Blockade of cannabinoid receptors by SR141716 selectively increases Fos expression in rat mesocorticolimbic areas via reduced dopamine D2 function

Neuroscience

Volumn 91, Issue 2, 1999, Pages 607-620

  Alonso, R ^a   Voutsinos, B ^a   Fournier, M ^a   Labie, C ^b   Steinberg, R ^a   Souilhac, J ^a   Le Fur, G ^a   Soubrie P ^a  

^a SANOFI   (France)

^b 195 Route d'Espagne ^*  (France)

Author keywords

C fos; Neurotensin; Quinpirole; SCH23390; SR141716

Indexed keywords

8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; CANNABINOID RECEPTOR; DOPAMINE; DOPAMINE 2 RECEPTOR; NEUROTENSIN; PROTEIN C FOS; QUINPIROLE; RIMONABANT;

ANIMAL EXPERIMENT; ARTICLE; CAUDATE NUCLEUS; CELLULAR DISTRIBUTION; DOPAMINE RELEASE; DOPAMINERGIC ACTIVITY; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; DRUG RECEPTOR BINDING; IMMUNOREACTIVITY; INTRAPERITONEAL DRUG ADMINISTRATION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUTAMEN; PYRAMIDAL NERVE CELL; RAT; RECEPTOR BLOCKING; TISSUE DISTRIBUTION;

ANIMALS; BRAIN; CANNABINOIDS; DOPAMINE; GENE EXPRESSION REGULATION; GENES, FOS; LIMBIC SYSTEM; MALE; MICRODIALYSIS; NEUROTENSIN; PIPERIDINES; PREFRONTAL CORTEX; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CANNABINOID; RECEPTORS, DOPAMINE D2; RECEPTORS, DRUG;

EID: 0032914945     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(98)00675-7     Document Type: Article

References (70)

