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Activation of mGluR5 modulates Ca2+ currents in retinal amacrine cells from the chick

Published online by Cambridge University Press:  25 February 2005

ROMINA SOSA  and
EVANNA GLEASON
ROMINA SOSA
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge Present address: Department of Neuroscience, University of Minnesota, Minneapolis, MN 70803, USA.
EVANNA GLEASON
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge
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Abstract

In the inner plexiform layer, amacrine cells receive glutamatergic input from bipolar cells. Glutamate can depolarize amacrine cells by activation of ionotropic glutamate receptors or mediate potentially more diverse changes via activation of G protein-coupled metabotropic glutamate receptors (mGluR5). Here, we asked whether selective activation of metabotropic glutamate receptor 5 is linked to modulation of the voltage-gated Ca2+ channels expressed by cultured GABAergic amacrine cells. To address this, we performed whole-cell voltage clamp experiments, primarily in the perforated-patch configuration. We found that agonists selective for mGluR5, including (RS)-2-chloro-5-hydroxyphenylglycine (CHPG), enhanced the amplitude of the voltage-dependent Ca2+ current. The voltage-dependent Ca2+ current and CHPG-dependent current enhancement were blocked by nifedipine, indicating that L-type Ca2+ channels, specifically, were being modulated. We have previously shown that activation of mGluR5 produces Ca2+ elevations in cultured amacrine cells (Sosa et al., 2002). Loading the cells with 5 mM BAPTA inhibited the mGluR5-dependent enhancement, suggesting that the cytosolic Ca2+ elevations are required for modulation of the current. Although activation of mGluR5 is typically linked to activation of protein kinase C, we found that direct activation of this kinase leads to inhibition of the Ca2+ current, indicating that stimulation of this enzyme is not responsible for the mGluR5-dependent enhancement. Interestingly, direct stimulation of protein kinase A produced an enhancement of the Ca2+ current similar to that observed with activation of mGluR5. Thus, activation of mGluR5 may modulate the L-type voltage-gated Ca2+ current in these GABAergic amacrine cells via activation of protein kinase A, possibly via direct activation of a Ca2+-dependent adenylate cyclase.

Keywords

Metabotropic glutamate receptorsAmacrine cellsL-type calcium channelsModulation
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 6 , November 2004 , pp. 807 - 816
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

Abe, T., Sugihara, H., Nawa, H., Sheemoto, R., Mizuno, N., & Nakanishi, S. (1992). Molecular characterization of a novel metabotrophic glutamate receptor mGluR5 coupled to inosito phosphate Ca2+ signal transduction. Journal of Biological Chemistry 267, 13361–13368.Google Scholar
Anderson, M.E., Braun, A.P., Schulman, H., & Premack, B.A. (1994). Multifunctional Ca2+/calmodulin-dependent protein kinase mediates Ca(2+)-induced enhancement of the L-type Ca2+ current in rabbit ventricular myocytes. Circulatory Research 75, 854–861.Google Scholar
Bean, B.P., Nowycky, M.C., & Tsien, R.W. (1984). β-Adrenergic modulation of calcium channels in frog ventricular heart cells. Nature 307, 371–375.Google Scholar
Bünemann, M., Gerhardstein, B.L., Gao, T., & Hosey, M.M. (1999). Functional regulation of L-type calcium channels via protein kinase A-mediated phosphorylation of the β2 subunit. Journal of Biological Chemistry 274, 33851–33854.Google Scholar
