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Neurotensin induces calcium oscillations in cultured amacrine cells

Published online by Cambridge University Press:  02 June 2009

Salvador Borges ,
Evanna Gleason ,
Matthew Frerking  and
Martin Wilson
Salvador Borges
Affiliation:
Division of Biological Sciences, Section of Neurobiology, Physiology and Behavior, University of California, Davis
Evanna Gleason
Affiliation:
Division of Biological Sciences, Section of Neurobiology, Physiology and Behavior, University of California, Davis
Matthew Frerking
Affiliation:
Division of Biological Sciences, Section of Neurobiology, Physiology and Behavior, University of California, Davis
Martin Wilson
Affiliation:
Division of Biological Sciences, Section of Neurobiology, Physiology and Behavior, University of California, Davis
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Abstract

The peptide, neurotensin, is found in a class of amacrine cells synapsing chiefly withother amacrine cells in the chicken retina (Li & Lam, 1990; Watt et al., 1991). Toinvestigate the possible effects of neurotensin, we have used Ca2+ imaging to measure cytosolic Ca2+ concentrations in cultured chick amacrine cells. Following a delay of about 2 min, neurotensin (300 nM) induced oscillations in Ca2+ concentration that typically had a period of 2 min and peak values of about 300 nM when averaged over the cell body. The phospholipase C inhibitors U-73, 112 and 4′-bromophenacyl bromide terminated oscillations induced by neurotensin but the protein kinase inhibitors H7 and staurosporine did not inhibit oscillations, increasing their frequency instead. In the absence of external Ca2+, neurotensin induced only a single Ca2+ transient, much briefer than when external Ca2+ was present. Together these results suggest that neurotensin activates phospholipase C, thereby producing IP3 that triggers Ca2+ release from an internal store. Although this released Ca2+ contributes to periodic Ca2+ peaks, the majority of cytosolic Ca2+, even in the first peak, comes from Ca2+ influx across the plasmalemma.

Keywords

RetinaNeurotensinCalciumCalcium oscillationPhospholipase CAmacrine cell
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 2 , March 1996 , pp. 311 - 318
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Adler, E.M., Augustine, G.J., Duffy, S.N. & Charlton, M.P. (1991). Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. Journal of Neuroscience 11, 1496–1507.CrossRefGoogle ScholarPubMed
Amar, S., Kitabgi, P. & Vincent, J.-P. (1986). Activation of phosphatidylinositol turnover by neurotensin receptors in the human colonic adenocarcinoma cell line HT29. FEBS Letters 201, 31–36.CrossRefGoogle ScholarPubMed
Amar, S., Kitabgi, P. & Vincent, J.-P. (1987). Stimulation of inositol phosphate production by neurotensin in neuroblastoma N1E115 cells: Implication of GTP-binding proteins and relationship with the cyclic GMP response. Journal of Neurochemistry 49, 999–1006.CrossRefGoogle ScholarPubMed
Amar, S., Mazella, J., Checler, F., Kitabgi, P. & Vincent, J.-P. (1985). Regulation of cyclic GMP levels by neurotensin in neuroblastoma clone N1E115. Biochemical and Biophysical Research Communications 129, 117–125.CrossRefGoogle ScholarPubMed
Augustine, G.J., Adler, E.M. & Charlton, M.P. (1991). The calcium signal for transmitter secretion from presynaptic nerve terminals. Annals of the New York Academy of Sciences 635, 365–381.CrossRefGoogle ScholarPubMed
Bauer, B., Ehinger, B. & Waga, J. (1985). Neurotransmitter release by certain neuropeptides in the chicken retina. Acta Ophthalmologica 63, 581–587.CrossRefGoogle ScholarPubMed
Berridge, M. (1993). Inositol trisphosphate and calcium signalling. Nature 361, 315–325.CrossRefGoogle ScholarPubMed
Berridge, M. & Irvine, R. (1989). Inositol phosphates and cell signalling. Nature 341, 197–205.CrossRefGoogle ScholarPubMed
