Retroinhibition of presynaptic Ca2+ currents by endocannabinoids released via postsynaptic mGluR activation at a calyx synapse

Journal of Neuroscience

Volumn 24, Issue 26, 2004, Pages 5955-5965

  Kushmerick, Christopher ^a,d   Price, Gareth D ^a   Taschenberger, Holger ^b   Puente, Nagore ^c   Renden, Robert ^a   Wadiche, Jacques I ^a   Duvoisin, Robert M ^a   Grandes, Pedro ^c   Von Gersdorff, Henrique ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b M P Inst for Biophysical Chem   (Germany)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^d FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Calyx of Held; Cannabinoids; CB1 receptor; Exocytosis; Group I mGluRs; MNTB; Presynaptic Ca channels; Retrograde signaling

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 3,5 DIHYDROXYPHENYLGLYCINE; [2,3 DIHYDRO 5 METHYL 3 (4 MORPHOLINYLMETHYL)PYRROLO[1,2,3 DE] 1,4 BENZOXAZIN 6 YL] 1 NAPHTHALENYLMETHANONE; AMPA RECEPTOR; CALCIUM CHANNEL; CALCIUM ION; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR AGONIST; CANNABINOID RECEPTOR ANTAGONIST; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GLUTAMIC ACID; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR AGONIST; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC RECEPTOR; UNCLASSIFIED DRUG; 2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 2 AMINO 5 PHOSPHONOVALERIC ACID; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 2,3 DIOXO 6 NITRO 7 SULFAMOYLBENZO(F)QUINOXALINE; 2,3-DIOXO-6-NITRO-7-SULFAMOYLBENZO(F)QUINOXALINE; 3,5-DIHYDROXYPHENYLGLYCINE; AMINO ACID; CYCLOPROPYL 4 PHOSPHONOPHENYLGLYCINE; CYCLOPROPYL-4-PHOSPHONOPHENYLGLYCINE; DRUG DERIVATIVE; ENDOCANNABINOID; GLYCINE; METABOTROPIC GLUTAMATE RECEPTOR TYPE 1; MORPHOLINE DERIVATIVE; NAPHTHALENE DERIVATIVE; PICROTOXIN; PIPERIDINE DERIVATIVE; PRESYNAPTIC RECEPTOR; PYRAZOLE DERIVATIVE; QUINOXALINE DERIVATIVE; RESORCINOL DERIVATIVE; SCOPOLAMINE; XANTHENE DERIVATIVE;

ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; AUDITORY BRAIN STEM; AUDITORY NERVOUS SYSTEM; BRAIN NUCLEUS; BRAIN STEM; CALCIUM CURRENT; CALYX OF HELD; EXCITATORY POSTSYNAPTIC POTENTIAL; EXOCYTOSIS; GENE EXPRESSION; MICROSCOPY; NERVE ENDING; NEUROTRANSMITTER RELEASE; NEWBORN; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RECEPTOR UPREGULATION; RETROGRADE SIGNALING; SIGNAL TRANSDUCTION; SYNAPSE; TRAPEZOID BODY MEDIAL NUCLEUS; VOLTAGE CLAMP; WAVEFORM; ACTION POTENTIAL; ANIMAL; CALCIUM SIGNALING; DRUG EFFECT; EVOKED BRAIN STEM AUDITORY RESPONSE; ION TRANSPORT; PATCH CLAMP; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPTIC TRANSMISSION;

2-AMINO-5-PHOSPHONOVALERATE; ACTION POTENTIALS; AMINO ACIDS; ANIMALS; BRAIN STEM; CALCIUM SIGNALING; ENDOCANNABINOIDS; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; GLYCINE; ION TRANSPORT; MORPHOLINES; NAPHTHALENES; NERVE ENDINGS; PATCH-CLAMP TECHNIQUES; PICROTOXIN; PIPERIDINES; PYRAZOLES; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, PRESYNAPTIC; RESORCINOLS; SCOPOLAMINE; SYNAPTIC TRANSMISSION; XANTHENES;

EID: 3042751071     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0768-04.2004     Document Type: Article

References (67)

