dependent upon both the intracellular and extracellular chloride concentration: its reversal potential follows the predicted Nernst potential for a chloride permeable channel. The glutamate-elicited current also requires the presence of extracellular sodium. This glutamate-elicited current is pharmacologically like a glutamate transporter: it is elicited, in order of efficacy, by L-glutamate, L-aspartate, L-cysteate, D-aspartate, and D-glutamate, all shown to activate glutamate transport in other systems. Furthermore, it is reduced by the glutamate transport antagonists dihydrokainate (DHKA) and D, L-threo-3–hydroxyaspartate (THA). THA, when applied alone, elicits a current similar to that elicited by glutamate. The current cannot be activated by the glutamate receptor agonists kainate, quisqualate, NMDA and APB, nor can it be blocked by the glutamale receptor antagonists CNQX and APV. Thus, the current does not appear to be mediated by a conventional glutamate receptor. Taken together, the ionic dependence and pharmacology of this current suggest that it is generated by glutamate transporter coupled to a chloride channel.

Keywords

RodPhotoreceptorGlutamateTransportRetina
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 1 , January 1996 , pp. 135 - 144
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

Ariel, M., Lasater, E.M., Mangel, S.C. & Dowling, J.E. (1984). On the sensitivity of H1 horizontal cells of the carp retina to gluta-mate, aspartate and their agonists. Brain Research 295, 179–183.CrossRefGoogle Scholar
Arriza, J.L., Fairman, W.A., Wadiche, J.I., Murdoch, G.H., Kavanaugh, M.P. & Amara, S.P. (1994). Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. Journal of Neuroscience 14 (9), 5559–5569.CrossRefGoogle ScholarPubMed
Ascher, P. & Nowak, L. (1987). Electrophysiological studies of NMDA receptors. Trends in Neuroscience 10(7), 284–288.CrossRefGoogle Scholar
Attwell, D., Werblin, F.S., Wilson, M. & Wu, S.M. (1983). A sign-reversing pathway from rods to double and single cones in the retina of the tiger salamander. Journal of Physiology 336, 313–333.CrossRefGoogle ScholarPubMed
Attwell, D. & Wilson, M. (1980). Behavior of the rod network in the tiger salamander retina mediated by membrane properties of individual rods. Journal of Physiology 309, 287–315.CrossRefGoogle ScholarPubMed
Bader, C.R., Bertrand, D. & Schwartz, E.A. (1982). Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. Journal of Physiology 331, 253–284.CrossRefGoogle ScholarPubMed
Balcar, V.J. & Johnston, G.A.R. (1972). The structural specificity of the high affinity uptake of L-glutamate and L-aspartate by rat brain slices. Journal of Neurochemistry 19, 2657–2666.CrossRefGoogle ScholarPubMed
Barbour, B., Brew, H. & Attwell, D. (1991). Electrogenic uptake of glutamate and aspartate into glial cells isolated from the salamander (ambystoma) retina. Journal of Physiology 436, 169–193.CrossRefGoogle ScholarPubMed
Baylor, D.A., Fuortes, M.G.F. & O'Bryan, P.M. (1971). Receptive fields of cones in the retina of the turtle. Journal of Physiology 214, 265–294.CrossRefGoogle ScholarPubMed
Corey, D.P., Dubinsky, J.M. & Schwartz, E.A. (1984). The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. Journal of Physiology 354, 557–575.CrossRefGoogle ScholarPubMed
Eliasof, S. & Werblin, F.S. (1993). Characterization of the glutamate transporter in retinal cones of the tiger salamander. Journal of Neuroscience 13(1), 402–411.CrossRefGoogle ScholarPubMed
Eliasof, S.D., Arriza, J.L., Kavanaugh, M.P., Amara, S.G. & Jahr, C.E. (1995). Functional characterization of glutamate transporter subtypes cloned from salamander retina. Investigative Ophthalmology and Visual Science (Abstract) 36(4), 500–500.Google Scholar
Fenwick, E.M., Marty, A. & Neher, E. (1982). A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. Journal of Physiology 331, 577–597.CrossRefGoogle ScholarPubMed
Grant, G.B. & Dowling, J.E. (1995). A glutamate-activated chloride current in cone ON bipolar cells of the white perch retina. Journal of Neuroscience 15(5), 3852–3862.CrossRefGoogle ScholarPubMed
Grant, G.B. & Werblin, F.S. (1994). Low-cost data acquisition and analysis programs for electrophysiology. Journal of Neuroscience Methods 55, 89–98.CrossRefGoogle ScholarPubMed
