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Vasoactive intestinal polypeptide modulates GABAA receptor function through activation of cyclic AMP

Published online by Cambridge University Press:  02 June 2009

Margaret L. Veruki  and
Hermes H. Yeh
Margaret L. Veruki
Affiliation:
Graduate Program in Neuroscience, University of Rochester School of Medicine and Dentistry, Rochester
Hermes H. Yeh
Affiliation:
Graduate Program in Neuroscience, University of Rochester School of Medicine and Dentistry, Rochester Bowman Gray School of Medicine, Wake Forest University, Winston-Salem
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Abstract

Vasoactive intestinal polypeptide (VIP) has been shown to potentiate current responses elicited by activation of the GABAA receptor (IGABA) in freshly dissociated ganglion cells of the rat retina. Here we tested the hypothesis that this heteroreceptor cross talk is mediated by an intracellular cascade of events that includes the sequential activation of a stimulatory guanine nucleotide binding (Gs) protein and adenylate cyclase, the subsequent increase in levels of cyclic AMP and, finally, the action of the cyclic AMP-dependent protein kinase (PKA). Intracellular dialysis of freshly dissociated ganglion cells with GTPγs irreversibly potentiated IGABA, while GDPßs either decreased or had no effect on IGABA. Additionally, GDPßs blocked the potentiation of IGABA by VIP. Cholera toxin rendered VIP ineffective in potentiating IGABA, while pertussis toxin had no effect on the VIP-induced potentiation of IGABA. Extracellular application of either forskolin or 8-bromo-cyclic AMP potentiated IGABA, as did the introduction of cyclic AMP directly into the intracellular compartment through the recording pipet. Intracellular application of cyclic AMP-dependent protein kinase (PKA) potentiated IGABA, while a PKA inhibitor blocked the potentiating effect of VIP. These results lead us to conclude that activation of a cyclic AMP-dependent second-messenger system mediates the modulation of GABAA receptor function by VIP in retinal ganglion cells.

Keywords

GABAVIPCyclic AMPGanglion cellsG proteinRat retina
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 5 , September 1994 , pp. 899 - 908
Copyright
Copyright © Cambridge University Press 1994

