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The influences of metabotropic receptor activation on cellular signaling and synaptic function in amacrine cells

Published online by Cambridge University Press:  25 August 2011

EVANNA GLEASON*
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana
*
*Address correspondence and reprint requests to: Evanna Gleason, Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803. E-mail: egleaso@lsu.edu

Abstract

Amacrine cells receive glutamatergic input from bipolar cells and GABAergic, glycinergic, cholinergic, and dopaminergic input from other amacrine cells. Glutamate, GABA, glycine, and acetylcholine (ACh) interact with ionotropic receptors and it is these interactions that form much of the functional circuitry in the inner retina. However, glutamate, GABA, ACh, and dopamine also activate metabotropic receptors linked to second messenger pathways that have the potential to modify the function of individual cells as well as retinal circuitry. Here, the physiological effects of activating dopamine receptors, metabotropic glutamate receptors, GABAB receptors, and muscarinic ACh receptors on amacrine cells will be discussed. The retina also expresses metabotropic receptors and the biochemical machinery associated with the synthesis and degradation of endocannabinoids and sphingosine-1-phosphate (S1P). The effects of activating cannabinoid receptors and S1P receptors on amacrine cell function will also be addressed.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2011

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References

Alger, B.E. (2002). Retrograde signaling in the regulation of synaptic transmission: Focus on endocannabinoids. Progress in Neurobiology 68, 247286.CrossRefGoogle ScholarPubMed
Aramori, I. & Nakanishi, S. (1992). Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron 8, 757765.Google Scholar
Begg, M., Pacher, P., Batkai, S., Osei-Hyiaman, D., Offertaler, L., Mo, F.M., Liu, J. & Kunos, G. (2005). Evidence for novel cannabinoid receptors. Pharmacology & Therapeutics 106, 133145.CrossRefGoogle ScholarPubMed
Bieda, M.C. & Copenhagen, D.R. (2004). N-type and L-type calcium channels mediate glycinergic synaptic inputs to retinal ganglion cells of tiger salamanders. Visual Neuroscience 21, 545550.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Volgyi, B. (2004). Function and plasticity of homologous coupling between AII amacrine cells. Vision Research 44, 32973306.CrossRefGoogle ScholarPubMed
Bloomfield, S.A., Xin, D. & Osborne, T. (1997). Light-induced modulation of coupling between AII amacrine cells in the rabbit retina. Visual Neuroscience 14, 565576.CrossRefGoogle ScholarPubMed
Borges, S., Lindstrom, S., Walters, C., Warrier, A. & Wilson, M. (2008). Discrete influx events refill depleted Ca2+ stores in a chick retinal neuron. The Journal of Physiology 586, 605626.CrossRefGoogle Scholar
Brandstatter, J.H., Koulen, P., Kuhn, R., van der Putten, H. & Wassle, H. (1996). Compartmental localization of a metabotropic glutamate receptor (mGluR7): Two different active sites at a retinal synapse. The Journal of Neuroscience 16, 47494756.CrossRefGoogle Scholar
Cai, W. & Pourcho, R.G. (1999). Localization of metabotropic glutamate receptors mGluR1alpha and mGluR2/3 in the cat retina. The Journal of Comparative Neurology 407, 427437.Google Scholar
Caramelo, O.L., Santos, P.F., Carvalho, A.P. & Duarte, C.B. (1999). Metabotropic glutamate receptors modulate [(3)H]acetylcholine release from cultured amacrine-like neurons. Journal of Neuroscience Research 58, 505514.Google Scholar
Cheng, K.T., Liu, X., Ong, H.L., Swaim, W. & Ambudkar, I.S. (2011). Local Ca2+ entry via Orai1 regulates plasma membrane recruitment of TRPC1 and controls cytosolic Ca2+ signals required for specific cell functions. PLoS Biology 9, e1001025.Google Scholar
