Cannabinoids modulate the P-type high-voltage-activated calcium currents in Purkinje neurons

Journal of Neurophysiology

Volumn 96, Issue 3, 2006, Pages 1267-1277

  Fisyunov, Alexander ^a   Tsintsadze, Vera ^a   Min, Rogier ^b   Burnashev, Nail ^b   Lozovaya, Natalia ^a,b  

^a BOGOMOLETZ INSTITUTE OF PHYSIOLOGY   (Ukraine)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ANANDAMIDE; CALCIUM CHANNEL; CANNABINOID; CANNABINOID 1 RECEPTOR; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CALCIUM CURRENT; CEREBELLUM; CONTROLLED STUDY; IC 50; NONHUMAN; PATCH CLAMP; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PURKINJE CELL; RAT;

ANIMALS; ARACHIDONIC ACIDS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, P-TYPE; CALCIUM CHANNELS, R-TYPE; CANNABINOIDS; CEREBELLUM; KINETICS; PATCH-CLAMP TECHNIQUES; POLYUNSATURATED ALKAMIDES; PURKINJE CELLS; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; TRPV CATION CHANNELS;

EID: 33748579212     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01227.2005     Document Type: Article

References (73)

1. Adams IB, Compton DR, and Martin BR. Assessment of anandamide interaction with the cannabinoid brain receptor: SR 141716A antagonism studies in mice and autoradiographic analysis of receptor binding in rat brain. J Pharmacol Exp Ther 284: 1209-1217, 1998.
2. Alger BE. Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68: 247-286, 2002.
3. Barrett CF, Liu L, and Rittenhouse AR. Arachidonic acid reversibly enhances N-type calcium current at an extracellular site. Am J Physiol Cell Physiol 280: C1306-C1318, 2001.
4. Baskfield CY, Martin BR, and Wiley JL. Differential effects of delta9-tetrahydrocannabinol and methanandamide in CB1 knockout and wild-type mice. J Pharmacol Exp Ther 309: 86-91, 2004.
5. Bean BP. Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature 340: 153-156, 1989.
6. Bisogno T, Sepe N, Melck D, Maurelli S, De Petrocellis L, and Di Marzo V. Biosynthesis, release and degradation of the novel endogenous cannabimimetic metabolite 2-arachidonoylglycerol in mouse neuroblastoma cells. Biochem J 322: 671-677, 1997.
7. Bouaboula M, Poinot-Chazel C, Bourrie B, Canat X, Calandra B, Rinaldi-Carmona M, Le Fur G, and Casellas P. Activation of mitogen-activated protein kinases by stimulation of the central cannabinoid receptor CB1. Biochem J 312: 637-641, 1995.
8. Breivogel CS, Griffin G, Di Marzo V, and Martin BR. Evidence for a new G-protein-coupled cannabinoid receptor in mouse brain. Mol Pharmacol 60: 155-163, 2001.
9. Brown SP, Brenowitz SD, and Regehr WG. Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci 6: 1048-1057, 2003.
10. Brown SP, Safo PK, and Regehr WG. Endocannabinoids inhibit transmission at granule cell to Purkinje cell synapses by modulating three types of presynaptic calcium channels. J Neurosci 24: 5623-5631, 2004.
11. Chemin J, Monteil A, Perez-Reyes E, Nargeot J, and Lory P. Direct inhibition of T-type calcium channels by the endogenous cannabinoid anandamide. EMBO J 20: 7033-7040, 2001.
12. Currie KP and Fox AP. Comparison of N- and P/Q-type voltage-gated calcium channel current inhibition. J Neurosci 17: 4570-4579, 1997.
13. Dar MS. Cerebellar CB(1) receptor mediation of Delta(9)-THC-induced motor incoordination and its potentiation by ethanol and modulation by the cerebellar adenosinergic A(1) receptor in the mouse. Brain Res 864: 186-194, 2000.
14. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, and Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258: 1946-1949, 1992.
15. Di Marzo V, Breivogel CS, Tao Q, Bridgen DT, Razdan RK, Zimmer AM, Zimmer A, and Martin BR. Levels, metabolism, and pharmacological activity of anandamide in CB(1) cannabinoid receptor knockout mice: evidence for non-CB(1), non-CB(2) receptor-mediated actions of anandamide in mouse brain. J Neurochem 75: 2434-2444, 2000.
16. Di Marzo V, De Petrocellis L, Fezza F, Ligresti A, and Bisogno T. Anandamide receptors. Prostaglandins Leukot Essent Fatty Acids 66: 377-391, 2002.
17. Di Marzo V, Fontana A, Cadas H, Schinelli S, Cimino G, Schwartz JC, and Piomelli D. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372: 686-691, 1994.
18. Diana MA, Levenes C, MacKie K, and Marty A. Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J Neurosci 22: 200-208, 2002.