Bleasdale, J.E., Bundy, G.L., Bunting, S., Fitzpatrick, F.A., Huff, R.M., Sun, F.F. & Pike, J.E. (1989). Inhibition of phospholipase C-dependent processes by U-73, 122. In Advances in Prostaglandin, Thromboxane and Leukotriene Research, Vol. 19, ed. Samuelsson, P., Wong, P.Y.-K. & Sun, F.F., pp. 590–593. New York: Raven Press.Google Scholar
Bozou, J.-C., Amar, S., Vincent, J.-P. & Kitabgi, P. (1986). Neurotensin-mediated inhibition of cyclic AMP formation in neuroblastoma N1E115 cells: Involvement of the inhibitory GTP-binding component of adenylate cyclase. Molecular Pharmacology 29, 489–496.Google ScholarPubMed
Bozou, J.-C., De Nadai, F., Vincent, J.-P. & Kitabgi, P. (1989 a). Neurotensin, bradykinin and somatostatin inhibit cAMP production in neuroblastoma N1E115 cells via both pertussis toxin sensitive and insensitive mechanisms. Biochemical and Biophysical Research Communications 161, 1144–1150.CrossRefGoogle ScholarPubMed
Bozou, J.-C., Rochet, N., Magnaldo, I., Vincent, J.-P. & Kitabgi, P. (1989 b). Neurotensin stimulates inositol trisphosphate-mediated calcium mobilization but not protein kinase C activation in HT29 cells. Biochemical Journal 264, 871–878.CrossRefGoogle Scholar
Brecha, N. & Karten, H. (1985). Localization of biologically active peptides in the retina. In Retinal Transmitters and Modulators: Models for the Brain, ed. Morgan, W.W., pp. 93–118. Boca Raton, Florida: CRC Press.Google Scholar
Carraway, R. & Ferris, C. (1983). Isolation, biological and chemical characterization, and synthesis of a neurotensin-related hexapeptide from chicken intestine. Journal of Biological Chemistry 258, 2475–2479.CrossRefGoogle ScholarPubMed
Chabry, J., Labbé-Jullié, C., Gully, D., Kitabgi, P., Vincent, J.-P. & Mazella, J. (1994). Stable expression of the cloned rat brain neurotensin receptor into fibroblasts: Binding properties, photoaffinity labelling, transduction mechanisms, and internalization. Journal of Neurochemistry 63, 19–27.CrossRefGoogle Scholar
Chen, Q. & Wong, R. (1995). Suppression of GABAA receptor responses by NMDA application in hippocampal neurones acutely isolated from the adult guinea-pig. Journal of Physiology 482, 353–362.CrossRefGoogle ScholarPubMed
Clapham, D. (1995). Calcium signalling. Cell 80, 259–268.CrossRefGoogle Scholar
Eldred, W., Li, H., Carraway, R. & Dowling, J. (1987). Immunocytochemical localization of LANT-6-like immunoreactivity within neurons in the inner nuclear and ganglion cell layers in vertebrate retinas. Brain Research 424, 361–370.CrossRefGoogle ScholarPubMed
Gilbert, J.A. & Richelson, E. (1984). Neurotensin stimulates formation of cyclic GMP in murine neuroblastoma clone N1E-115. European Journal of Pharmacology 99, 245–246.CrossRefGoogle ScholarPubMed
Gleason, E., Mobbs, P., Nuccitelli, R. & Wilson, M. (1992). Development of functional calcium channels in cultured avian photoreceptors. Visual Neuroscience 8, 315–327.CrossRefGoogle ScholarPubMed
Gleason, E., Borges, S. & Wilson, M. (1993). Synaptic transmission between pairs of retinal amacrine cells in culture. Journal of Neuroscience 13, 2359–2370.CrossRefGoogle ScholarPubMed
Gleason, E., Borges, S. & Wilson, M. (1994). Control of transmitter release from retinal amacrine cells by Ca2+ influx and efflux. Neuron 13, 1109–1117.CrossRefGoogle ScholarPubMed
Goedert, M., Pinnock, R.D., Downes, C.P., Mantyh, P.W. & Emson, P.C. (1984). Neurotensin stimulates inositol phospholipid hydrolysis in rat brain slices. Brain Research 323, 193–197.CrossRefGoogle ScholarPubMed
Grynkiewicz, G., Poenie, M. & Tsien, R.Y. (1985). A new generation of calcium indicators with greatly improved fluorescence properties. Journal of Biological Chemistry 260, 3440–3450.CrossRefGoogle ScholarPubMed
Heidelberger, R. & Matthews, G. (1992). Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. Journal of Physiology 447, 235–256.CrossRefGoogle ScholarPubMed
