Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-15T13:25:28.727Z Has data issue: false hasContentIssue false

Pharmacological characterization, localization, and regulation of ionotropic glutamate receptors in skate horizontal cells

Published online by Cambridge University Press:  14 August 2009

MATTHEW A. KREITZER*
Affiliation:
Department of Biological Sciences, University of Illinois at Chicago, Chicago, Illinois Department of Biology, Indiana Wesleyan University, Marion, Indiana
ANDREA D. BIRNBAUM
Affiliation:
Department of Biological Sciences, University of Illinois at Chicago, Chicago, Illinois Department of Ophthalmology and Visual Sciences, University of Illinois at Chicago, Chicago, Illinois
HAOHUA QIAN
Affiliation:
Department of Biological Sciences, University of Illinois at Chicago, Chicago, Illinois Department of Ophthalmology and Visual Sciences, University of Illinois at Chicago, Chicago, Illinois
ROBERT PAUL MALCHOW
Affiliation:
Department of Biological Sciences, University of Illinois at Chicago, Chicago, Illinois Department of Ophthalmology and Visual Sciences, University of Illinois at Chicago, Chicago, Illinois
*
*Address correspondence and reprint requests to: Matthew A. Kreitzer, Department of Biology, Indiana Wesleyan University, 4201 South Washington Street, Marion, IN 46953. E-mail: [email protected]

Abstract

Glutamate is believed to be the primary excitatory neurotransmitter in the vertebrate retina, and its fast postsynaptic effects are elicited by activating NMDA-, kainate-, or AMPA-type glutamate receptors. We have characterized the ionotropic glutamate receptors present on retinal horizontal cells of the skate, which possess a unique all-rod retina simplifying synaptic circuitry within the outer plexiform layer (OPL). Isolated external horizontal cells were examined using whole-cell voltage-clamp techniques. Glutamate and its analogues kainate and AMPA, but not NMDA, elicited dose-dependent currents. The AMPA receptor antagonist GYKI 52466 at 100 μm abolished glutamate-elicited currents. Desensitization of glutamate currents was removed upon coapplication of cyclothiazide, known to potentiate AMPA receptor responses, but not by concanavalin A, which potentiates kainate receptor responses. The dose–response curve to glutamate was significantly broader in the presence of the desensitization inhibitor cyclothiazide. Polyclonal antibodies directed against AMPA receptor subunits revealed prominent labeling of isolated external horizontal cells with the GluR2/3 and GluR4 antibodies. 1-Naphthylacetyl spermine, known to block calcium-permeable AMPA receptors, significantly reduced glutamate-gated currents of horizontal cells. Downregulation of glutamate responses was induced by increasing extracellular ion concentrations of Zn2+ and H+. The present study suggests that Ca2+-permeable AMPA receptors likely play an important role in shaping the synaptic responses of skate horizontal cells and that alterations in extracellular concentrations of calcium, zinc, and hydrogen ions have the potential to regulate the strength of postsynaptic signals mediated by AMPA receptors within the OPL.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 2009

