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Endocannabinoid signaling regulates spontaneous transmitter release from embryonic retinal amacrine cells

Published online by Cambridge University Press:  11 April 2007

AJITHKUMAR WARRIER
Affiliation:
Section of Neurobiology, Physiology and Behavior, Division of Biological Sciences, Davis, California
MARTIN WILSON
Affiliation:
Section of Neurobiology, Physiology and Behavior, Division of Biological Sciences, Davis, California

Abstract

GABAergic amacrine cells, cultured from embryonic chick retina, display spontaneous mini frequencies ranging from 0–4.6 Hz as a result of the release of quanta of transmitter from both synapses and autapses. We show here that at least part of this variation originates from differences in the degree to which endocannabinoids, endogenously generated within the culture, are present at terminals presynaptic to individual cells. Though all cells examined scored positive for cannabinoid receptor type I (CB1R), only those showing a low initial rate of spontaneous minis responded to CB1R agonists with an increase in mini frequency, caused by a Gi/o-mediated reduction in [cAMP]. Cells displaying a high initial rate of spontaneous minis, on the other hand, were unaffected by CB1R agonists, but they did show a rate decrease with CB1R antagonists. Such a regulation of spontaneous transmitter release by endocannabinoids might be important in network maintenance in amacrine cells and other inhibitory interneurons.

