Direct and indirect interactions between cannabinoid CB1 receptor and group II metabotropic glutamate receptor signalling in layer V pyramidal neurons from the rat prefrontal cortex

European Journal of Neuroscience

Volumn 17, Issue 5, 2003, Pages 981-990

  Barbara, Jean Gaël ^a   Auclair, Nathalie ^a   Roisin, Marie Paule ^b   Otani, Satoru ^a   Valjent, Emmanuel ^a   Caboche, Jocelyne ^a   Soubrie, Philippe ^c   Crepel, Francis ^a  

^a Team Compensation in Neurodegenerative and Aging   (France)

^b université Paris Cité   (France)

^c SANOFI   (France)

Author keywords

ERK; Patch clamp; Plasticity; THC

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 (2,3 DICARBOXYCYCLOPROPYL)GLYCINE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ALPHA METHYLSERINE O PHOSPHATE MONOPHENYL ESTER; CANNABINOID 1 RECEPTOR; DIZOCILPINE; GLUTAMIC ACID; GLYCINE DERIVATIVE; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR ANTAGONIST; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SR 141716 A; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPRESSION; DRUG EFFECT; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME LOCALIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOCYTOCHEMISTRY; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PHOSPHORYLATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION; STIMULATION; SYNAPSE;

ANIMALS; ANTICONVULSANTS; CALCIUM CHANNEL BLOCKERS; CYCLOPROPANES; EXCITATORY POSTSYNAPTIC POTENTIALS; GLYCINE; IMMUNOHISTOCHEMISTRY; LONG-TERM POTENTIATION; MITOGEN-ACTIVATED PROTEIN KINASES; MORPHOLINES; NAPHTHALENES; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; PHOSPHORYLATION; PHOSPHOSERINE; PIPERIDINES; PREFRONTAL CORTEX; PYRAMIDAL CELLS; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CANNABINOID; RECEPTORS, DRUG; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION;

EID: 0037353847     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02533.x     Document Type: Article

References (51)