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

Ayoub, G.S., Korenbrot, J.I. & Copenhagen, D.R. (1989). Release of endogenous glutamate from isolated cone photoreceptors of the lizard. Neuroscience Research Supplement 10, S47S55.CrossRefGoogle ScholarPubMed
Bettler, B., Boutler, J., Hermans-Borgmeyer, I., O’Shea-Greenfield, A., Deneris, E.S., Moll, C., Borgmeyer, U., Hollmann, M. & Heinemann, S. (1990). Cloning of a novel glutamate receptor subunit, GluR5: Expression in the nervous system during development. Neuron 5, 583595.CrossRefGoogle ScholarPubMed
Blanco, R. & de la Villa, P. (1999). Ionotropic glutamate receptors in isolated horizontal cells of the rabbit retina. The European Journal of Neuroscience 11, 867873.Google Scholar
Bresink, I., Ebert, B., Parsons, C.G. & Mutschler, E. (1996). Zinc changes AMPA receptor properties: Results of binding studies and patch clamp recordings. Neuropharmacology 35, 503509.CrossRefGoogle ScholarPubMed
Buldakova, S.L., Bolshakov, K.V., Tikhonov, D.B. & Magazanik, L.G. (2000). Ca2+-dependent desensitization of AMPA receptors. Neuroreport 11, 29372941.Google Scholar
Cadetti, L., Tranchina, D. & Thoreson, W.B. (2005). A comparison of release kinetics and glutamate receptor properties in shaping rod-cone differences in EPSC kinetics in the salamander retina. The Journal of Physiology 569, 773788.Google Scholar
Christensen, B.N. & Hida, E. (1990). Protonation of histidine groups inhibits gating of the quisqualate/kainate channel protein in isolated catfish cone horizontal cells. Neuron 5, 471478.Google Scholar
Copenhagen, D.R. & Jahr, C.E. (1989). Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341, 536539.CrossRefGoogle ScholarPubMed
DeVries, S.H. (2001). Exocytosed protons feedback to suppress the Ca2+ current in mammalian cone photoreceptors. Neuron 32, 11071117.CrossRefGoogle ScholarPubMed
Dingledine, R., Borges, K., Bowie, D. & Traynelis, S.F. (1999). The glutamate receptor ion channels. Pharmacological Reviews 51, 761.Google ScholarPubMed
Donevan, S.D. & Rogawski, M.A. (1993). GYKI 52466, a 2,3-benzodiazepine, is a highly selective, noncompetitive antagonist of AMPA/kainate receptor responses. Neuron 10, 5159.CrossRefGoogle Scholar
Dowling, J. (1987). The Retina: An Approachable Part of the Brain. Cambridge, MA: Harvard University Press.Google Scholar
Egebjerg, J., Bettler, B., Hermans-Borgmeyer, I. & Heinemann, S. (1991). Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 351, 745748.CrossRefGoogle Scholar
Eliasof, S. & Jahr, C.E. (1997). Rapid AMPA receptor desensitization in catfish cone horizontal cells. Visual Neuroscience 14, 1318.CrossRefGoogle ScholarPubMed
Fletcher, E.J. & Lodge, D. (1996). New developments in the molecular pharmacology of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate and kainate receptors. Pharmacological Therapy 70, 6589.CrossRefGoogle ScholarPubMed
Gallemore, R.P., Li, J.D., Govardovskii, V.I. & Steinberg, R.H. (1994). Calcium gradients and light-evoked calcium changes outside rods in the intact cat retina. Visual Neuroscience 11, 753761.Google Scholar
Green, D.G., Dowling, J.E., Siegel, I.M. & Ripps, H. (1975). Retinal mechanisms of visual adaptation in the skate. The Journal of General Physiology 65, 483502.Google Scholar
Hack, I., Frech, M., Dick, O., Peichl, L. & Brandstatter, J.H. (2001). Heterogeneous distribution of AMPA glutamate receptor subunits at the photoreceptor synapses of rodent retina. The European Journal of Neuroscience 13, 1524.CrossRefGoogle ScholarPubMed
Hals, G., Christensen, B.N., O’Dell, T., Christensen, M. & Shingai, R. (1986). Voltage-clamp analysis of currents produced by glutamate and some glutamate analogues on horizontal cells isolated from the catfish retina. Journal of Neurophysiology 56, 1931.Google Scholar
Hamassaki-Britto, D.E., Hermans-Borgmeyer, I., Heinemann, S. & Hughes, T.E. (1993). Expression of glutamate receptor genes in the mammalian retina: The localization of GluR1 through GluR7 mRNAs. The Journal of Neuroscience 13, 18881898.CrossRefGoogle ScholarPubMed
Hirasawa, H., Shiells, R. & Yamada, M. (2001). Blocking AMPA receptor desensitization prolongs spontaneous EPSC decay times and depolarizes H1 horizontal cells in carp retinal slices. Neuroscience Research 40, 217225.Google Scholar