Cimini, B.A., Strang, C.E., Wotring, V.E., Keyser, K.T. & Eldred, W.D. (2008). Role of acetylcholine in nitric oxide production in the salamander retina. The Journal of Comparative Neurology 507, 19521963.CrossRefGoogle ScholarPubMed
Crousillac, S., Colonna, J., McMains, E. & Gleason, E.L. (2009). Sphingosine-1-phosphate elicits receptor-dependent calcium signaling in retinal amacrine cells. Journal of Neurophysiology 102, 32953309.CrossRefGoogle ScholarPubMed
Dumitrescu, O.N., Pucci, F.G., Wong, K.Y. & Berson, D.M. (2009). Ectopic retinal ON bipolar cell synapses in the OFF inner plexiform layer: Contacts with dopaminergic amacrine cells and melanopsin ganglion cells. The Journal of Comparative Neurology 517, 226244.CrossRefGoogle ScholarPubMed
Feigenspan, A. & Bormann, J. (1994). Facilitation of GABAergic signaling in the retina by receptors stimulating adenylate cyclase. Proceedings of the National Academy of Sciences of the United States of America 91, 1089310897.Google Scholar
Feigenspan, A., Teubner, B., Willecke, K. & Weiler, R. (2001). Expression of neuronal connexin36 in AII amacrine cells of the mammalian retina. The Journal of Neuroscience 21, 230239.Google Scholar
Filip, M. & Frankowska, M. (2008). GABA(B) receptors in drug addiction. Pharmacological Reports 60, 755770.Google ScholarPubMed
Fischer, A.J., McKinnon, L.A., Nathanson, N.M. & Stell, W.K. (1998). Identification and localization of muscarinic acetylcholine receptors in the ocular tissues of the chick. The Journal of Comparative Neurology 392, 273284.Google Scholar
Francesconi, A. & Duvoisin, R.M. (1998). Role of the second and third intracellular loops of metabotropic glutamate receptors in mediating dual signal transduction activation. The Journal of Biological Chemistry 273, 56155624.Google Scholar
Ghosh, T.K., Bian, J. & Gill, D.L. (1994). Sphingosine 1-phosphate generated in the endoplasmic reticulum membrane activates release of stored calcium. The Journal of Biological Chemistry 269, 2262822635.CrossRefGoogle ScholarPubMed
Gleason, E., Borges, S. & Wilson, M. (1993). Synaptic transmission between pairs of retinal amacrine cells in culture. The Journal of Neuroscience 13, 23592370.Google Scholar
Gleason, E., Borges, S. & Wilson, M. (1994). Control of transmitter release from retinal amacrine cells by Ca2+ influx and efflux. Neuron 13, 11091117.Google Scholar
Gomes, A.R., Cunha, P., Nuriya, M., Faro, C.J., Huganir, R.L., Pires, E.V., Carvalho, A.L. & Duarte, C.B. (2004). Metabotropic glutamate and dopamine receptors co-regulate AMPA receptor activity through PKA in cultured chick retinal neurones: Effect on GluR4 phosphorylation and surface expression. Journal of Neurochemistry 90, 673682.Google Scholar
Habermann, C.J., O’Brien, B.J., Wassle, H. & Protti, D.A. (2003). AII amacrine cells express L-type calcium channels at their output synapses. The Journal of Neuroscience 23, 69046913.CrossRefGoogle ScholarPubMed
Hampson, E.C., Vaney, D.I. & Weiler, R. (1992). Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina. The Journal of Neuroscience 12, 49114922.Google Scholar
Hartveit, E. (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. Journal of Neurophysiology 81, 29232936.CrossRefGoogle ScholarPubMed
Hensler, J.G. & Dubocovich, M.L. (1986). D1-dopamine receptor activation mediates [3H]acetylcholine release from rabbit retina. Brain Research 398, 407412.CrossRefGoogle ScholarPubMed
Hla, T., Lee, M.J., Ancellin, N., Liu, C.H., Thangada, S., Thompson, B.D. & Kluk, M. (1999). Sphingosine-1-phosphate: Extracellular mediator or intracellular second messenger? Biochemical Pharmacology 58, 201207.Google Scholar
Hoffpauir, B.K. & Gleason, E.L. (2002). Activation of mGluR5 modulates GABA(A) receptor function in retinal amacrine cells. Journal of Neurophysiology 88, 17661776.Google Scholar
Hoffpauir, B., McMains, E. & Gleason, E. (2006). Nitric oxide transiently converts synaptic inhibition to excitation in retinal amacrine cells. Journal of Neurophysiology 95, 28662877.CrossRefGoogle ScholarPubMed