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References

Adams, S.R., Harootunian, A.T., Buechler, Y.J., Taylor, S.S. & Tsien, R.Y. (1991). Fluorescence ratio imaging of cyclic AMP in single cells. Nature 349, 694–697.CrossRefGoogle ScholarPubMed
Birnbaumer, L. (1990). G proteins in signal transduction. Annual Review of Pharmacological Toxicology 30, 675–705.CrossRefGoogle ScholarPubMed
Brecha, N.C. (1992). Expression of GABAA receptors in the vertebrate retina. Progress in Brain Research 90, 3–27.CrossRefGoogle ScholarPubMed
Browning, M.D., Endo, S., Smith, G., Dudeck, E.M. & Olsen, R.W. (1993). Phosphorylation of the GABAA receptor by cAMP-dependent protein kinase and by protein kinase C: Analysis of the substrate domain. Neurochemical Research 18, 95–100.CrossRefGoogle ScholarPubMed
Casini, G. & Brecha, N. (1991). Co-expression of vasoactive intestinal polypeptide (VIP) and GABA in amacrine cells of rat and rabbit retinas. Investigative Ophthalmology and Visual Science Abstracts 32, 993.Google Scholar
Casini, G. & Brecha, N.C. (1991). Vasoactive intestinal polypeptide-containing cells in the rabbit retina: Immunohistochemical localization and quantitative analysis. Journal of Comparative Neurology 305, 313–327.CrossRefGoogle ScholarPubMed
Casini, G. & Brecha, N.C. (1992). Colocalization of vasoactive intestinal polypeptide and GABA immunoreactivities in a population of wide-field amacrine cells in the rabbit retina. Visual Neuroscience 8, 373–378.CrossRefGoogle Scholar
Chen, Q.X., Stelzer, A., Kay, A.R. & Wong, R.K.S. (1990). GABAA receptor function is regulated by phosphorylation in acutely dissociated guinea-pig hippocampal neurons. Journal of Physiology 420, 207–221.CrossRefGoogle Scholar
Cheun, J.E., Grigorenko, E.V. & Yeh, H.H. (1993). Modulation of GABAA receptor function by cyclic AMP-dependent protein kinase (PKA). Society for Neuroscience Abstracts 19, 1183.Google Scholar
Eckstein, F., Cassel, D., Levkovitz, H., Lowe, M. & Selinger, Z. (1979). Guanosine 5′-O-(2-thiodiphosphate). Journal of Biological Chemistry 254, 9829–9834.CrossRefGoogle ScholarPubMed
Fishman, P.H. (1980). Mechanisms of action of cholera toxin: Studies on the lag period. Journal of Membrane Biology 54, 61–72.CrossRefGoogle ScholarPubMed
Fukuda, M., Yeh, H.H. & Puro, D.G. (1987). A vasoactive intestinal polypeptide system in retinal cell cultures: Immunocytochemistry and physiology. Brain Research 414, 177–181.CrossRefGoogle ScholarPubMed
Gilman, A.G. (1987). G proteins: Transducers of receptor-generated signals. Annual Review of Biochemistry 56, 615–649.CrossRefGoogle ScholarPubMed
Gozes, I. & Brenneman, D.E. (1989). VIP: Molecular biology and neurobiological function. Molecular Neurobiology 3, 201–236.CrossRefGoogle ScholarPubMed
Greferath, U., Müller, F., Wässle, H., Shivers, B. & Seeburg, P. (1993). Localization of GABAA receptors in the rat retina. Visual Neuroscience 10, 551–561.CrossRefGoogle ScholarPubMed
Grigorenko, E.V. & Yeh, H.H. (1994). Expression profiling of GABAA receptor ß-subunits in the rat retina. Visual Neuroscience 11, 379–387.CrossRefGoogle Scholar
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
Hinton, D.R., Blanks, J.C., Fong, H.K.W., Casey, P.J., Hil-Debrandt, E. & Simon, M.I. (1990). Novel localization of a G protein, Gz–a, in neurons of brain and retina. Journal of Neuroscience 10, 2763–2770.CrossRefGoogle Scholar
Huganir, R.L. & Greengard, P. (1990). Regulation of neurotrans-mitter receptor desensitization by protein phosphorylation. Neuron 5, 555–567.CrossRefGoogle Scholar
Ishihara, T., Shigemoto, R., Mori, K., Takahashi, K. & Nagato, S. (1992). Functional expression and tissue distribution of a novel receptor for vasoactive intestinal polypeptide. Neuron 8, 811–819.CrossRefGoogle ScholarPubMed
Jensen, R.J. (1993). Effects of vasoactive intestinal polypeptide on ganglion cells in the rabbit retina. Visual Neuroscience 10, 181–189.CrossRefGoogle ScholarPubMed