Heidelberger, R., Heinemann, C., Neher, E. & Matthews, G. (1994). Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513–515.CrossRefGoogle Scholar
Hidaka, H., Inagaki, M., Kawamoto, S. & Sasaki, Y. (1984). Isoquinolinesulfonamides, novel potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. Biochemistry 23, 5036–5041.CrossRefGoogle ScholarPubMed
Huba, R. & Hofmann, H.-D. (1990). Identification of GABAergic amacrine cell-like neurons developing in chick retinal monolayer cultures. Neuroscience Letters 117, 37–42.CrossRefGoogle ScholarPubMed
Huba, R. & Hofmann, H.-D. (1991). Transmitter-gated currents of GABAergic amacrine-like cells in chick retinal cultures. Visual Neuroscience 6, 303–314.CrossRefGoogle ScholarPubMed
Irvine, R. (1991). Inositol tetrakisphosphate as a second messenger: Confusions, contradictions, and a potential resolution. BioEssays 13, 419–427.CrossRefGoogle Scholar
Jennes, L., Stumpf, W.E. & Kalivas, P.W. (1982). Neurotensin: Topographical distribution in rat brain by immunohistochemistry. Journal of Comparative Neurology 210, 211–224.CrossRefGoogle ScholarPubMed
Krishek, B., Xie, X., Blackstone, C., Huganir, R., Moss, S. & Smart, T. (1994). Regulation of GABAA receptor function by protein kinase C phosphorylation. Neuron 12, 1081–1095.CrossRefGoogle ScholarPubMed
Kyger, E. & Franson, R. (1984). Nonspecific inhibition of enzymes by p-bromophenacyl bromide: Inhibition of human platelet phospholipase C and modification of sulphydryl groups. Biochimica et Biophysica Acta 794, 96–103.CrossRefGoogle Scholar
Leidenheimer, N., McQuilkin, S., Hahner, L., Whiting, P. & Harris, R. (1992). Activation of protein kinase C selectively inhibits the γ-aminobutyric acidA receptor: Role of desensitization. Molecular Pharmacology 41, 1116–1123.Google ScholarPubMed
LI, H.-B. & Lam, D.M.-K. (1990). Synaptic organization of neurotensin immunoreactive amacrine cells in the chicken retina. Journal of Comparative Neurology 294, 252–261.CrossRefGoogle ScholarPubMed
Lin, Y.-F., Browning, M., Dudek, E. & Macdonald, R. (1994). Protein kinase C enhances recombinant bovine α1β1γ2L GABAA receptor whole-cell currents expressed in L929 fibroblasts. Neuron 13, 1421–1431.CrossRefGoogle Scholar
Liscovitch, M. & Cantley, L. (1994). Lipid second messengers. Cell 77, 329–334.CrossRefGoogle ScholarPubMed
Lückhoff, A. & Clapham, D. (1992). Inositol 1,3,4,5 tetrakisphosphate activates an endothelial Ca2+- permeable channel. Nature 355, 356–358.CrossRefGoogle Scholar
Mangel, S.C., Baldridge, W.H., Weiler, R. & Dowling, J.E. (1994). Threshold and chromatic sensitivity changes in fish cone horizontal cells following prolonged darkness. Brain Research 659, 55–61.CrossRefGoogle ScholarPubMed
McDonald, B. & Moss, S. (1994). Differential phosphorylation of intracellular domains of γ-aminobutyric acid type A receptor subunits by calcium/calmodulin type 2-dependent protein kinase and cGMP-dependent protein kinase. Journal of Biological Chemistry 269, 18111–18117.CrossRefGoogle ScholarPubMed
Morgan, I.G., Wellard, J.W. & Boelen, M.K. (1994). A role for the enkephalin-immunoreactive amacrine cells of the chicken retina in adaptation to light and dark. Neuroscience Letters 174, 64–66.CrossRefGoogle ScholarPubMed
Nishizuka, Y. (1986). Studies and perspectives of protein kinase C. Science 233, 305–312.CrossRefGoogle ScholarPubMed
Putney, J. (1990). Capacitative calcium entry revisited. Cell Calcium 11, 611–624.CrossRefGoogle ScholarPubMed
Roberts, W.M., Jacobs, R.A. & Hudspeth, A.J. (1990). Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. Journal of Neuroscience 10, 3664–3684.CrossRefGoogle ScholarPubMed
Schulman, H., Hanson, P. & Meyer, T. (1992). Decoding calcium signals by multifunctional CaM kinase. Cell Calcium 13, 401–411.CrossRefGoogle ScholarPubMed