19. Dolphin AC. The G.L. Brown Prize Lecture. Voltage-dependent calcium channels and their modulation by neurotransmitters and G proteins. Exp Physiol 80: 1-36, 1995.
20. Eccles JC, Ito, M, and Szentagothai, J. The Cerebellum as a Neuronal Machine. Berlin: Springer-Verlag, 1967.
21. Elmslie KS, Zhou W, and Jones SW. LHRH and GTP-gamma-S modify calcium current activation in bullfrog sympathetic neurons. Neuron 5: 75-80, 1990.
22. Felder CC, Briley EM, Axelrod J, Simpson JT, MacKie K, and Devane WA. Anandamide, an endogenous cannabimimetic eicosanoid, binds to the cloned human cannabinoid receptor and stimulates receptor-mediated signal transduction. Proc Natl Acad Sci USA 90: 7656-7660, 1993.
23. Godlewski G, Gothert M, and Malinowska B. Cannabinoid receptor-independent inhibition by cannabinoid agonists of the peripheral 5-HT3 receptor-mediated von Bezold-Jarisch reflex. Br J Pharmacol 138: 767-774, 2003.
24. Grassi F and Lux HD. Voltage-dependent GABA-induced modulation of calcium currents in chick sensory neurons. Neurosci Lett 105: 113-119, 1989.
25. Hamill OP, Marty A, Neher E, Sakmann B, and Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluegers 391: 85-100, 1981.
26. Hampson AJ, Bornheim LM, Scanziani M, Yost CS, Gray AT, Hansen BM, Leonoudakis DJ, and Bickler PE. Dual effects of anandamide on NMDA receptor-mediated responses and neurotransmission. J Neurochem 70: 671-676, 1998.
27. Hejazi N, Zhou C, Oz M, Sun H, Ye JH, and Zhang L. Delta9- tetrahydrocannabinol and endogenous cannabinoid anandamide directly potentiate the function of glycine receptors. Mol Pharmacol 69: 991-997, 2006.
28. Hillard CJ, Wilkison DM, Edgemond WS, and Campbell WB. Characterization of the kinetics and distribution of N-arachidonylethanolamine (anandamide) hydrolysis by rat brain. Biochim Biophys Acta 1257: 249-256, 1995.
29. Hillman D, Chen S, Aung TT, Cherksey B, Sugimori M, and Llinas RR. Localization of P-type calcium channels in the central nervous system. Proc Natl Acad Sci USA 88: 7076-7080, 1991.
30. Hoffman AF and Lupica CR. Mechanisms of cannabinoid inhibition of GABA(A) synaptic transmission in the hippocampus. J Neurosci 20: 2470-2479, 2000.
31. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, MacKie K, Martin BR, Mechoulam R, and Pertwee RG. International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54: 161-202, 2002.
32. Huang CC, Lo SW, and Hsu KS. Presynaptic mechanisms underlying cannabinoid inhibition of excitatory synaptic transmission in rat striatal neurons. J Physiol 532: 731-748, 2001.
33. Ito M. The Cerebellum and Neural Control. New York: Raven, 1984.
34. Keyser DO and Alger BE. Arachidonic acid modulates hippocampal calcium current via protein kinase C and oxygen radicals. Neuron 5: 545-553, 1990.
35. Kreitzer AC and Regehr WG. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29: 717-727, 2001.
36. Kreitzer AC and Regehr WG. Retrograde signaling by endocannabinoids. Curr Opin Neurobiol 12: 324-330, 2002.
37. 2+/calmodulin binds to and modulates P/Q-type calcium channels. Nature 399: 155-159, 1999.
38. Liang YC, Huang CC, Hsu KS, and Takahashi T. Cannabinoid-induced presynaptic inhibition at the primary afferent trigeminal synapse of juvenile rat brain stem slices. J Physiol 555: 85-96, 2004.
39. Liu L, Barrett CF, and Rittenhouse AR. Arachidonic acid both inhibits and enhances whole cell calcium currents in rat sympathetic neurons. Am J Physiol Cell Physiol 280: C1293-C1305, 2001.
40. Llinas R and Sugimori M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol 305: 171-195, 1980.
41. Lozovaya N, Yatsenko N, Beketov A, Tsintsadze T, and Burnashev N. Glycine receptors in CNS neurons as a target for nonretrograde action of cannabinoids. J Neurosci 25: 7499-7506, 2005.
42. Maejima T, Ohno-Shosaku T, and Kano M. Endogenous cannabinoid as a retrograde messenger from depolarized postsynaptic neurons to presynaptic terminals. Neurosci Res 40: 205-210, 2001.
43. McDonough SI, Mintz IM, and Bean BP. Alteration of P-type calcium channel gating by the spider toxin omega-Aga-IVA. Biophys J 72: 2117-2128, 1997.
44. Mintz IM, Venema VJ, Swiderek KM, Lee TD, Bean BP, and Adams ME. P-type calcium channels blocked by the spider toxin omega-Aga-IVA. Nature 355: 827-829, 1992.