1. Auclair, N., Otani, S., Soubrie, P. & Crepel, F. (2000) Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J. Neurophysiol., 83, 3287-3293.
2. Bienenstock, E.L., Cooper, L.N. & Munro, P.W. (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci., 2, 32-48.
3. Carlson, G., Wang, Y. & Alger, B.E. (2002) Endocannabinoids facilitate the induction of LTP in the hippocampus. Nature Neurosci., 5, 723-724.
4. Childers, S.R. & Deadwyler, S.A. (1996) Role of cyclic AMP in the actions of cannabinoid receptors. Biochem. Pharmacol., 52, 819-827.
5. Cho, K., Aggleton, J.P., Brown, M.W. & Bashir, Z.I. (2001) An experimental test of the role of postsynaptic calcium levels in determining synaptic strength using perirhinal cortex of rat. J. Physiol. (Lond.), 532, 459-466.
6. Daniel, H. & Crepel, F. (2001) Control of Ca(2+) influx by cannabinoid and metabotropic glutamate receptors in rat cerebellar cortex requires K(+) channels. J. Physiol. (Lond.), 537, 793-800.
7. Diana, M.A., Levenes, C., Mackie, K. & Marry, A. (2002) Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J. Neurosci., 22, 200-208.
8. Egertova, M., Giang, D.K., Cravatt, B.F. & Elphick, M.R. (1998) A new perspective on cannabinoid signalling: complementary localization of fatty acid amide hydrolase and the CB1 receptor in rat brain. Proc. R. Soc. Lond. B. Biol. Sci., 265, 2081-2085.
9. Fernandez-Ruiz, J., Berrendero, F., Hernandez, M.L. & Ramos, J.A. (2000) The endogenous cannabinoid system and brain development. Trends Neurosci., 23, 14-20.
10. Gerdeman, G. & Lovinger, D.M. (2001) CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J. Neurophysiol., 85, 468-471.
11. Gerdeman, G.L., Ronesi, J. & Lovinger, D.M. (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nature Neurosci., 5, 446-451.
12. Hajos, N., Katona, I., Naiem, S.S., MacKie, K., Ledent, C., Mody, I. & Freund, T.F. (2000) Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur. J. Neurosci., 12, 3239-3249.
13. Hajos, N., Ledent, C. & Freund, T.F. (2001) Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience, 106, 1-4.
14. Hoffman, A.F. & Lupica, C.R. (2001) Direct actions of cannaboids on synaptic transmission in the nucleus accumbens: a comparison with opioids. J. Neurophysiol., 85, 72-83.
15. Huang, L.Q., Rowan, M.J. & Anwyl, R. (1997) MGluR II inhibition of LTP induction, and mGluR II antagonist inhibition of LTD induction, in the dentate gyms in vitro. Neuroreport, 10, 687-693.
16. Jung, M., Calassi, R., Rinaldi-Carmona, M., Chardenot, P., Le Fur, G., Soubrie, P. & Oury-Donat, F. (1997) Characterization of CB1 receptors on rat neuronal cell cultures: binding and functional studies using the selective receptor antagonist SR 141716A. J. Neurochem., 68, 402-409.
17. Katona, I., Rancz, E.A., Acsady, L., Ledent, C., Mackie, K., Hajos, N. & Freund, T.F. (2001) Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J. Neurosci., 21, 9506-9518.
18. Kemp, M.C., Jane, D.E., Tse, H.W. & Roberts, P.J. (1996) Agonists of cyclic AMP-coupled metabotropic glutamate receptors in adult rat cortical slices. Eur. J. Pharmacol., 309, 79-85.
19. Kreitzer, A.C. & Regehr, W.G. (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron, 29, 717-727.
20. Levenes, C., Daniel, H., Soubrie, P. & Crepel, F. (1998) Cannabinoids decrease excitatory synaptic transmission and impair long-term depression in rat cerebellar Purkinje cells. J. Physiol. (Lond.), 510, 867-879.
21. Leweke, F.M., Giuffrida, A., Wurster, U., Emrich, H.M. & Piomelli, D. (1999) Elevated endogenous cannabinoids in schizophrenia. Neuroreport, 10, 1665-1669.
22. Lin, H.C., Wang, S.J., Luo, M.Z. & Gean, P.W. (2000) Activation of group II metabotropic glutamate receptors induces long-term depression of synaptic transmission in the rat amygdala. J. Neurosci., 20, 9017-9024.
23. Lu, X.R., Ong, W.Y. & Mackie, K. (1999) A light and electron microscopic study of the CB1 cannabinoid receptor in monkey basal forebrain. J. Neurocytol., 28, 1045-1051.
24. Maccarrone, M., Attina, M., Cartoni, A., Bari, M. & Finazzi-Agro, B. (2001) A gas chromatography-mass spectrometry analysis of endogenous cannabinoids in healthy and tumoral human brain and human cells in culture. J. Neurochem., 76, 594-601.
