Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain

European Journal of Neuroscience

Volumn 11, Issue 12, 1999, Pages 4213-4225

  Marsicano, Giovanni ^a   Lutz, Beat ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

Calcium binding proteins; Cholecystokinin; GABAergic system; Hippocampus; In situ hybridization

Indexed keywords

CALBINDIN; CALRETININ; CANNABINOID RECEPTOR; CHOLECYSTOKININ; GLUTAMATE DECARBOXYLASE; MESSENGER RNA; PARVALBUMIN;

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; ENTORHINAL CORTEX; FOREBRAIN; GABAERGIC SYSTEM; HIPPOCAMPUS; IN SITU HYBRIDIZATION; INTERNEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL;

AMYGDALA; ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CANNABINOIDS; CHOLECYSTOKININ; CORPUS STRIATUM; ENTORHINAL CORTEX; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; HYPOTHALAMUS; IN SITU HYBRIDIZATION; INTERNEURONS; ISOENZYMES; MICE; MICE, INBRED STRAINS; NEOCORTEX; NEURONS; OLFACTORY PATHWAYS; PARVALBUMINS; PROSENCEPHALON; RECEPTORS, CANNABINOID; RECEPTORS, DRUG;

EID: 0033452718     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.1999.00847.x     Document Type: Article

References (65)