Cachelin, A.B., Peyer, J.E., Kokubun, S., & Reuter, H. (1983). Ca2+ channel modulation by 8-bromocyclic AMP in cultured heart cells. Nature 304, 462–464.Google Scholar
Cai, W. & Pourcho, R.G. (1999). Localization of metabotropic glutamate receptors mGluR1alpha and mGluR2/3 in the cat retina. Journal of Computational Neurology 407, 427–437.Google Scholar
Carvalho, A.L., Duarte, C.B., Faro, C.J., Carvalho, A.P., & Pires, E.V. (1998). Calcium influx trough AMPA receptors and through calcium channels is regulated by protein kinase C in cultured retinal amacrine-like cells. Journal of Neurochemistry 70, 2112–2119.Google Scholar
Catterall, W.A. (2000). Structure and regulation of voltage-gated Ca2+ channels. Annual Review of Cell Developmental Biology 16, 521–555.Google Scholar
Conn, C. & Pin, J.P. (1997). Pharamcology and functions of metabotropic glutamate receptors. Annual Review of Pharmacology and Toxicology 37, 205–237.Google Scholar
Cook, P.B. & Werblin, F.S. (1994). Spike initiation and propagation in wide-field transient amacrine cells of the salamander retina. Journal of Neuroscience 14, 3852–3861.Google Scholar
Defer, N., Best-Belpomme, M., & Hanoune, J. (2000). Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase. American Journal of Physiology—Renal Physiology 279, F400–F416.Google Scholar
De Jongh, K.S., Warner, C., Colvin, A.A., & Catterall, W.A. (1991). Characterization of the two size forms of the α1 subunit of skeletal muscle L-type calcium channels. Proceedings of the National Academy of Sciences of the U.S.A. 88, 10778–10782.Google Scholar
Doherty, A.J., Palmer, M.J., Henley, J.M., Collingridge, G.L., & Jane, D.E. (1997). (RS)-2-choloro-5-hydroxyphenylglycine (CHPG) activates mGlu5 but not mGlu1, receptors expressed in CHO cells and potentiates NMDA responses in the hippocampus. Neuropharmacology 36, 2665–2667.Google Scholar
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the National Academy of Sciences of the U.S.A. 166, 80–111.Google Scholar
Dubin, M.W. (1970). The inner plexiform layer of the vertebrate retina: A quantitative and comparative electron-microscopic analysis. Journal of Comparative Neurology 140, 479–506.Google Scholar
Dzhura, I., Wu, Y., Zhang, R., Colbran, R.J., Hamilton, S.L., & Anderson, M.E. (2003). C terminus L-type Ca2+ channel calmodulin-binding domains are ‘auto-agonist’ ligands in rabbit ventricular myocytes. Journal of Physiology 550.3, 731–738.Google Scholar
Firth, S.I., Morgan, I.G., Boelen, M.K., & Morgans, C.W. (2001). Localization voltage-sensitive L-Type calcium channels in the chicken retina. Clinical and Experimental Ophthalmology 29, 183–187.Google Scholar
Francesconi, A. & Duvoisin, R.M. (1998). Role of the second third intracellular loops of the metabotropic glutamate receptors in the mediation dual signal transduction activation. Journal of Biological Chemistry 273, 5615–5624.Google Scholar
French, S.W., Palmer, D.S., & Caldwell, M. (1978). Cytochemical localization of adenylate cyclase in broken cell preparations of the cerebral cortex. Canadian Journal of Neurological Sciences 5, 33–40.Google Scholar
Gleason, E., Mobbs, P., Nuccitelli, R., & Wilson, M. (1992). Development of functional calcium channels in the cultured avian photoreceptors. Visual Neuroscience 8, 315–327.Google Scholar
Gleason, E., Borges, S., & Wilson, M. (1993). Synaptic transmission between pairs of retinal amacrine cells in culture. Journal of Neuroscience 13, 2359–2370.Google Scholar
Gleason, E., Borges, S., & Wilson, M. (1994). Control of transmitter release from retinal amacrine cells by Ca2+ influx and efflux. Neuron 13, 1109–1117.Google Scholar