Hu, S.S., Arnold, A., Hutchens, J.M., Radicke, J., Cravatt, B.F., Wager-Miller, J., Mackie, K. & Straiker, A. (2010). Architecture of cannabinoid signaling in mouse retina. The Journal of Comparative Neurology 518, 38483866.Google Scholar
Jensen, R.J. (2006). Activation of group II metabotropic glutamate receptors reduces directional selectivity in retinal ganglion cells. Brain Research 1122, 8692.CrossRefGoogle ScholarPubMed
Joly, C., Gomeza, J., Brabet, I., Curry, K., Bockaert, J. & Pin, J.P. (1995). Molecular, functional, and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: Comparison with mGluR1. The Journal of Neuroscience 15, 39703981.Google Scholar
Kajimoto, T., Okada, T., Yu, H., Goparaju, S.K., Jahangeer, S. & Nakamura, S. (2007). Involvement of sphingosine-1-phosphate in glutamate secretion in hippocampal neurons. Molecular & Cellular Biology 27, 34293440.CrossRefGoogle ScholarPubMed
Kanno, T., Nishizaki, T., Proia, R.L., Kajimoto, T., Jahangeer, S., Okada, T. & Nakamura, S. (2010). Regulation of synaptic strength by sphingosine 1-phosphate in the hippocampus. Neuroscience 171, 973980.CrossRefGoogle ScholarPubMed
Kim, R.H., Takabe, K., Milstien, S. & Spiegel, S. (2009). Export and functions of sphingosine-1-phosphate. Biochimica et Biophysica Acta 1791, 692696.Google Scholar
Kothmann, W.W., Massey, S.C. & O’Brien, J. (2009). Dopamine-stimulated dephosphorylation of connexin 36 mediates AII amacrine cell uncoupling. The Journal of Neuroscience 29, 1490314911.Google Scholar
Koulen, P. & Brandstatter, J.H. (2002). Pre- and postsynaptic sites of action of mGluR8a in the mammalian retina. Investigative Ophthalmology & Visual Science 43, 19331940.Google ScholarPubMed
Koulen, P., Kuhn, R., Wassle, H. & Brandstatter, J.H. (1997). Group I metabotropic glutamate receptors mGluR1alpha and mGluR5a: Localization in both synaptic layers of the rat retina. The Journal of Neuroscience 17, 22002211.Google Scholar
Koulen, P., Malitschek, B., Kuhn, R., Bettler, B., Wassle, H. & Brandstatter, J.H. (1998). Presynaptic and postsynaptic localization of GABA(B) receptors in neurons of the rat retina. The European Journal of Neuroscience 10, 14461456.CrossRefGoogle ScholarPubMed
Koulen, P., Malitschek, B., Kuhn, R., Wassle, H. & Brandstatter, J.H. (1996). Group II and group III metabotropic glutamate receptors in the rat retina: Distributions and developmental expression patterns. The European Journal of Neuroscience 8, 21772187.CrossRefGoogle ScholarPubMed
Kreimborg, K.M., Lester, M.L., Medler, K.F. & Gleason, E.L. (2001). Group I metabotropic glutamate receptors are expressed in the chicken retina and by cultured retinal amacrine cells. Journal of Neurochemistry 77, 452465.CrossRefGoogle Scholar
Kreitzer, A.C. & Regehr, W.G. (2001). Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29, 717727.Google Scholar
Liou, J., Kim, M.L., Heo, W.D., Jones, J.T., Myers, J.W., Ferrell, J.E. Jr & Meyer, T. (2005). STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Current Biology 15, 12351241.Google Scholar
Lu, Q., Straiker, A. & Maguire, G. (2000). Expression of CB2 cannabinoid receptor mRNA in adult rat retina. Visual Neuroscience 17, 9195.Google Scholar
Marc, R.E. & Liu, W. (2000). Fundamental GABAergic amacrine cell circuitries in the retina: Nested feedback, concatenated inhibition, and axosomatic synapses. The Journal of Comparative Neurology 425, 560582.Google Scholar
Masu, M., Iwakabe, H., Tagawa, Y., Miyoshi, T., Yamashita, M., Fukuda, Y., Sasaki, H., Hiroi, K., Nakamura, Y., Shigemoto, R., Takada, M., Nakamura, K., Nakao, K., Katsoki, M. &Nakanishi, S. (1995). Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80, 757765.Google Scholar
Mills, S.L., O’Brien, J.J., Li, W., O’Brien, J. & Massey, S.C. (2001). Rod pathways in the mammalian retina use connexin 36. The Journal of Comparative Neurology 436, 336350.CrossRefGoogle ScholarPubMed