Johnson, D.A., Leathers, V.L., Martinez, A.-M., Walsh, D.A. & Fletcher, W.H. (1993). Fluorescence resonance energy transfer within a heterochromatic cAMP-dependent protein kinase holoenzyme under equilibrium conditions: New insights into conformational changes that result in cAMP-dependent activation. Biochemistry 3202, 6402–6410.CrossRefGoogle Scholar
Karten, H.J., Keyser, K.T. & Brecha, N.C. (1990). Biochemical and morphological heterogeneity of retinal ganglion cells. In Vision and the Brain: The Organization of the Central Visual System. Research Publications: Association for Research in Nervous and Mental Disease, Vol. 67, ed. Cohen, B. & Bodis-Wollner, I., pp. 19–32. New York: Raven Press.Google Scholar
Kassis, S., Hagmann, J., Fishman, P.H., Chang, P.P. & Moss, J. (1982). Mechanism of action of cholera toxin on intact cells. Journal of Biological Chemistry 257(20), 12148–12152.CrossRefGoogle ScholarPubMed
Kirkness, E.F., Bovenkerk, C.F., Ueda, T. & Turner, A.J. (1989). Phosphorylation of Γ-aminobutyrate (GABA)/benzodiazepine receptors by cyclic AMP-dependent protein kinase. Biochemical Journal 259, 613–616.CrossRefGoogle ScholarPubMed
Knighton, D.R., Zheng, J., Ten Eyck, L.F., Xuong, N.-H., Taylor, S.S. & Sowadski, J.M. (1991). Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253, 414–420.CrossRefGoogle Scholar
Kondo, H., Kuramoto, H., Wainer, B.H. & Yanaihara, N. (1985). Discrete distribution of cholinergic and vasoactive intestinal poly-peptidergic amacrine cells in the rat retina. Neuroscience Letters 54, 213–218.CrossRefGoogle ScholarPubMed
Lad, R.P., Simons, C., Gierschik, P., Milligan, G., Woodard, C., Griffo, M., Goldsmith, P., Ornberg, R., Gerfen, C.R. & Spiegel, A. (1987). Differential distribution of signal-transducing G-proteins in retina. Brain Research 423, 237–246.CrossRefGoogle ScholarPubMed
Lasater, E.M., Watling, K.J. & Dowling, J.E. (1983). Vasoactive intestinal peptide alters membrane potential and cyclic nucleotide levels in retinal horizontal cells. Science 221, 1070–1072.CrossRefGoogle ScholarPubMed
Lolait, S.J., O'Carroll, A.-M., Kusano, K., Muller, J.-M., Brown-Stein, M.J. & Mahan, L.C. (1989). Cloning and expression of a novel rat GABAA receptor. FEBS Letters 246, 145–148.CrossRefGoogle ScholarPubMed
Longshore, M.A. & Makman, M.H. (1981). Stimulation of retinal adenylate cyclase by vasoactive intestinal peptide (VIP). European Journal of Pharmacology 70, 237–240.CrossRefGoogle ScholarPubMed
Loren, I., Tornqvist, K. & Alumets, J. (1980). VIP (vasoactive intestinal polypeptide)-immunoreactive neurons in the retina of the rat. Cell Tissue Research 210, 167–170.CrossRefGoogle ScholarPubMed
McKnight, G.S. (1991). Cyclic AMP second messenger systems. Current Opinion in Cell Biology 3, 213–217.CrossRefGoogle ScholarPubMed
Moss, J. & Vaughan, M. (1988). ADP-ribosylation of guanyl nucleotide-binding regulatory proteins by bacterial toxins. Advances in Enzymology and Related Areas of Molecular Biology 61, 303–379.Google ScholarPubMed
Moss, S.J., Smart, T.G., Blackstone, C.D. & Huganir, R.L. (1992). Functional modulation of GABAA receptors by cAMP-dependent protein phosphorylation. Science 257, 661–665.CrossRefGoogle ScholarPubMed
Pachter, J.A. & Lam, D.M.-K. (1986). Interactions between vasoactive intestinal peptide and dopamine in the rabbit retina: Stimulation of a common adenylate cyclase. Journal of Neurochemistry 46, 257–263.CrossRefGoogle ScholarPubMed
Porter, N.M., Twyman, R.E., Uhler, M.D. & Macdonald, R.L. (1990). Cyclic AMP-dependent protein kinase decreases GABAA receptor current in mouse spinal neurons. Neuron 5, 789–796.CrossRefGoogle ScholarPubMed
Pritchett, D.B., Sontheimer, H., Gorman, C.M., Kettenmann, H., Seeburg, P.H. & Schofield, P.R. (1988). Transient expression shows ligand gating and allosteric potentiation of GABAA receptor sub-units. Science 242, 1306–1308.CrossRefGoogle Scholar