Gray, R. & Johnston, D. (1987). Noradrenaline and β-adrenoceptor agonists increase activity of voltage-dependent calcium channels in hippocampal neurons. Nature 327, 620–622.Google Scholar
Gross, R.A., Uhler, M.D., & MacDonald, R.L. (1990). The cyclic AMP-dependent protein kinase catalytic subunit selectively enhances calcium currents in rat nodose neurones. Journal of Physiology 429, 483–496.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. Journal of Neuroscience 23, 6904–6913.Google Scholar
He, J., Pi, Y., Walker, J.W., & Kamp, T.J. (2000). Endothelin-1 and photoreleased diacyclglycerol increase L-type Ca2+ current by activation of protein kinase C in rat ventricular myocytes. Journal of Physiology 524.3, 807–820.Google Scholar
Hell, J.W., Yokoyama, C.T., Wong, S.T., Warner, C., Snutch, T.P., & Catterall, W.A. (1993). Differential phosphorylation of two size forms of the neuronal class C L-type calcium channel α1 subunit. Journal of Biological Chemistry 268, 19451–19457.Google Scholar
Hoffpauir, B.K. & Gleason, E.L. (2002). Activation of mGluR5 modulates GABAA receptor function in retinal amacrine cells. Journal of Neurophysiology 88, 1–11.Google Scholar
Huba, R. & Hofmann, H.D. (1991). Transmitter-gated currents of GABAergic amacrine-like cells in chick retinal cultures. Visual Neuroscience 6, 303–314.Google Scholar
Huba, R., Schneider, H., & Hofmann, H.D. (1992). Voltage gated currents of putative GABAergic amacrine cells in primary cultures and in the retinal slice preparations. Brain Research 577, 10–18.Google Scholar
Joly, C., Gomeza, J., Brabert, 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. Journal of Neuroscience 15, 3970–3981.Google Scholar
Kamp, T.J. & Hell, J.W. (2000). Regulation of cardiac L-type calcium channels by protein kniase A and protein kinase C. Circulation Research 87, 1095–1102.Google Scholar
Kavalali, E.T., Hwang, K.S., & Plummer, M.R. (1997). cAMP-dependent enhancement of dihydropyridine-sensitive calcium channel availability in hippocampal neurons. Journal of Neuroscience 17, 5334–5348.Google Scholar
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of cat retina. Science 18, 647–649.Google Scholar
Koulen, P., Kuhn, R., Wassle, H., & Brandstatter, J.H. (1997). Group 1 metabotropic glutamate receptors mGluR1 alpha and mGluR5a: Localization in both synaptic layers of the rat retina. Journal of Neuroscience 17, 2200–2211.Google Scholar
Kreimborg, K.M., Lester, M.L., Medler, K.F., & Gleason, E.L. (2001). Group 1 metabotropic glutamate receptors are expressed in the chicken retina and by cultured retinal amacrine cells. Journal of Neurochemistry 77, 452–465.Google Scholar
Lacerda, A.E., Rampe, D., & Brown, A.M. (1988). Effects of protein kinase C activators on cardiac Ca2+ channels. Nature 335, 249–251.Google Scholar
Maguire, G. (1999). Spatial heterogeneity and function of voltage- and ligand-gated ion channels in retinal amacrine neurons. Proceedings of the Royal Society B (London) 266, 987–992.Google Scholar
McCool, B.A., Pin, J.P., Harpold, M.M., Brust, B.F., Stauderman, K.A., & Lovinger, D.M. (1998). Rat group I metabotropic glutamate receptors inhibit neuronal Ca2+ channels via multiple signal-transduction pathways in HEK 293 cells. Journal of Neurophysiology 79, 379–391.Google Scholar
McHugh, D., Sharp, E.M., Scheuer, T., & Catterall, W.A. (2000). Inhibition of cardiac L-type calcium channels by protein kinase C phosphorylation of two sites in the N-terminal domain. Proceedings of the National Academy of Sciences of the U.S.A 97, 12334–12338.Google Scholar