Mills, S.L., Xia, X.B., Hoshi, H., Firth, S.I., Rice, M.E., Frishman, L.J. & Marshak, D.W. (2007). Dopaminergic modulation of tracer coupling in a ganglion-amacrine cell network. Visual Neuroscience 24, 593608.Google Scholar
Neal, M.J. & Cunningham, J.R. (1995). Baclofen enhancement of acetylcholine release from amacrine cells in the rabbit retina by reduction of glycinergic inhibition. The Journal of Physiology 482(Pt 2), 363372.Google Scholar
Okamoto, H., Takuwa, N., Gonda, K., Okazaki, H., Chang, K., Yatomi, Y., Shigematsu, H. & Takuwa, Y. (1998). EDG1 is a functional sphingosine-1-phosphate receptor that is linked via a Gi/o to multiple signaling pathways, including phospholipase C activation, Ca2+ mobilization, Ras-mitogen-activated protein kinase activation, and adenylate cyclase inhibition. The Journal of Biological Chemistry 273, 2710427110.Google Scholar
Olivera, A., Rosenthal, J. & Spiegel, S. (1996). Effect of acidic phospholipids on sphingosine kinase. Journal of Cellular Biochemistry 60, 529537.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Prakriya, M., Feske, S., Gwack, Y., Srikanth, S., Rao, A. & Hogan, P.G. (2006). Orai1 is an essential pore subunit of the CRAC channel. Nature 443, 230233.Google Scholar
Quraishi, S., Gayet, J., Morgans, C.W. & Duvoisin, R.M. (2007). Distribution of group-III metabotropic glutamate receptors in the retina. The Journal of Comparative Neurology 501, 931943.Google Scholar
Quraishi, H., Rush, S.J. & Brown, I.R. (1996). Expression of mRNA species encoding heat shock protein 90 (hsp90) in control and hyperthermic rabbit brain. Journal of Neuroscience Research 43, 335345.Google Scholar
Sanchez, T. & Hla, T. (2004). Structural and functional characteristics of S1P receptors. Journal of Cellular Biochemistry 92, 913922.CrossRefGoogle ScholarPubMed
Sen, M. & Gleason, E. (2006). Immunolocalization of metabotropic glutamate receptors 1 and 5 in the synaptic layers of the chicken retina. Visual Neuroscience 23, 221231.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Bai, S.H. (1989). Differential effects of baclofen on sustained and transient cells in the mudpuppy retina. Journal of Neurophysiology 61, 374381.Google Scholar
Sosa, R. & Gleason, E. (2004). Activation of mGluR5 modulates Ca2+ currents in retinal amacrine cells from the chick. Visual Neuroscience 21, 807816.Google Scholar
Sosa, R., Hoffpauir, B., Rankin, M.L., Bruch, R.C. & Gleason, E.L. (2002). Metabotropic glutamate receptor 5 and calcium signaling in retinal amacrine cells. Journal of Neurochemistry 81, 973983.Google Scholar
Straiker, A., Stella, N., Piomelli, D., Mackie, K., Karten, H.J. & Maguire, G. (1999). Cannabinoid CB1 receptors and ligands in vertebrate retina: Localization and function of an endogenous signaling system. Proceedings of the National Academy of Sciences of the United States of America 96, 1456514570.Google Scholar
Strang, C.E., Renna, J.M., Amthor, F.R. & Keyser, K.T. (2010). Muscarinic acetylcholine receptor localization and activation effects on ganglion response properties. Investigative Ophthalmology & Visual Science 51, 27782789.Google Scholar
Sutherland, C.M., Moretti, P.A., Hewitt, N.M., Bagley, C.J., Vadas, M.A. & Pitson, S.M. (2006). The calmodulin-binding site of sphingosine kinase and its role in agonist-dependent translocation of sphingosine kinase 1 to the plasma membrane. The Journal of Biological Chemistry 281, 1169311701.Google Scholar
Vardi, N. & Morigiwa, K. (1997). ON cone bipolar cells in rat express the metabotropic receptor mGluR6. Visual Neuroscience 14, 789794.Google Scholar
Veruki, M.L. (1997). Dopaminergic neurons in the rat retina express dopamine D2/3 receptors. The European Journal of Neuroscience 9, 10961100.CrossRefGoogle ScholarPubMed