25. Macek, TA., Winder, D.G., Gereau, R.W., Ladd, C.O. & Conn, P.J. (1996) Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. J. Neurophysiol., 76, 3798-3806.
26. 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.
27. Manahan-Vaughan, D. (1997) Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats. J. Neurosci., 17, 3303-3311.
28. Manzoni, O.J. & Bockaert, J. (2001) Cannabinoids inhibit GABAergic synaptic transmission in mice nucleus accumbens. Eur. J. Pharmacol., 412, R3-R5.
29. Marsicano, G. & Lutz, B. (1999) Expression of the cannabinoid receptor CB 1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur. J. Neurosci., 11, 4213-4225.
30. 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, 530-534.
31. Martin, B.R., Mechoulam, R. & Razdan, R.K. (1999) Discovery and characterization of endogenous cannabinoids. Life Sci., 65, 573-595.
32. Misner, D.L. & Sullivan, J.M. (1999) Mechanism of cannabinoid effects on long-term potentiation and depression in hippocampal CA1 neurons. J. Neurosci., 19, 6795-6805.
33. Moldrich, G. & Wenger, T. (2000) Localization of the CB1 cannabinoid receptor in the rat brain. An immunohistochemical study. Peptides, 21, 1735-1742.
34. Mu, J., Zhuang, S.Y., Kirby, M.T., Hampson, R.E. & Deadwyler, S.A. (1999) Cannabinoid receptors differentially modulate potassium A and D currents in hippocampal neurons in culture. J. Pharmacol. Exp. Ther., 291, 893-902.
35. 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.
36. Ong, W.Y. & Mackie, K. (1999) A light and electron microscopic study of the CB1 cannabinoid receptor in primate brain. Neuroscience, 92, 1177-1191.
37. Otani, S., Auclair, N., Desce, J.M., Roisin, M.P. & Crepel, F. (1999) Dopamine receptors and groups I and II mGluRs cooperate for long-term depression induction in rat prefrontal cortex through converging postsynaptic activation of MAP kinases. J. Neurosci., 19, 9788-9802.
38. Otani, S., Daniel, H., Takita, M. & Crepel, F. (2002) Long-term depression induced by post-synaptic group II mGluRs linked to phospholipase C and intracellular calcium rises in rat prefrontal cortex. J. Neurosci., 22, 3434-3444.
39. Palazzo, E., Marabese, I., de Novellis, V., Oliva, P., Rossi, F., Berrino, L., Rossi, F. & Maione, S. (2001) Metabotropic and NMDA glutamate receptors participate in the cannabinoid-induced antinociception. Neuropharmacology, 40, 319-326.
40. Pertwee, R.G. (1997) Pharmacology of cannabinoid CB1 and CB2 receptors. Pharmacol. Ther., 174, 129-180.
41. Petralia, R.S., Wang, Y.X., Niedzielski, A.S. & Wenthold, R.J. (1996) The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience, 71, 949-976.
42. 2+ channels in metabotropic glutamate receptor 2/3-dependent presynaptic long-term depression at nucleus accumbens synapses. J. Neurosci., 22, 4346-4356.
43. Robbe, D., Alonso, G., Duchamp, F., Bockaert, J. & Manzoni, O.J. (2001) Localization and mechanisms of action of cannabinoid receptors at the glutamatergic synapses of the mouse nucleus accumbens. J. Neurosci., 21, 109-116.
44. Robbe, D., Kopf, M., Remaury, A., Bockaert, J. & Manzoni, O.J. (2002a) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc. Natl Acad. Sci. USA, 99, 8384-8388.
45. Sejnowski, T.J. (1977) Storing covariance with nonlinearly interacting neurons. J. Math. Biol., 4, 303-321.
46. Sweatt, J.D. (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem., 76, 1-10.
47. Szabo, B., Wallmichrath, I., Mathonia, P. & Pfreundtner, C. (2000) Cannabinoids inhibit excitatory neurotransmission in the substantia nigra pars reticulata. Neuroscience, 97, 89-97.
48. Valjent, E., Pages, C., Rogard, M., Besson, M.J., Maldonado, R. & Caboche, J. (2001) Delta 9-tetrahydrocannabinol-induced MAPK/ERK and Elk-1 activation in vivo depends on dopaminergic transmission. Eur. J. Neurosci., 14, 342-352.
49. Varma, N., Carlson, G.C., Ledent, C. & Alger, B.E. (2001) Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J. Neurosci., 21, RC188.
50. Vasquez, C. & Lewis, D.L. (1999) The CB1 cannabinoid receptor can sequester G-proteins, making them unavailable to couple to other receptors. J. Neurosci., 19, 9271-9280.
51. Wilson, R.I., Kunos, G. & Nicoll, R.A. (2001) Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron, 31, 453-462.