Shi, W.-X. & Bunney, B.S. (1992). Actions of neurotensin: A review of the electrophysiological studies. In The Neurobiology of Neurotensin, Vol. 668, ed. Kitabgi, P. & Nemeroff, C.B., pp. 129–145. New York: Annals of the New York Academy of Sciences.Google Scholar
Slusher, B., Zacco, A., Maslanski, J., Norris, T., McLane, M., Moore, W., Rogers, N. & Ignarro, L. (1994). The cloned neurotensin receptor mediates cyclic GMP formation when coexpressed with nitric oxide synthase cDNA. Molecular Pharmacology 46, 115–121.Google ScholarPubMed
Smith, R.J., Sam, L.M., Justen, J.M., Bundy, G.L., Bala, G.A. & Bleasdale, J.E. (1990). Receptor-coupled signal transduction in human polymorphonuclear neutrophils: Effects of a novel inhibitor of phospholipase C-dependent processes on cell responsiveness. Journal of Pharmacology and Experimental Therapeutics 253, 688–697.Google ScholarPubMed
Stelzer, A. & Shi, H. (1994). Impairment of GABAA receptor function by N-methyl-D-aspartate-mediated calcium influx in isolated CA1 pyramidal cells. Neuroscience 62, 813–828.CrossRefGoogle ScholarPubMed
Stowe, Z.N. & Nemeroff, C.B. (1991). The electrophysiological actions of neurotensin in the central nervous system. Life Sciences 49, 987–1002.CrossRefGoogle ScholarPubMed
Tamaoki, T., Nomoto, H., Takahashi, I., Kato, Y., Morimotot, M. & Tomita, F. (1986). Staurosporine, a potent inhibitor of phospholipid/Ca2+ dependent protein kinase. Biochemical and Biophysical Research Communications 135, 397–402.CrossRefGoogle Scholar
Tanaka, K., Masu, M. & Nakanishi, S. (1990). Structure and functional expression of the cloned rat neurotensin receptor. Neuron 4, 847–854.CrossRefGoogle ScholarPubMed
Tsien, R.Y. & Harootunian, A.T. (1990). Practical design criteria for a dynamic ratio imaging system. Cell Calcium 11, 93–110.CrossRefGoogle ScholarPubMed
Tsien, R.W. & Tsien, R.Y. (1990). Calcium channels, stores, and oscillations. Annual Review of Cell Biology 6, 715–760.CrossRefGoogle ScholarPubMed
Turner, J.T., James-Kracke, M.R. & Camden, J.M. (1990). Regulation of the neurotensin receptor and intracellular calcium mobilization in HT29 cells. Journal of Pharmacology and Experimental Therapeutics 253, 1049–1056.Google ScholarPubMed
Wagner, H.J. & Djamgoz, M.B. (1993). Spinules: A case for retinal synaptic plasticity. Trends in Neurosciences 16, 201–206.CrossRefGoogle ScholarPubMed
Watt, C.B. & Florack, V.J. (1994). A triple-label analysis demonstrating that enkephalin-, somatostatin-, and neurotensin-like immunoreactivities are expressed by a single population of amacrine cells in the chicken retina. Brain Research 634, 310–324.CrossRefGoogle ScholarPubMed
Watt, C.B., Glazebrook, P.A. & Li, H.B. (1991 a). Coexistence of somatostatin and neurotensin in amacrine cells of the chicken retina. Brain Research 546, 166–170.CrossRefGoogle ScholarPubMed
Watt, C.B., Florack, V.J. & Lam, D.M.K. (1991 b). A double-label analysis demonstrating that all enkephalin-immunoreactive amacrine cells in the chicken retina express neurotensin immunoreactivity. Brain Research 566, 337–341.CrossRefGoogle ScholarPubMed
Weiler, R. & Ball, A.K. (1984). Co-localization of neurotensin-like immunoreactivity and 3H-glycine uptake system in sustained amacrine cells of turtle retina. Nature 311, 759–761.CrossRefGoogle ScholarPubMed
Weiss, S., Schmidt, B.H., Sebben, M., Kemp, D.E., Bockaert, J. & Sladeczek, F. (1988). Neurotransmitter-induced inositol phosphate formation in neurons in primary culture. Journal of Neurochemistry 50, 1425–1433.CrossRefGoogle ScholarPubMed
Yamada, M., Yamada, M., Watson, M. & Richelson, E. (1993). Neurotensin stimulates cyclic AMP formation in CHO-rNTR-10 cells expressing the cloned rat neurotensin receptor. European Journal of Pharmacology 244, 99–101.CrossRefGoogle ScholarPubMed
Zalutsky, R.A. & Miller, R.F. (1986). Neurotensin actions in the retina: Mechanisms and variability. Brain Research 371, 360–363.CrossRefGoogle ScholarPubMed