Robberecht, P., De Neff, P., Lammens, M., Deschodt-Lanckman, M. & Christophe, J. (1978). Specific binding of vasoactive intestinal polypeptide to brain membranes from the guinea pig. European Journal of Biochemistry 90, 147–154.CrossRefGoogle ScholarPubMed
Ross, E.M. (1989). Signal sorting and amplification through G protein-coupled receptors. Neuron 3, 141–152.CrossRefGoogle ScholarPubMed
Sagar, S.M. (1987). Vasoactive intestinal polypeptide (VIP) immuno-histochemistry in the rabbit retina. Brain Research 426, 157–163.CrossRefGoogle Scholar
Schofield, P.R., Darlison, M.G., Fujita, N., Burt, D.R., Rodriguez, F.A., Rhee, L.M., Ramachamdran, J., Reale, V., Glencorse, T.A., Seeburg, P.H. & Barnard, E.A. (1987). Sequence and functional expression of the GABAA receptor shows a ligand-gated receptor super-family. Nature 328, 221–227.CrossRefGoogle Scholar
Schorderet, M., Sovilla, J.-Y. & Magistretti, P.J. (1981). VIP- and glucagon-induced formation of cyclic AMP in intact retinae in vitro. European Journal of Pharmacology 71, 131–133.CrossRefGoogle ScholarPubMed
Song, Y. & Huang, L.-Y.M. (1990). Modulation of glycine receptor chloride channels by cAMP-dependent protein kinase in spinal tri-geminal neurons. Nature 348, 242–245.CrossRefGoogle Scholar
Terashima, T., Katada, T., Oinuma, M., Inoue, Y. & Ui, M. (1987 a). Immunohistochemical localization of guanine nucleotide-binding protein in rat retina. Brain Research 410, 97–100.CrossRefGoogle ScholarPubMed
Terashima, T., Katada, T., Okada, E., Ui, M. & Inoue, Y. (1987 b). Light microscopy of GTP-binding protein (G0) immunoreactivity within the retina of different vertebrates. Brain Research 436, 384–389.CrossRefGoogle Scholar
Terubayashi, H., Tsuto, T., Fukui, K., Obata, H.L., Okamura, H., Fujisawa, H., Itoi, M., Yanaihara, C., Yanaihara, N. & Ibata, Y. (1983). VIP-like immunoreactive amacrine cells in the retina of the rat. Experimental Eye Research 36, 743–749.CrossRefGoogle ScholarPubMed
Tornqvist, K., Uddman, R. & Ehinger, B. (1982). Somatostatin and VIP neurons in the retina of different species. Histochemistry 76, 137–152.CrossRefGoogle ScholarPubMed
Vardi, N., Matesic, D.F., Manning, D.R., Leibman, P.A. & Sterling, P. (1993). Identification of a G-protein in depolarizing rod bipolar cells. Visual Neuroscience 10, 473–478.CrossRefGoogle ScholarPubMed
Veruki, M.L. & Yeh, H.H. (1992). Vasoactive intestinal polypeptide modulates GABAA receptor function in bipolar cells and ganglion cells of the rat retina. Journal of Neurophysiology 67, 791–797.CrossRefGoogle ScholarPubMed
Wang, Y.-Y. & Aghajanian, G.K. (1989). Excitation of locus coeruleus neurons by vasoactive intestinal peptide: Evidence for a G-protein-mediated inward current. Brain Research 500, 107–118.CrossRefGoogle ScholarPubMed
Wang, Y.-Y. & Aghajanian, G.K. (1990). Excitation of locus coeruleus neurons by vasoactive intestinal peptide: Role of cAMP and protein kinase A. Journal of Neuroscience 10, 3335–3343.CrossRefGoogle ScholarPubMed
Watling, K.J. & Dowling, J.E. (1983). Effects of vasoactive intestinal peptide and other peptides on cyclic AMP accumulation in intact pieces and isolated horizontal cells of the teleost retina. Journal of Neurochemistry 41, 1205–1213.CrossRefGoogle ScholarPubMed
Ymer, S., Schofield, P.R., Draghun, A., Werner, P., Kohler, M. & Seeburg, P.H. (1989). GABAA receptor beta subunit heterogeneity: Functional expression of cloned cDNAs. EMBO Journal 8, 1665–1670.CrossRefGoogle ScholarPubMed
Zalutsky, R.A. & Miller, R.F. (1990 a). The physiology of somato-statin in the rabbit retina. Journal of Neuroscience 10, 383–393.CrossRefGoogle Scholar
Zalutsky, R.A. & Miller, R.F. (1990 b). The physiology of substance P in the rabbit retina. Journal of Neuroscience 10, 394–402.CrossRefGoogle ScholarPubMed
Zhang, D. (1990). Neuropeptide systems in the developing rat retina. Ph.D. Dissertation, University of Rochester.Google Scholar