Huang, S.-Y. & Liang, P.-J. (2005). Ca2+-permeable and Ca2+ impermeable AMPA receptors coexist on horizontal cells. Neuroreport 16, 263266.Google Scholar
Itazawa, S.-I., Isa, T. & Ozawa, S. (1997). Inwardly rectifying & Ca2+-permeable AMPA-type glutamate receptor channels in rat neocortical neurons. Journal of Neurophysiology 78, 25922605.Google Scholar
Keinanen, K., Wisden, W., Somer, B., Werner, P., Herb, A., Verdoorn, T.A., Sakmann, B. & Seeburg, P.H. (1990). A family of AMPA-selective glutamate receptors. Science 249, 556560.Google Scholar
Kiskin, N.I., Kristal, O.A. & Tsyndrenko, A.Y. (1986). Excitatory amino acid receptors in hippocampal neurons: Kainate fails to desensitize them. Neuroscience Letters 63, 225230.CrossRefGoogle Scholar
Klooster, J., Studholme, K.M. & Yazulla, S. (2001). Localization of the AMPA subunit GluR2 in the outer plexiform layer of goldfish retina. The Journal of Comparative Neurology 441, 155167.Google Scholar
Koike, M., Iino, M. & Ozawa, S. (1997). Blocking effect of 1-naphthyl acetyl spermine on Ca(2+)-permeable AMPA receptors in cultured rat hippocampal neurons. Neuroscience Research 29, 2736.Google Scholar
Kreitzer, M.A., Andersen, K.A. & Malchow, R.P. (2003). Glutamate modulation of GABA transport in retinal horizontal cells of the skate. The Journal of Physiology 546, 717731.CrossRefGoogle ScholarPubMed
Lasater, E.M., Dowling, J.E. & Ripps, H. (1984). Pharmacological properties of isolated horizontal and bipolar cells from the skate retina. The Journal of Neuroscience 4, 19661975.CrossRefGoogle ScholarPubMed
Linn, C.L. & Gafka, A.C. (2001). Modulation of a voltage-gated calcium channel linked to activation of glutamate receptors and calcium-induced calcium release in the catfish retina. The Journal of Physiology 535, 4763.Google Scholar
Linn, C.P. & Christensen, B.N. (1992). Excitatory amino acid regulation of intracellular Ca2+ in isolated catfish cone horizontal cells measured under voltage- and concentration-clamp conditions. The Journal of Neuroscience 12, 21562164.Google Scholar
Liu, J. & Zukin, R.S. (2007). Ca2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends in Neurosciences 30, 126134.CrossRefGoogle ScholarPubMed
Lukasiewicz, P.D., Wilson, J.A. & Lawrence, J.E. (1997). AMPA-preferring receptors mediate excitatory synaptic inputs to retinal ganglion cells. Journal of Neurophysiology 77, 5764.Google Scholar
Lu, T., Shen, Y., & Yang, XL. (1998). Desensitization of AMPA receptors on horizontal cells isolated from crucian carp retino. Neuroscience Research 31, 123135.CrossRefGoogle Scholar
O’Dell, T.J. & Christensen, B.N. (1989 a). Horizontal cells isolated from catfish retina contain two types of excitatory amino acid receptors. Journal of Neurophysiology 61, 10971109.CrossRefGoogle ScholarPubMed
O’Dell, T.J. & Christensen, B.N. (1989 b). A voltage-clamp study of isolated stingray horizontal cell non-NMDA excitatory amino acid receptors. Journal of Neurophysiology 61, 162172.Google Scholar
Okada, T., Schultz, K., Geurtz, W., Hatt, H. & Weller, R. (1999). AMPA-preferring receptors with high Ca2+ permeability mediate dendritic plasticity of retinal horizontal cells. The European Journal of Neuroscience 11, 10851095.CrossRefGoogle ScholarPubMed
Ozawa, S., Kamiya, H. & Tsuzuki, K. (1998). Glutamate receptors in the mammalian central nervous system. Progress in Neurobiology 54, 581618.CrossRefGoogle ScholarPubMed
Partin, K.M., Patneau, D.K, Winters, C.A., Mayer, M.L. & Buonanno, A. (1993). Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11, 10691082.Google Scholar
Patneau, D.K., Vyklicky, L. & Mayer, M.L. (1993). Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate. The Journal of Neuroscience 13, 34963509.CrossRefGoogle ScholarPubMed
Peng, Y.W., Blackstone, C.D., Huganir, R.L. & Yau, K.W. (1995). Distribution of glutamate receptor subtypes in the vertebrate retina. Neuroscience 66, 483497.CrossRefGoogle ScholarPubMed
Qin, P. & Pourcho, R.G. (1996). Distribution of AMPA-selective glutamate receptor subunits in the cat retina. Brain Research 710, 303307.Google Scholar