Type
Research Article
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Alger, B.E. (2002). Retrograde signaling in the regulation of synaptic transmission: Focus on endocannabinoids. Progress In Neurobiology 68, 247286.Google Scholar
Bacci, A., Huguenard, J.R. & Prince, D.A. (2004). Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 431, 312316.Google Scholar
Bernard, C., Milh, M., Morozov, Y.M., Ben-Ari, Y., Freund, T.F. & Gozlan, H. (2005). Altering cannabinoid signaling during development disrupts neuronal activity. Proceedings of the National Academy of Science of the USA 102, 93889393.Google Scholar
Bieda, M.C. & Copenhagen, D.R. (1999). Sodium action potentials are not required for light-evoked release of GABA or glycine from retinal amacrine cells. Journal of Neurophysiology 81, 30923095.Google Scholar
Bouron, A. (2001). Modulation of spontaneous quantal release of neurotransmitters in the hippocampus. Progressive Neurobiology 63, 613635.Google Scholar
Chan, P.K., Chan, S.C. & Yung, W.H. (1998). Presynaptic inhibition of GABAergic inputs to rat substantia nigra pars reticulata neurones by a cannabinoid agonist. Neuroreport 9, 671675.Google Scholar
Diana, M.A., Levenes, C., Mackie, K. & Marty, A. (2002). Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. Journal of Neuroscience 22, 200208.Google Scholar
Diana, M.A. & Marty, A. (2004). Endocannabinoid-mediated short-term synaptic plasticity: depolarization-induced suppression of inhibition (DSI) and depolarization-induced suppression of excitation (DSE). British Journal of Pharmacology 142, 919.Google Scholar
Ding, L., Perkel, D.J. & Farries, MA. (2003). Presynaptic depression of glutamatergic synaptic transmission by D1-like dopamine receptor activation in the avian basal ganglia. Journal of Neuroscience 23, 60866095.Google Scholar
Evans, G.J. & Morgan, A. (2003). Regulation of the exocytotic machinery by cAMP-dependent protein kinase: Implications for presynaptic plasticity. Biochemical Society Transactions 31, 824827.Google Scholar
Fan, S.F. & Yazulla, S. (2005). Reciprocal inhibition of voltage-gated potassium currents (I K(V)) by activation of cannabinoid CB1 and dopamine D1 receptors in ON bipolar cells of goldfish retina. Visual Neuroscience 22, 5563.Google Scholar
Fatt, P. & Katz, B. (1950). Some observations on biological noise. Nature 166, 597598.Google Scholar
Feany, M.B., Lee, S., Edwards, R.H. & Buckley, K.M. (1992). The synaptic vesicle protein SV2 is a novel type of transmembrane transporter. Cell 70, 861867.Google Scholar
Fortin, D.A., Trettel, J. & Levine, E.S. (2004). Brief trains of action potentials enhance pyramidal neuron excitability via endocannabinoid-mediated suppression of inhibition. Journal of Neurophysiology 92, 21052112.Google Scholar
Frech, M.J., Perez-Leon, J., Wassle, H. & Backus, K.H. (2001). Characterization of the spontaneous synaptic activity of amacrine cells in the mouse retina. Journal of Neurophysiology 86, 16321643.Google Scholar
Frerking, M., Borges, S. & Wilson, M. (1995). Variation in GABA mini amplitude is the consequence of variation in transmitter concentration. Neuron 15, 885895.Google Scholar
Frerking, M., Borges, S. & Wilson, M. (1997). Are some minis multiquantal? Journal of Neurophysiology 78, 12931304.Google Scholar
Freund, T.F. (2003). Interneuron Diversity series: Rhythm and mood in perisomatic inhibition. Trends in Neuroscience 26, 489495.Google Scholar
Gleason, E., Borges, S. & Wilson, M. (1993). Synaptic transmission between pairs of retinal amacrine cells in culture. 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
Gleason, E. & Wilson, M. (1989). Development of synapses between chick retinal neurons in dispersed culture. The Journal of Comparative Neurology 287, 213224.Google Scholar
Green, K., Kim, K. & Bowman, K. (1976). Ocular effects of delta(9)-tetrahydrocannabinol. In The Therapeutic Aspects of Marihuana, ed. Stillman, R., pp. 4962. New York: Plenum Press.
Hajos, N. & Freund, T.F. (2002a). Distinct cannabinoid sensitive receptors regulate hippocampal excitation and inhibition. Chemistry and Physics of Lipids 121, 7382.Google Scholar
Hajos, N. & Freund, T.F. (2002b). Pharmacological separation of cannabinoid sensitive receptors on hippocampal excitatory and inhibitory fibers. Neuropharmacology 43, 503510.Google Scholar
Hajos, N., Ledent, C. & Freund, T.F. (2001). Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106, 14.Google Scholar
Hillard, C.J. (2000). Biochemistry and pharmacology of the endocannabinoids arachidonylethanolamide and 2-arachidonylglycerol. Prostaglandins & Other Lipid Mediators 61, 318.Google Scholar
Hillard, C.J., Manna, S., Greenberg, M.J., DiCamelli, R., Ross, R.A., Stevenson, L.A., Murphy, V., Pertwee, R.G. & Campbell, W.B. (1999). Synthesis and characterization of potent and selective agonists of the neuronal cannabinoid receptor (CB1). The Journal of Pharmacology and Experimental Therapeutics 289, 14271433.Google Scholar
Hoffman, A.F. & Lupica, C.R. (2000). Mechanisms of cannabinoid inhibition of GABA(A) synaptic transmission in the hippocampus. Journal of Neuroscience 20, 24702479.Google Scholar
Hoffman, A.F., Macgill, A.M., Smith, D., Oz, M. & Lupica, C.R. (2005). Species and strain differences in the expression of a novel glutamate-modulating cannabinoid receptor in the rodent hippocampus. European Journal of Neuroscience 22, 23872391.Google Scholar
Howlett, A.C., Barth, F., Bonner, T.I., Cabral, G., Casellas, P., Devane, W.A., Felder, C.C., Herkenham, M., Mackie, K., Martin, B.R., Mechoulam, R. & Pertwee, R.G. (2002). International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacology Review 54, 161202.Google Scholar
Howlett, A.C., Breivogel, C.S., Childers, S.R., Deadwyler, S.A., Hampson, R.E. & Porrino, L.J. (2004). Cannabinoid physiology and pharmacology: 30 years of progress. Neuropharmacology 47 Suppl 1, 345358.Google Scholar