1. Alger BE (2002) Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68:247-286.
2. Anwyl R (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Rev 29:83-120.
3. Banks MI, Smith PH (1992) Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J Neurosci 12:2819-2837.
4. Barnes-Davies M, Forsythe ID (1995) Pre- and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices. J Physiol (Lond) 488:387-406.
5. Borst JG, Sakmann B (1998) Calcium current during a single action potential in a large presynaptic terminal of the rat brainstem. J Physiol (Lond) 506:143-157.
6. Borst JG, Sakmann B (1999) Depletion of calcium in the synaptic cleft of a calyx-type synapse in the rat brainstem. J Physiol (Lond) 521:123-133.
7. Brenowitz SD, Regehr WG (2003) Calcium dependence of retrograde inhibition by endocannabinoids at synapses onto Purkinje cells. J Neurosci 23:6373-6384.
8. Cartmell J, Schoepp DD (2000) Regulation of neurotransmitter release by metabotropic glutamate receptors. J Neurochem 75:889-907.
9. Caulfield MP, Brown DA (1992) Cannabinoid receptor agonists inhibit Ca current in NG108-15 neuroblastoma cells via a pertussis toxin-sensitive mechanism. Br J Pharmacol 106:231-232.
10. Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461-472.
11. Conn PJ, Pin JP (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37:205-237.
12. Dale LB, Babwah AV, Ferguson SS (2002) Mechanisms of metabotropic glutamate receptor desensitization: role in the patterning of effector enzyme activation. Neurochem Int 41:319-326.
13. D'Ambra TE, Estep KG, Bell MR, Eissenstat MA, Josef KA, Ward SJ, Haycock DA, Baizman ER, Casiano FM, Beglin NC, Chippari SM, Grego JD, Kullnig RK, Daley GT (1992) Conformationally restrained analogues of pravadoline: nanomolar potent, enantioselective, (aminoalkyl)indole agonists of the cannabinoid receptor. J Med Chem 35:124-135.
14. Diana MA, Marty A (2003) Characterization of depolarization-induced suppression of inhibition using paired interneuron-Purkinje cell recordings. J Neurosci 23:5906-5918.
15. Diana MA, Levenes C, Mackie K, Marty A (2002) Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J Neurosci 22:200-208.
16. Doherty J, Dingledine R (2003) Functional interactions between cannabinoid and metabotropic glutamate receptors in the central nervous system. Curr Opin Pharmacol 3:46-53.
17. Elezgarai I, Benitez R, Mateos JM, Lazaro E, Osorio A, Azkue JJ, Bilbao A, Lingenhoehl K, van der Putten H, Hampson DR, Kuhn R, Knöpfel T, Grandes P (1999) Developmental expression of group III metabotropic glutamate receptor mGluR4a in the medial nucleus of the trapezoid body of the rat. J Comp Neurol 411:431-440.
18. Elezgarai I, Bilbao A, Mateos JM, Azkue JJ, Benitez R, Osorio A, Diez J, Puente N, Donate-Oliver F, Grandes P (2001) Group II metabotropic glutamate receptors are differentially expressed in the medial nucleus of the trapezoid body in the developing and adult rat. Neuroscience 104:487-498.
19. Elezgarai I, Puente N, Diez J, Azkue J, Hermida D, Bilbao A, Donate-Oliver F, von Gersdorff H, Grandes P (2003) Group I metabotropic glutamate receptors are localized in developing calyces of Held. Soc Neurosci Abstr 29:800.6.
20. Ene FA, Kullmann PH, Gillespie DC, Kandler K (2003) Glutamatergic calcium responses in the developing lateral superior olive: receptor types and their specific activation by synaptic activity patterns. J Neurophysiol 90:2581-2591.
21. Faas GC, Adwanikar H, Gereau RW, Saggau P (2002) Modulation of presynaptic calcium transients by metabotropic glutamate receptor activation: a differential role in acute depression of synaptic transmission and long-term depression. J Neurosci 22:6885-6890.
22. Forsythe ID (1994) Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. J Physiol (Lond) 479:381-387.
23. Forsythe ID, Tsujimoto T, Barnes-Davies M, Cuttle MF, Takahashi T (1998) Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron 20:797-807.
24. 2+ pathway by phosphorylation of the receptor-G protein-coupling domain. Proc Natl Acad Sci USA 97:6185-6190.
25. Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017-1066.
26. Gee CE, Benquet P, Gerber U (2003) Group I metabotropic glutamate receptors activate a calcium-sensitive transient receptor potential-like conductance in rat hippocampus. J Physiol (Lond) 546:655-664.
27. 2+. Eur J Neurosci 12:987-993.
28. Guatteo E, Mercuri NB, Bernardi G, Knöpfel T (1999) Group I metabotropic glutamate receptors mediate an inward current in rat substantia nigra dopamine neurons that is independent from calcium mobilization. J Neurophysiol 82:1974-1981.
29. Hajos N, Katona I, Naiem SS, MacKie K, Ledent C, Mody I, Freund TF (2000) Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12:3239-3249.
30. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54:161-202.
31. Ikeda SR (1996) Voltage-dependent modulation of N-type calcium channels by G-protein beta gamma subunits. Nature 380:255-258.
32. Ito I, Kohda A, Tanabe S, Hirose E, Hayashi M, Mitsunaga S, Sugiyama H (1992) 3,5-Dihydroxyphenyl-glycine: a potent agonist of metabotropic glutamate receptors. NeuroReport 11:1013-1016.
33. Iwasaki S, Takahashi T (1998) Developmental changes in calcium channel types mediating synaptic transmission in rat auditory brainstem. J Physiol (Lond) 509:419-423.