Hamill, O.P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F.J. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Archives 391, 85–100.CrossRefGoogle ScholarPubMed
Honore, T., Davies, S.N., Drejer, J., Fletcher, E.J., Jacobsen, P., Lodge, D. & Nielsen, F.E. (1988). Quinoxalinediones: Potent competitive non-NMDA glutamate receptor antagonists. Science 241, 701–703.CrossRefGoogle ScholarPubMed
Ishida, A.T. & Fain, G.L. (1981). D-Aspartate potentiates the effects of L-glutamate on horizontal cell in goldfish retina. Proceedings of the National Academy of Sciences of the U.S.A. 78(9), 5890–5894.CrossRefGoogle ScholarPubMed
Johnston, G.A.R., Kennedy, S.M.E. & Twitchin, B. (1979). Action of the neurotoxin kainic acid on high affinity uptake of L-glutamic acid in rat brain slices. Journal of Neurochemistry 32, 121–127.CrossRefGoogle ScholarPubMed
Kaneko, A. & Tachibana, M. (1986). Effects of gamma-aminobutyric acid on isolated cone photoreceptors of the turtle retina. Journal of Physiology 373, 443–461.CrossRefGoogle ScholarPubMed
Klockner, U., Storck, T., Conradt, M. & Stoffel, W. (1994). Functional properties and substrate specificity of the cloned L-glutamate/L-aspartate transporter GLAST-1 from rat brain expressed in Xen-opus oocytes. Journal of Neuroscience 14(10), 5759–5765.CrossRefGoogle ScholarPubMed
Mangel, S.C, Ariel, M. & Dowling, J.E. (1989). D-aspartate potentiates the effects of both L-aspartate and L-glutamate on carp horizontal cells. Neuroscience 32, 19–26.CrossRefGoogle ScholarPubMed
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, 7639–7643.CrossRefGoogle ScholarPubMed
Miller, R.F. & Dacheux, R.F. (1983). Intracellular chloride in retinal neurons: Measurement and meaning. Vision Research 23(4), 399–411.CrossRefGoogle ScholarPubMed
Murakami, M., Ohtsu, K. & Ohtsuka, T. (1972). Effects of chemicals on receptors and horizontal cells in the retina. Journal of Physiology 227, 899–913.CrossRefGoogle ScholarPubMed
Sarantis, M., Everett, K. & Attwell, D. (1988). A presynaptic action of glutamate at the cone output synapse. Nature 332, 451–453.CrossRefGoogle ScholarPubMed
Schwartz, E.A. & Tachibana, M. (1990). Electrophysiology of glutamate and sodium co-transport in a glial cell of the salamander retina. Journal of Physiology 426, 43–80.CrossRefGoogle Scholar
Shiells, R.A., Falk, G. & Naghshineh, S. (1986). Iontophoretic study of the action of excitatory amino acids on rod horizontal cells of the dogfish retina. Proceedings of the Royal Society B (London) 227, 121–135.Google Scholar
Slaughter, M.M. & Miller, R.F. (1981). 2–Amino-4–phosphonobutyric acid: A new pharmacological tool for retinal research. Science 211, 182–185.CrossRefGoogle Scholar
Spray, D.C., White, R.L., Campos de Carvalho, A., Harris, A.L. & Bennett, M.V.L. (1984). Gating of gap junction channels. Biophysical Journal 45, 219–230.CrossRefGoogle ScholarPubMed
Szatkowski, M., Barbour, B. & Attwell, D. (1991). The potassium-dependence of excitatory amino acid transport: Resolution of a paradox. Brain Research 555, 343–345.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1988). L-Glutamate-induced depolarization in solitary photoreceptors: A process that may contribute to the interaction between photoreceptors in situ. Proceedings of the National Academy of Sciences of the U.S.A. 85, 5315–5319.CrossRefGoogle Scholar
Tang, C.-M., Dichter, M. & Morad, M. (1989). Quisqualate activates a rapidly inactivating high conductance ionic channel in hippocam-pal neurons. Science 243, 1474–1477.CrossRefGoogle Scholar
Wadiche, J.I., Vandenberc, R.J., Arriza, J.L., Amara, S.G. & Kavanaugh, M.P. (1995). Ligand-gated chloride conductance associated with a human glutamate transporter. Biophysical Journal (Abstract) 68(2), A437–A437.Google Scholar
Watkins, J.C. (1981). Pharmacology of excitatory amino acid transmitters. In Amino Acid Neurotransmitters, ed. DeFeudis, F.V. & Mandel, P., pp. 205–212. New York: Raven Press.Google Scholar
Werblin, F.S. (1978). Transmission along and between rods in the tiger salamander retina. Journal of Physiology 280, 449–470.CrossRefGoogle ScholarPubMed
Yang, X.-L. & Wu, S.M. (1989). Effects of CNQX, APB, PDA, and kynurenate on horizontal cells of the tiger salamander retina. Visual Neuroscience 3, 207–212.CrossRefGoogle ScholarPubMed