Howlett, A.C. & Mukhopadhyay, S. (2000). Cellular signal transduction by anandamide and 2-arachidonoylglycerol. Chemistry and Physics of Lipids 108, 5370.Google Scholar
Hurtado, J., Borges, S. & Wilson, M. (2002). Na(+)-Ca(2+) exchanger controls the gain of the Ca(2+) amplifier in the dendrites of amacrine cells. Journal of Neurophysiology 88, 27652777.Google Scholar
Kaneko, M. & Takahashi, T. (2004). Presynaptic mechanism underlying cAMP-dependent synaptic potentiation. Journal of Neuroscience 24, 52025208.Google 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
Lukasiewicz, P.D. (2005). Synaptic mechanisms that shape visual signaling at the inner retina. Progress in Brain Research 147, 205218.Google Scholar
Marc, R.E. & Liu, W. (2000). Fundamental GABAergic amacrine cell circuitries in the retina: Nested feedback, concatenated inhibition, and axosomatic synapses. Journal of Comparative Neurology 425, 560582.Google Scholar
Marcaggi, P. & Attwell, D. (2005). Endocannabinoid signaling depends on the spatial pattern of synapse activation. Nature Neuroscience 8, 776781.Google Scholar
Marinelli, S., Di Marzo, V., Berretta, N., Matias, I., Maccarrone, M., Bernardi, G. & Mercuri, N.B. (2003). Presynaptic facilitation of glutamatergic synapses to dopaminergic neurons of the rat substantia nigra by endogenous stimulation of vanilloid receptors. Journal of Neuroscience 23, 31363144.Google Scholar
Marinelli, S., Pascucci, T., Bernardi, G., Puglisi-Allegra, S. & Mercuri, N.B. (2005). Activation of TRPV1 in the VTA excites dopaminergic neurons and increases chemical- and noxious-induced dopamine release in the nucleus accumbens. Neuropsychopharmacology 30, 864870.Google Scholar
Marinelli, S., Vaughan, C.W., Christie, M.J. & Connor, M. (2002). Capsaicin activation of glutamatergic synaptic transmission in the rat locus coeruleus in vitro. Journal of Physiology 543, 531540.Google Scholar
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G. & Wu, C. (2004). Interneurons of the neocortical inhibitory system. Nature Reviews Neuroscience 5, 793807.Google Scholar
Marsicano, G., Wotjak, C.T., Azad, S.C., Bisogno, T., Rammes, G., Cascio, M.G., Hermann, H., Tang, J., Hofmann, C., Zieglgansberger, W., Di Marzo, V. & Lutz, B. (2002). The endogenous cannabinoid system controls extinction of aversive memories. Nature 418, 530534.Google Scholar
Melis, M., Pistis, M., Perra, S., Muntoni, A.L., Pillolla, G. & Gessa, G.L. (2004). Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. Journal of Neuroscience 24, 5362.Google Scholar
Pertwee, R.G. (2005). Inverse agonism and neutral antagonism at cannabinoid CB1 receptors. Life Sciences 76, 13071324.Google Scholar
Piomelli, D. (2003). The molecular logic of endocannabinoid signalling. Nature Reviews Neuroscience 4, 873884.Google Scholar
Prange, O. & Murphy, T.H. (1999). Correlation of miniature synaptic activity and evoked release probability in cultures of cortical neurons. Journal of Neuroscience 19, 64276438.Google Scholar
Rinaldi-Carmona, M., Barth, F., Heaulme, M., Shire, D., Calandra, B., Congy, C., Martinez, S., Maruani, J., Neliat, G., Caput, D. & et al. (1994). SR141716A, a potent and selective antagonist of the brain cannabinoid receptor. FEBS Letters 350, 240244.Google Scholar
Rinaldi-Carmona, M., Pialot, F., Congy, C., Redon, E., Barth, F., Bachy, A., Breliere, J.C., Soubrie, P. & Le Fur, G. (1996). Characterization and distribution of binding sites for [3H]-SR 141716A, a selective brain (CB1) cannabinoid receptor antagonist, in rodent brain. Life Sciences 58, 12391247.Google Scholar
Ronesi, J., Gerdeman, G.L. & Lovinger, D.M. (2004). Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport. Journal of Neuroscience 24, 16731679.Google Scholar
Sakaba, T. & Neher, E. (2001). Preferential potentiation of fast-releasing synaptic vesicles by cAMP at the calyx of Held. Proceedings of the National Academy of Sciences of the USA 98, 331336.Google Scholar
Sakaba, T. & Neher, E. (2003). Direct modulation of synaptic vesicle priming by GABA(B) receptor activation at a glutamatergic synapse. Nature 424, 775778.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 USA 96, 1456514570.Google Scholar
Straiker, A. & Sullivan, J.M. (2003). Cannabinoid receptor activation differentially modulates ion channels in photoreceptors of the tiger salamander. Journal of Neurophysiology 89, 26472654.Google Scholar
Sullivan, J.M. (1999). Mechanisms of cannabinoid-receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. Journal of Neurophysiology 82, 12861294.Google Scholar
Takahashi, K.A. & Linden, D.J. (2000). Cannabinoid receptor modulation of synapses received by cerebellar Purkinje cells. Journal of Neurophysiology 83, 11671180.Google Scholar
Turrigiano, G.G. & Nelson, S.B. (2004). Homeostatic plasticity in the developing nervous system. Nature Reviews Neuroscience 5, 97107.Google Scholar
Van Der Stelt, M. & Di Marzo, V. (2004). Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. European Journal of Biochemistry 271, 18271834.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
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
Watanabe, 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, 18261834.Google Scholar
Wiley, J.L. & Martin, B.R. (2002). Cannabinoid pharmacology: Implications for additional cannabinoid receptor subtypes. Chemistry and Physics of Lipids 121, 5763.Google Scholar
Wilson, R.I. & Nicoll, R.A. (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588592.Google Scholar
Yazulla, S. & Studholme, K.M. (2004). Vanilloid receptor like 1 (VRL1) immunoreactivity in mammalian retina: colocalization with somatostatin and purinergic P2X1 receptors. Journal of Comparative Neurology 474, 407418.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. Journal of Comparative Neurology 415, 8090.Google Scholar
Zygmunt, P.M., Petersson, J., Andersson, D.A., Chuang, H., Sorgard, M., Di Marzo, V., Julius, D. & Hogestatt, E.D. (1999). Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400, 452457.Google Scholar