34. Kim J, Alger BE (2001) Random response fluctuations lead to spurious paired-pulse facilitation. J Neurosci 21:9608-9618.
35. Kingston AE, Ornstein PL, Wright RA, Johnson BG, Mayne NG, Burnett JP, Belagaje R, Wu S, Schoepp (1998) LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology 37:1-12.
36. Kopp-Scheinpflug C, Lippe WR, Dorrscheidt GJ, Rubsamen R (2003) Themedial nucleus of the trapezoid body in the gerbil is more than a relay: comparison of pre- and postsynaptic activity. J Assoc Res Otolaryngol 4:1-23.
37. Kotak VC,Sanes DH (1995) Synaptically evoked prolonged depolarizations in the developing auditory system. J Neurophysiol 74:1611-1620.
38. Kreitzer AC, Regehr WG (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727.
39. Kreitzer AC, Regehr WG (2002) Retrograde signaling by endocannabinoids. Curr Opin Neurobiol 12:324-330.
40. Leão RM, von Gersdorff H (2002) Noradrenaline increases high-frequency firing at the calyx of Held synapse during development by inhibiting glutamate release. J Neurophysiol 87:2297-2306.
41. Losonczy A, Biro AA, Nusser Z (2004) Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons. Proc Natl Acad Sci USA 101:1362-1367.
42. Mackie K, Hille B (1992) Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc Natl Acad Sci USA 89:3825-3829.
43. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M (2001) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463-475.
44. Mateos JM, Benitez R, Elezgarai I, Azkue JJ, Lazaro E, Osorio A, Bilbao A, Donate F, Sarria R, Conquet F, Ferraguti F, Kuhn R, Knopfel T, Grandes P (2000) Immunolocalization of the mGluR1b splice variant of the metabotropic glutamate receptor 1 at parallel fiber-Purkinje cell synapses in the rat cerebellar cortex. J Neurochem 74:1301-1309.
45. Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327:535-550.
46. Mizoguchi A, Kim S, Ueda T, Kikuchi A, Yorifuji H, Hirokawa N, Takai Y (1990) Localization and subcellular distribution of smg p25A, a Ras p21-like GTP-binding protein, in rat brain. J Biol Chem 265:11872-11879.
47. Morishita W, Kirov SA, Alger BE (1998) Evidence for metabotropic glutamate receptor activation in the induction of depolarization-induced suppression of inhibition in hippocampal CA1. J Neurosci 18:4870-4882.
48. i at the mouth of a calcium channel. J Neurosci 17:6961-6973.
49. Oertel D (1999) The role of timing in the brain stem auditory nuclei of vertebrates. Annu Rev Physiol 61:497-519.
50. Ohno-Shosaku T, Shosaku J, Tsubokawa H, Kano M (2002) Cooperative endocannabinoid production by neuronal depolarization and group I metabotropic glutamate receptor activation. Eur J Neurosci 15:953-961.
51. Robbe D, Alonso G, Duchamp F, Bockaert J, Manzoni OJ (2001) Localization and mechanisms of action of cannabinoid receptors at the glutamatergic synapses of the mouse nucleus accumbens. J Neurosci 21:109-116.
52. Rodriguez-Moreno A, Sistiaga A, Lerma J, Sanchez-Prieto J (1998) Switch from facilitation to inhibition of excitatory synaptic transmission by group I mGluR desensitization. Neuron 21:1477-1486.
53. Schneggenburger R, Meyer AC, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23:399-409.
54. Schoepp DD, Goldsworthy J, Johnson BG, Salhoff CR, Baker SR (1994) 3,5-Dihydroxyphenylglycine is a highly selective agonist for phosphoinositide-linked metabotropic glutamate receptors in the rat hippocampus. J Neurochem 63:769-772.
55. Sullivan JM (1999) Mechanisms of cannabinoid-receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. J Neurophysiol 82:1286-1294.
56. Sun JY, Wu XS, Wu LG (2002) Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature 417:555-559.
57. Taschenberger H, von Gersdorff H (2000) Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20:9162-9173.
58. Taschenberger H, Leão RM, Rowland KC, Spirou GA, von Gersdorff H (2002) Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 36:1127-1143.
59. Trussell LO (2002) Modulation of transmitter release at giant synapses of the auditory system. Curr Opin Neurobiol 12:400-404.
60. Twitchell W, Brown S, Mackie K (1997) Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J Neurophysiol 78:43-50.
61. Varma N, Carlson GC, Ledent C, Alger BE (2001) Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J Neurosci 21:RC188(1-5).
62. von Gersdorff H, Schneggenburger R, Weis S, Neher E (1997) Presynaptic depression at a calyx synapse: the small contribution of metabotropic glutamate receptors. J Neurosci 17:8137-8146.
63. Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science 296:678-682.
64. Wilson RI, Kunos G, Nicoll RA (2001) Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31:453-462.
65. Wu LG, Westenbroek RE, Borst JG, Catterall WA, Sakmann B (1999) Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses. J Neurosci 19:726-736.
66. Zirpel L, Rubel EW (1996) Eighth nerve activity regulates intracellular calcium concentration of avian cochlear nucleus neurons via a metabotropic glutamate receptor. J Neurophysiol 76:4127-4139.
67. Zirpel L, Janowiak MA, Taylor DA, Parks TN (2000) Developmental changes in metabotropic glutamate receptor-mediated calcium homeostasis. J Comp Neurol 421:95-106.