Vigh, J. & Lasater, E.M. (2003). Intracellular calcium release resulting from mGluR1 receptor activation modulates GABAA currents in wide-field retinal amacrine cells: A study with caffeine. The European Journal of Neuroscience 17, 22372248.Google Scholar
Vigh, J. & Lasater, E.M. (2004). L-type calcium channels mediate transmitter release in isolated, wide-field retinal amacrine cells. Visual Neuroscience 21, 129134.Google Scholar
Vigh, J., Li, G.L., Hull, C. & von Gersdorff, H. (2005). Long-term plasticity mediated by mGluR1 at a retinal reciprocal synapse. Neuron 46, 469482.CrossRefGoogle Scholar
Warrier, A., Borges, S., Dalcino, D., Walters, C. & Wilson, M. (2005). Calcium from internal stores triggers GABA release from retinal amacrine cells. Journal of Neurophysiology 94, 41964208.Google Scholar
Wagner, H.J., Luo, B.G., Ariano, M.A., Sibley, D.R. & Stell, W.K. (1993). Localization of D2 dopamine receptors in vertebrate retinae with anti-peptide antibodies. The Journal of Comparative Neurology 331, 469481.Google Scholar
Warrier, A. & Wilson, M. (2007). Endocannabinoid signaling regulates spontaneous transmitter release from embryonic retinal amacrine cells. Visual Neuroscience 24, 2535.CrossRefGoogle ScholarPubMed
Wilson, R.I., Kunos, G. & Nicoll, R.A. (2001). Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31, 453462.Google Scholar
Xia, X.B. & Mills, S.L. (2004). Gap junctional regulatory mechanisms in the AII amacrine cell of the rabbit retina. Visual Neuroscience 21, 791805.Google Scholar
Yamada, E.S., Dmitrieva, N., Keyser, K.T., Lindstrom, J.M., Hersh, L.B. & Marshak, D.W. (2003). Synaptic connections of starburst amacrine cells and localization of acetylcholine receptors in primate retinas. The Journal of Comparative Neurology 461, 7690.Google Scholar
Yazulla, S. (2008). Endocannabinoids in the retina: from marijuana to neuroprotection. Progress in Retinal & Eye Research 27, 501526.Google Scholar
Yazulla, S., Studholme, K.M., McIntosh, H.H. & Deutsch, D.G. (1999). Immunocytochemical localization of cannabinoid CB1 receptor and fatty acid amide hydrolase in rat retina. The Journal of Comparative Neurology 415, 8090.Google Scholar
Yazulla, S., Studholme, K.M., McIntosh, H.H. & Fan, S.F. (2000). Cannabinoid receptors on goldfish retinal bipolar cells: Electron-microscope immunocytochemistry and whole-cell recordings. Visual Neuroscience 17, 391401.CrossRefGoogle ScholarPubMed
Yeh, H.H., Battelle, B.A. & Puro, D.G. (1984). Dopamine regulates synaptic transmission mediated by cholinergic neurons of the rat retina. Neuroscience 13, 901909.Google Scholar
Zhang, C., Bettler, B. & Duvoisin, R.M. (1998). Differential localization of GABA(B) receptors in the mouse retina. Neuroreport 9, 34933497.Google Scholar
Zhang, Y.H., Fehrenbacher, J.C., Vasko, M.R. & Nicol, G.D. (2006). Sphingosine-1-phosphate via activation of a G-protein-coupled receptor(s) enhances the excitability of rat sensory neurons. Journal of Neurophysiology 96, 10421052.Google Scholar
Zhang, J., Jung, C.S. & Slaughter, M.M. (1997). Serial inhibitory synapses in retina. Visual Neuroscience 14, 553563.Google Scholar
Zhang, D.Q., Wong, K.Y., Sollars, P.J., Berson, D.M., Pickard, G.E. & McMahon, D.G. (2008). Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons. Proceedings of the National Academy of Sciences of the United States of America 105, 1418114186.CrossRefGoogle ScholarPubMed
Zhang, D.Q., Zhou, T.R. & McMahon, D.G. (2007). Functional heterogeneity of retinal dopaminergic neurons underlying their multiple roles in vision. The Journal of Neuroscience 27, 692699.Google Scholar
Zucker, C.L. & Ehinger, B. (2001). Complexities of retinal circuitry revealed by neurotransmitter receptor localization. Progress in Brain Research 131, 7181.Google Scholar
Zucker, C.L., Nilson, J.E., Ehinger, B. & Grzywacz, N.M. (2005). Compartmental localization of gamma-aminobutyric acid type B receptors in the cholinergic circuitry of the rabbit retina. The Journal of Comparative Neurology 493, 448459.Google Scholar