Morgans, C.W. (2001). Localization of the alpha(1F) calcium channel subunit in the rat retina. Investigative Ophthalmology and Visual Science 42, 2414–2418.Google Scholar
Puri, T.S., Gerhardstein, B.L., Zhao, X.L., Ladner, M.B., & Hosey, M.M. (1997). Differential effects of subunit interactions on protein kinase A- and C-mediated phosphorylation of L-type calcium channels. Biochemistry 36, 9605–9615.Google Scholar
Röhrkasten, A., Meyer, H.E., Nastainczyk, W.N., Sierber, M., & Hofmann, F. (1988). cAMP-dependent protein kinase rapidly phosphoryaltes serine-687 of the skeletal muscle receptor for calcium channel blockers. Journal of Biological Chemistry 263, 15325–15329.Google Scholar
Rotman, E.I., DeJongh, K.S., Florio, V., Lai, Y., & Catterall, W.A. (1992). Specific phosphoryaltion of a COOH-terminal site on the full-length form of the α1 subunit of the skeletal muscle calcium channel by cAMP-dependent protein kinase. Journal of Biological Chemistry 267, 16100–16105.Google Scholar
Sanders, E.J. (1987). Ultrastructural cytochemical localization of adenylate cyclase in the early chick embryo. Cell Tissue Research 247, 465–468.Google Scholar
Sculptoreanu, A. & de Groat, W.C. (2003). Protein kinase C is involved in neurokinin receptor modulation of N- and L-type Ca2+ channels in DRG neurons of the adult rat. Journal of Neurophysiology 90, 21–31.Google Scholar
Sculptoreanu, A., Scheuer, T., & Catterall, W.A. (1993). Voltage-dependent potentiation of L-type Ca2+ channel due to phosphorylation by cAMP-dependent protein kinase. Nature 364, 240–243.Google Scholar
Selkirk, J.V., Price, G.W., Nahorski, S.R., & Cahlliss, R.A.J. (2001). Cell type-specific differences in the coupling of recombinant mGlu1 alpha receptors to endogenous G protein sub-populations. Neuropharmacology 40, 645–646.Google Scholar
Sen, M. & Gleason, E. (2003). Immuno-localization of mGluR1 and 5 in the synaptic layers of the chicken retina. Society for Neuroscience Abstract 33.Google Scholar
Sosa, R., Hoffpauir, B., Rankin, M.L., Bruch, R.C., & Gleason, E.L. (2002). Metabotrophic glutamate receptor 5 and calcium signaling in retinal amacrine cells. Journal of Neurochemistry 81, 973–983.Google Scholar
Wantanabe, S., Koizumi, A., Matsunaga, S., Stocker, J.W., & Kaneko, A. (2000). GABA-mediated inhibition between amacrine cells in the goldfish retina. Journal of Neurophysiology 84, 1826–1834.Google Scholar
West, A.E., Chen, W.G., Dalva, M.B., Dolmetsch, R.E., Kornhauser, J.M., Shaywitz, A.J., Takasu, M.A., Tao, X., & Greenburg, M.E. (2001). Calcium regulation of neuronal gene expression. Proceedings of the National Academy of Sciences of the U.S.A. 98, 11024–11031.Google Scholar
Wu, Y., Dzhura, I., Colbran, R.J., & Anderson, M.E. (2001). Calmodulin kinase and a calmodulin-binding ‘IQ’ domain facilitate L-type Ca2+ current in rabbit ventricular myocytes by a common mechanism. Journal of Physiology 535.3, 679–687.Google Scholar
Xiao, R.P., Cheng, H., Lederer, W.J., Suzuki, T., & Lakatta, E.G. (1994). Dual regulation of Ca2+/calmodulin-dependent kinase II activity by membrane voltage and by calcium influx. Proceedings of the National Academy of Sciences of the U.S.A. 91, 9659–9663.Google Scholar
Yamamoto, S., Kawamura, K., & James, T.N. (1998). Intracellular distribution of adenylate cyclase in human cardiocytes determined by electron microscopic cytochemistry. Microscopy Research and Technique 40, 479–487.Google Scholar
Yuan, W. & Bers, D.M. (1994). Ca-dependent facilitation of cardiac Ca current is due to Ca-calmodulin-dependent protein kinase. American Journal of Physiology 267, 982–993.Google Scholar