45. Nam SC and Hockberger PE. Analysis of spontaneous electrical activity in cerebellar Purkinje cells acutely isolated from postnatal rats. J Neurobiol 33: 18-32, 1997.
46. 2+ signals in cerebellar granule neurons in culture. J Neurosci 19: 8765-8777, 1999.
47. Ohno-Shosaku T, Maejima T, and Kano M. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29: 729-738, 2001.
48. Oz M. Receptor-independent actions of cannabinoids on cell membranes: focus on endocannabinoids. Pharmacol Ther 2006.
49. Oz M, Ravindran A, Diaz-Ruiz O, Zhang L, and Morales M. The endogenous cannabinoid anandamide inhibits alpha7 nicotinic acetylcholine receptor-mediated responses in Xenopus oocytes. J Pharmacol Exp Ther 306: 1003-1010, 2003.
50. Panchenko VA, Krishtal OA, Tegtmeier F, and Tsyndrenko AY. R56865 as Ca(2+)-channel blocker in Purkinje neurons of rat: comparison with flunarizine and nimodipine. Neuroscience 54: 587-594, 1993.
51. Patel S and Hillard CJ. Cannabinoid CB(1) receptor agonists produce cerebellar dysfunction in mice. J Pharmacol Exp Ther 297: 629-637, 2001.
52. Pietrobon D. Calcium channels and channelopathies of the central nervous system. Mol Neurobiol 25: 31-50, 2002.
53. + channels. Neuropharmacology 35: 983-991, 1996.
54. Raman IM and Bean BP. Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19: 1663-1674, 1999.
55. Regan LJ. Voltage-dependent calcium currents in Purkinje cells from rat cerebellar vermis. J Neurosci 11: 2259-2269, 1991.
56. Regehr WG and Mintz IM. Participation of multiple calcium channel types in transmission at single climbing fiber to Purkinje cell synapses. Neuron 12: 605-613, 1994.
57. Rueda D, Galve-Roperh I, Haro A, and Guzman M. The CB(1) cannabinoid receptor is coupled to the activation of c-Jun N-terminal kinase. Mol Pharmacol 58: 814-820, 2000.
58. Schmitt H and Meves H. Modulation of neuronal calcium channels by arachidonic acid and related substances. J Membr Biol 145: 233-244, 1995.
59. Stella N, Schweitzer P, and Piomelli D. A second endogenous cannabinoid that modulates long-term potentiation. Nature 388: 773-778, 1997.
60. Sullivan JM. Mechanisms of cannabinoid-receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. J Neurophysiol 82: 1286-1294, 1999.
61. 2+ channels. J Neurosci 19: 890-899, 1999.
62. Tian X, Guo J, Yao F, Yang DP, and Makriyannis A. The conformation, location, and dynamic properties of the endocannabinoid ligand anandamide in a membrane bilayer. J Biol Chem 280: 29788-29795, 2005.
63. 2+ channels in supporting hippocampal synaptic transmission. Science 264: 107-111, 1994.
64. Wilson RI, Kunos G, and Nicoll RA. Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31: 453-462, 2001.
65. Wilson RI and Nicoll RA. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410: 588-592, 2001.
66. Wilson RI and Nicoll RA. Endocannabinoid signaling in the brain. Science 296: 678-682, 2002.
67. Womack M and Khodakhah K. Active contribution of dendrites to the tonic and trimodal patterns of activity in cerebellar Purkinje neurons. J Neurosci 22: 10603-10612, 2002.
68. Womack MD, Chevez C, and Khodakhah K. Calcium-activated potassium channels are selectively coupled to P/Q-type calcium channels in cerebellar Purkinje neurons. J Neurosci 24: 8818-8822, 2004.
69. Yoshida T, Fukaya M, Uchigashima M, Miura E, Kamiya H, Kano M, and Watanabe M. Localization of diacylglycerol lipase-alpha around postsynaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoyl-glycerol, and presynaptic cannabinoid CB1 receptor. J Neurosci 26: 4740-4751, 2006.
70. Yoshida T, Hashimoto K, Zimmer A, Maejima T, Araishi K, and Kano M. The cannabinoid CB1 receptor mediates retrograde signals for depolarization-induced suppression of inhibition in cerebellar Purkinje cells. J Neurosci 22: 1690-1697, 2002.
71. Zhang Y, Cribbs LL, and Satin J. Arachidonic acid modulation of alpha1H, a cloned human T-type calcium channel. AmJ Physiol Heart CircPhysiol 278: H184-H193, 2000.
72. Zygmunt PM, Julius I, Di Marzo I, and Hogestatt ED. Anandamide - the other side of the coin. Trends Pharmacol Sci 21: 43-44, 2000.
73. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, and Hogestatt ED. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400: 452-457, 1999.