Rabl, K. & Thoreson, W.B. (2002). Calcium-dependent inactivation and depletion of synaptic cleft calcium ions combine to regulate rod calcium currents under physiological conditions. The European Journal of Neuroscience 16, 20702077.CrossRefGoogle ScholarPubMed
Rassendren, F.A., Lory, P., Pin, J.P. & Nargeot, J. (1990). Zinc has opposite effects on NMDA and non-NMDA receptors expressed in Xenopus oocytes. Neuron 4, 733740.CrossRefGoogle ScholarPubMed
Redenti, S. & Chappell, R.L. (2005). Neuroimaging of zinc released by depolarization of rat retinal cells. Vision Research 45, 35203525.CrossRefGoogle ScholarPubMed
Redenti, S., Ripps, H. & Chappell, R.L. (2007). Zinc release at the synaptic terminals of rod photoreceptors. Experimental Eye Research 85, 580584.Google Scholar
Rivera, L., Blanco, R. & de la Villa, P. (2001). Calcium-permeable glutamate receptors in horizontal cells of the mammalian retina. Visual Neuroscience 18, 9951002.Google Scholar
Rosenstein, F.J. & Chappell, R.L. (2003). Endogenous zinc as a retinal neuromodulator: Evidence from the skate (Raja erinacea). Neuroscience Letters 345, 8184.Google Scholar
Schmidt, K.F. (1999). Divalent cations modulate glutamate receptors in retinal horizontal cells of the perch (Perca fluviatilis). Neuroscience Letters 262, 109112.CrossRefGoogle ScholarPubMed
Schultz, K., Janssen-Bienhold, U. & Weiler, R. (2001). Selective synaptic distribution of AMPA and kainate receptor subunits in the outer plexiform layer of the carp retina. The Journal of Comparative Neurology 435, 433449.CrossRefGoogle ScholarPubMed
Shen, W., Finnegan, S.G. & Slaughter, M.M. (2004). Glutamate receptor subtypes in human retinal horizontal cells. Visual Neuroscience 21, 8995.Google Scholar
Shen, Y., Zhang, M., Jin, Y. & Yang, X.L. (2006). Functional N-methyl-D-aspartate receptors are expressed in cone-driven horizontal cells in carp retina. Neuro-Signals 15, 174179.Google Scholar
Shen, Y.Z., Zhou, Y. & Yang, X.L. (1999). Characterization of AMPA receptors on isolated amacrine-like cells in carp retina. The European Journal of Neuroscience 11, 42334240.Google Scholar
Sommer, B., Burnashev, N., Verdoorn, T.A., Keinanen, K., Sakmann, B. & Seeburg, P.H. (1992). A glutamate receptor channel with high affinity for domoate and kainate. The EMBO Journal 11, 16511656.Google Scholar
Szamier, R.B. & Ripps, H. (1983). The visual cells of the skate retina: Structure, histochemistry, and disc-shedding properties. The Journal of Comparative Neurology 215, 5162.CrossRefGoogle ScholarPubMed
Tang, C.M., Dichter, M. & Morad, M. (1990). Modulation of the N-methyl-D-aspartate channel by extracellular H+. Proceedings of the National Academy of Sciences of the United States of America 87, 64456449.CrossRefGoogle ScholarPubMed
Tarnawa, I., Farkas, S., Berzsenyi, P., Patfalusi, M. & Andrasi, F. (1990). Reflex inhibitory action of a non-NMDA type excitatory amino acid antagonist, GYKI 52466. Acta Physiologica Hungarica 75, 277278.Google Scholar
Thoreson, W.B. & Witkovsky, P. (1999). Glutamate receptors and circuits in the vertebrate retina. Progress in Retinal and Eye Research 18, 765810.CrossRefGoogle ScholarPubMed
Traynelis, S.F. & Cull-Candy, S.G. (1991). Pharmacological properties and H+ sensitivity of excitatory amino acid receptor channels in rat cerebellar granule neurones. The Journal of Physiology 433, 727763.Google Scholar
Ugarte, M. & Osborne, N.N. (2001). Zinc in the retina. Progress in Neurobiology 64, 219249.CrossRefGoogle ScholarPubMed
Wu, S.M., Qiao, X., Noebels, J.L. & Yang, X.L. (1993). Localization and modulatory actions of zinc in vertebrate retina. Vision Research 33, 26112616.Google Scholar
Wu, X. & Christensen, B.N. (1996). Proton inhibition of the NMDA-gated channel in isolated catfish cone horizontal cells. Vision Research 36, 15211528.Google Scholar
Yang, J.H., Maple, B., Gao, F., Maguire, G. & Wu, S.M. (1998). Postsynaptic responses of horizontal cells in the tiger salamander retina are mediated by AMPA-preferring receptors. Brain Research 797, 125134.CrossRefGoogle ScholarPubMed
Zhang, D.Q., Ribelayga, C., Mangel, S.C. & McMahon, D.G. (2002). Suppression by zinc of AMPA receptor-mediated synaptic transmission in the retina. Journal of Neurophysiology 88, 12451251.Google Scholar