1. Bachus, S.E., Hyde, T.M., Herman, M.M., Egan, M.F. & Kleinman, J.E. (1997) Abnormal cholecystokinin mRNA levels in entorhinal cortex of schizophrenics. J. Psychiat. Res., 31, 233-256.
2. Beinfeld, M.C. (1996) Cholecystokinin (CCK) release from rat brain slices in vitro is enhanced by agents which elevate intracellular cAMP. Regul. Pept., 67, 75-77.
3. Breivogel, C.S. & Childers, S.R. (1998) The functional neuroanatomy of brain cannabinoid receptors. Neurobiol. Dis., 5, 417-431.
4. Burgunder, J.-M. & Young, W.S. III (1988) The distribution of thalamic projection neurons containing cholecystokinin messenger RNA, using in situ hybridization histochemistry and retrograde labeling. Brain Res., 464, 179-189.
5. 2 dopamine receptors. Behav. Pharmacol., 8, 707-712.
6. Celio, M.R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience, 35, 375-475.
7. Crawley, J.N. (1991) Cholecystokinin-dopamine interactions. Trends Pharmacol. Sci., 12, 232-236.
8. Crawley, J.N. & Corwin, R.L. (1994) Biological actions of cholecystokinin. Peptides, 15, 731-755.
9. Deadwyler, S.A., Hampson, R.E., Bennett, B.A., Edwards, T.A., Mu, J., Pacheco, M.A., Ward, S.J. & Childers, S.R. (1993) Cannabinoids modulate potassium current in cultured hippocampal neurons. Receptors Channels, 1, 121-134.
10. Devane, W.A., Hanus, L., Breuer, A., Pertwee, R.G., Stevenson, L.A., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A. & Mechoulam, R. (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science, 258, 1946-1949.
11. Di Marzo, V. & Deutsch, D.G. (1998) Biochemistry of the endogenous ligands of cannabinoid receptors. Neurobiol. Dis., 5, 386-404.
12. Di Marzo, V., Melck, D., Bisogno, T. & De Petrocellis, L. (1998) Endocannabmoids: endogenous cannabinoid receptor ligands with neuromodulatory action. Trends Neurosci., 21, 521-528.
13. Duggan, A.W. (1992) Neuropharmacology of pain. Curr. Opin. Neurol. Neurosurg., 5, 503-507.
14. Emrich, H.M., Leweke, F.M. & Schneider, U. (1997) Towards a cannabinoid hypothesis of schizophrenia: cognitive impairments due to dysregulation of the endogenous cannabinoid system. Pharmacol. Biochem. Behav., 56, 803-807.
15. Faris, P.L., Komisaruk, B.R., Watkins, L.R. & Mayer, D.J. (1983) Evidence for the neuropeptide cholecystokinin as an antagonist of opiate analgesia. Science, 219, 310-312.
16. Felder, C.C., Joyce, K.E., Briley, E.M., Mansouri, J., Mackie, K., Blond, O., Lai, Y., Ma, A.L. & Mitchell, R. (1995) Comparison of the pharmacology and signal transduction of the human cannabinoid CB1 and CB2 receptors. Mol. Pharmacol., 48, 443-450.
17. Fink, H., Rex, A., Voits, M. & Voigt, J.P. (1998) Major biological actions of CCK - a critical evaluation of research findings. Exp. Brain Res., 123, 77-83.
18. Fredens, K., Stengaard-Pedersen, K. & Larsson, L.I. (1984) Localization of enkephalin and cholecystokinin immunoreactivities in the perforant path terminal fields of the rat hippocampal formation. Brain Res., 304, 255-263.
19. Freund, T.F. & Buszáki, G. (1996) Interneurons of the hippocampus. Hippocampus, 6, 347-470.
20. Gabriel, S.M., Davidson, M., Haroutunian, V., Powchik, P., Bierer, L.M., Purohit, D.P., Perl, D.P. & Davis, K.L. (1996) Neuropeptide deficits in schizophrenia vs. Alzheimer's disease cerebral cortex. Biol. Psychiatry, 39, 82-91.
21. Gifford, A.N. & Ashby, C.R. Jr (1996) Electrically evoked acetylcholine release from hippocampal slices is inhibited by the cannabinoid receptor agonist, WIN 55212-2, and is potentiated by the cannabinoid antagonist, SR 141716A. J. Pharmacol. Exp. Ther., 277, 1431-1436.
22. Giuffrida, A., Parsons, L.H., Kerr, T.M., Rodriguez de Fonseca, F., Navarro, M. & Piomelli, D. (1999) Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nature Neurosci., 2, 358-363.
23. s linkage to the CB1 receptor. J. Neurosci., 17, 5327-5333.
24. Greenwood, R.S., Godar, S.E., Reaves, T.A. & Hayward, J.N. (1981) Cholecystokinin in hippocampal pathways. J. Comp. Neurol., 203, 335-350.
25. Gulyás, A.I. & Freund, T.F. (1996) Pyramidal cell dendrites are the primary targets of calbindin D28k-immunoreactive interneurons in the hippocampus. Hippocampus, 6, 525-534.
26. Gulyás, A.I., Hájos, N. & Freund, T.F. (1996) Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J. Neurosci., 16, 3397-3411.
27. Gulyás, A.I., Tóth, K., Dános, P. & Freund, T.F. (1991) Subpopulations of GABAergic neurons containing parvalbumin, calbindin D28k, and cholecystokinin in the rat hippocampus. J. Comp. Neurol., 312, 371-378.
28. Herkenham, M., Lynn, A.B., Little, M.D., Johnson, M.R., Melvin, L.S., De Costa, B.R. & Rice, K.C. (1990) Cannabinoid receptor localization in brain. Proc. Natl Acad. Sci. USA, 87, 1932-1936.
29. Howlett, A.C. (1995) Pharmacology of cannabinoid receptors. Annu. Rev. Pharmacol. Toxicol., 35, 607-634.
30. Ingram, S.M., Krause, R.G. II., Baldino, F. Jr, Skeen, L.C. & Lewis, M.E. (1989) Neuronal localization of cholecystokinin mRNA in the rat brain by using in situ hybridization histochemistry. J. Comp. Neurol., 287, 260-272.
31. Katona, I., Sperlagh, B., Sik, A., Kafalvi, A., Vizi, E.S., Mackie, K. & Freund, T.F. (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci., 19, 4544-4558.
32. Kellstein, D.E. & Mayer, D.J. (1991) Spinal co-administration of cholecystokinin antagonists with morphine prevents the development of opioid tolerance. Pain, 47, 221-229.
33. Knowles, W.D. (1992) Normal anatomy and neurophysiology of the hippocampal formation. J. Clin. Neurophysiol., 9, 252-263.
34. Ledent, C., Valverde, O., Cossu, G., Petitet, F., Aubert, J.F., Beslot, F., Bohme, G.A., Imperato, A., Pedrazzini, T., Roques, B.P., Vassart, G., Fratta, W. & Parmentier, M. (1999) Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science, 283, 401-404.
35. Lopes da Silva, F.H., Witter, M.P., Boeijinga, P.H. & Lohman, A.H.M. (1990) Anatomic organization and physiology of the limbic cortex. Physiol. Rev., 70, 453-511.
36. Mackie, K. & Hille, B. (1992) Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc. Natl Acad. Sci. USA, 89, 3825-3829.
37. Mackie, K., Lai, Y., Westenbroek, R. & Mitchell, R. (1995) Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J. Neurosci., 15, 6552-6561.
38. Mailleux, P. & Vanderhaeghen, J.J. (1992) Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry. Neuroscience, 48, 655-668.
39. Martin, B.R. & Lichtman, A.H. (1998) Cannabinoid transmission and pain perception. Neurobiol. Dis., 5, 447-461.
40. Matsuda, L.A., Bonner, T.I. & Lolait, S.J. (1993) Localization of cannabinoid receptor mRNA in rat brain. J. Comp. Neurol., 327, 535-550.
41. Matsuda, L.A., Lolait, S.J., Brownstein, M.J., Young, A.C. & Bonner, T.I. (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature, 346, 561-564.
42. Mattes, R.D., Engelman, K., Shaw, L.M. & Elsohly, M.A. (1994) Cannabinoid and appetite stimulation. Pharmacol. Biochem. Behav., 49, 187-195.
43. Miller, L.A., Lai, R. & Munoz, D.G. (1998) Contributions of entorhinal cortex, amygdala and hippocampus to human memory. Neuropsychologia, 36, 1247-1256.
44. Morino, P., Herrera-Marschitz, M., Castel, M.N., Ungerstedt, U., Varro, A., Dockray, G. & Hökfelt, T. (1994) Cholecystokinin in cortico-striatal neurons in the rat: immunohistochemical studies at the light and electron microscopical level. Eur. J. Neurosci., 6, 681-692.
45. Ottersen, O.P. & Storm-Mathiesen, J. (1984) Neurons containing and accumulating transmitter amino acids. In Björklund, A., Hökfelt, T. & Kuhar, M.J. (eds), Handbook of Chemical Neuroanatomy, Vol. 3: Classical Transmitters and Transmitters Receptors in the CNS, P.II. Elsevier Science, Amsterdam, pp. 141-246.
46. Paton, G.S., Pertwee, R.G. & Davies, S.N. (1998) Correlation between cannabinoid mediated effects on paired pulse depression and induction of long-term potentiation in the rat hippocampal slice. Neuropharmacology., 37, 1123-1130.
47. Pettit, D.A., Harrison, M.P., Olson, J.M., Spencer, R.F. & Cabrai, G.A. (1998) Immunohistochemical localization of the neural cannabinoid receptor in rat brain. J. Neurosci. Res., 51, 391-402.
48. Piomelli, D., Beltramo, M., Giuffrida, A. & Stella, N. (1998) Endogenous cannabinoid signaling. Neurobiol. Dis., 5, 462-473.
49. Raiteri, M., Paudice, P. & Vallebuona, F. (1993) Release of cholecystokinin in the central nervous system. Neurochem. Int., 22, 519-527.
50. Reidelberger, R.D. (1994) Cholecystokinin and control of food intake. J. Nutr., 124 (Suppl.), 1327-1333.
51. Rhee, M.-H., Bayewitch, M., Avidor-Reiss, T., Levy, R. & Vogel, Z. (1998) Cannabinoid receptor activation differentially regulates the various adenylyl cyclase isozymes. J. Neurochem., 71, 1525-1534.
52. Roberts, G.W., Woodhams, P.L., Polak, J.M. & Crow, T.J. (1984) Distribution of neuropeptides in the limbic system of the rat: the hippocampus. Neuroscience, 11, 35-77.
53. Schlicker, E., Timm, J., Zentner, J. & Göthert, M. (1997) Cannabinoid CB1 receptor-mediated inhibition of noradrenaline release in the human and guinea-pig hippocampus. Naunyn Schmiedebergs Arch. Pharmacol., 356, 583-589.
54. Schneider, U., Leweke, F.M., Mueller-Vahl, K.R. & Emrich, H.M. (1998) Cannabinoid/anandamide system and schizophrenia: is there evidence for association? Pharmacopsychiatry, 31, 110-113.
55. Senatorov, V.V., Trudeau, V.L. & Hu, B. (1997) Expression of cholecystokinin messenger RNA in reciprocally connected auditory thalamus and cortex in the rat. Neuroscience, 79, 915-921.
56. Shen, M., Piser, T.M., Seybold, V.S. & Thayer, S.A. (1996) Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J. Neurosci., 16, 4322-4334.
57. Soriano, E., Nitsch, R. & Frotscher, M. (1990) Axo-axonic chandelier cells in the rat fascia dentata: Golgi-electron microscopy and immunocytochemical studies. J. Comp. Neurol., 293, 1-25.
58. Steiner, H., Bonner, T., Zimmer, A.M., Kitai, S.T. & Zimmer, A. (1999) Altered gene expression in striatal projection neurons in CB1 cannabinoid receptor knockout mice. Proc. Natl Acad. Sci. USA, 96, 5786-5790.
59. Stella, N., Schweitzer, P. & Piomelli, D. (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature, 388, 773-778.
60. Suzuki, W.A. (1996) The anatomy, physiology and functions of the perirhinal cortex. Curr. Opin. Neurobiol., 6, 179-186.
61. Tanda, G., Pontieri, F.E. & Di Chiara, G. (1997) Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu1 opioid receptor mechanism. Science, 276, 2048-2050.
62. Terranova, J.-P., Michaud, J.-C., Le Fur, G. & Soubrié, P. (1995) Inhibition of long-term potentiation in rat hippocampal slices by anandamide and WIN55212-2: reversal by SR141716A, a selective antagonist of CB1 cannabinoid receptors. Naunyn Schmiedebergs Arch. Pharmacol., 352, 576-579.
63. Tóth, K. & Freund, T.F. (1992) Calbindin D28k-containing nonpyramidal cells in the rat hippocampus: their immunoreactivity for GABA and projection to the medial septum. Neuroscience, 49, 793-805.
64. Tsou, K., Brown, S., Sanudo-Pena, M.C., Mackie, K. & Walker, J.M. (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience, 83, 393-411.
65. Zimmer, A., Zimmer, A.M., Hohmann, A.G., Herkenham, M. & Bonner, T.I. (1999) Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc. Natl Acad. Sci. USA, 96, 5780-5785.