1. Arnone M., Maruani J., Chaperon F., Thiebot M.H., Poncelet M., Soubrie P., Le Fur G. Selective inhibition of sucrose and ethanol intake by SR141716, an antagonist of central cannabinoid (CB1) receptors. Psychopharmacologia. 132:1997;104-106.
2. Augood S.J., Westmore K., Emson P.C. Phenotypic characterization of neurotensin messenger RNA-expressing cells in the neuroleptic-treated rat striatum: a detailed cellular co-expression study. Neuroscience. 76:1997;763-774.
3. Boegman R.J., Vincent S.R. Involvement of adenosine and glutamate receptors in the induction of c-fos in the striatum by haloperidol. Synapse. 22:1996;70-77.
4. Carelli R., West M. Representation of the body by single neurons in the dorsolateral striatum of the awake, unrestrained rat. J. comp. Neurol. 309:1991;231-249.
5. Carter D.A., Fibiger H.C. Ascending projections of presumed dopamine-containing neurons in the ventral tegmentum of the rat by horseradish peroxidase. Neuroscience. 2:1977;569-576.
6. Castle D.J., Ames F.R. Cannabis and the brain. Aust. N. Z. J. Psychiat. 30:1996;179-183.
7. Chaperon F., Soubrie P., Puech A.J., Thiebot M.H. Involvement of central cannabinoid (CB1) receptors in the establishment of place conditioning in rats. Psychopharmacologia. 135:1998;324-332.
8. Compton D.R., Aceto M.D., Lowe J., Martin B.R. In vivo characterization of a specific cannabinoid receptor antagonist (SR141716A): inhibition of delta 9-tetrahydrocannabinol-induced responses and apparent agonist activity. J. Pharmac. exp. Ther. 277:1996;586-594.
9. Dahmen N., Fischer V., Hodl P., Rujescu D., Reuss S., Bartoszyk G.D., Hiemke C. Induction of c-fos gene expression by the selective sigma receptor ligand EMD 57445 in rat brain. Eur. Neuropsychopharmac. 6:1996;237-243.
10. Deutch A.Y., Duman R.S. The effects of antipsychotic drugs on Fos protein expression in the prefrontal cortex: cellular localization and pharmacological characterization. Neuroscience. 70:1996;377-389.
11. Deutch A.Y., Lee M.C., Iadarola M.J. Regionally specific effects of atypical antipsychotic drugs on striatal Fos expression: the nucleus accumbens shell as a locus of antipsychotic action. Molec. cell. Neurosci. 3:1992;332-341.
12. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., Gibson D., Mandelbaum A., Etinger A., Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science. 258:1992;1946-1949.
13. Divac I., Markowitsch H.J., Pritzel M. Behavioral and anatomical consequences of small intrastriatal injections of kainic acid in the rat. Brain Res. 151:1978;523-532.
14. Emrich H.M., Leweke F.M., Schneider U. Towards a cannabinoid hypothesis of schizophrenia: cognitive impairments due to dysregulation of the endogenous cannabinoid system. Pharmac. Biochem. Behav. 56:1997;803-807.
15. French E.D. Delta9-tetrahydrocannabinol excites rat VTA dopamine neurons through activation of cannabinoid CB1 but not opioid receptors. Neurosci. Lett. 226:1997;159-162.
16. French E.D., Dillon K., Wu X. Cannabinoids excite dopamine neurons in the ventral tegmentum and substantia nigra. NeuroReport. 8:1997;649-652.
17. Fu L., Beckstead R.M. Cortical stimulation induces Fos expression in striatal neurons. Neuroscience. 46:1992;329-334.
18. Gerfen C.R., Herkenham M., Thiebault J. The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J. Neurosci. 7:1987;3915-3934.
19. Gessa G., Melis M., Muntoni A., Diana M. Cannabinoids activate mesolimbic dopamine neurons by an action on cannabinoid CB1 receptors. Eur. J. Pharmac. 341:1998;39-44.
20. Gessa G.L., Mascia M.S., Casu M.A., Carta G. Inhibition of hippocampal acetylcholine release by cannabinoids: reversal by SR 141716A. Eur. J. Pharmac. 327:1997;R1-R2.
21. Graybiel A.M., Moratalla R., Robertson H.A. Amphetamine and cocaine induce drug-specific activation of the c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Neurobiology. 87:1990;6912-6916.
22. Gueudet C., Santucci V., Rinaldi-Carmona M., Soubrie P., Le Fur G. The CB1 cannabinoid receptor antagonist SR 141716A affects A9 dopamine neuronal activity in the rat. NeuroReport. 6:1995;1421-1425.
23. Guo N., Klitenick M.A., Tham C.S., Fibiger H.C. Receptor mechanisms mediating clozapine-induced c-fos expression in the forebrain. Neuroscience. 65:1995;747-756.
24. Hall W., Solowij N. Long-term cannabis use and mental health. Br. J. Psychiat. 171:1997;107-108.
25. Hendry S.H.C., Jones E.G., Emson P.C., Lawson D.E.M., Heizmann C.W., Streit P. Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Expl Brain Res. 76:1989;467-472.
26. Herkenham M., Lynn A.B., Johnson M.R., Melvin L.S., De Costa B.R., Rice K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 11:1991;563-583.
27. Horn A.S., Cuello A.C., Miller R.J. Dopamine in the mesolimbic system of the rat brain: endogenous levels and the effects of drugs on the uptake mechanism and stimulation of adenylate cyclase activity. J. Neurochem. 22:1974;265-270.
28. Howlett A.C. Pharmacology of cannabinoid receptors. A. Rev. Pharmac. Toxic. 35:1995;607-634.
29. Kilts C.D., Anderson C.M., Bissette G., Ely T.D., Nemeroff C.B. Differential effects of antipsychotic drugs on the neurotensin concentration of discrete rat brain nuclei. Biochem. Pharmac. 37:1988;1547-1554.
30. Labie C., Saubusse P., Keane P.E., Le Fur G., Soubrie P. Effects of the sigma receptor ligand SR31742A on neurotensin biosynthesis in rat basal ganglia. Synapse. 19:1995;241-246.
31. Le Moine C., Bloch B. Expression of the D3 dopamine receptor in peptidergic neurons of the nucleus accumbens: comparison with the D1 and D2 dopamine receptors. Neuroscience. 73:1996;131-143.
32. Le Moine C., Normand E., Guitteny A.F., Fouque B., Teoule R., Bloch B. Dopamine receptor gene expression by enkephalin neurons in rat forebrain. Proc. natn. Acad. Sci. U.S.A. 87:1990;230-234.
33. Levant B., Bissette G., Widerlöv E., Nemeroff C.B. Alterations in regional brain neurotensin concentrations produced by atypical antipsychotic drugs. Regul. Pept. 32:1991;193-201.
34. MacGibbon G.A., Lawlor P.A., Bravo R., Dragunow M. Clozapine and haloperidol produce a differential pattern of immediate early gene expression in rat caudate-putamen, nucleus accumbens, lateral septum and islands of Calleja. Molec. Brain Res. 23:1994;21-32.
35. Mailleux P., Vanderhaeghen J.-J. Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding radioautography and in situ hybridization histochemistry study. Neuroscience. 48:1992;655-668.
36. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature. 346:1990;561-564.
37. Mechoulam R., Ben-Shabat S., Hanus L., Ligumsky M., Kaminski N.E., Schatz A.R., Gopher A., Almog S., Martin B.R., Compton D.R. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmac. 50:1995;83-90.
38. Merchant K.M., Bush L.G., Gibb J.W., Hanson G.R. Dopamine D2 receptors exert tonic regulation over discrete neurotensin systems of the rat brain. Brain Res. 500:1989;21-29.
39. Merchant K.M., Dorsa D.M. Differential induction of neurotensin and c-fos gene expression by typical versus atypical antipsychotics. Proc. natn. Acad. Sci. U.S.A. 90:1993;3447-3451.
40. Miller J.C. Induction of c-fos mRNA expression in rat striatum by neuroleptic drugs. J. Neurochem. 54:1990;1453-1455.
41. Miyamoto A., Yamamoto T., Ohno M., Watanabe S., Tanaka H., Morimoto S., Shoyama Y. Roles of dopamine D1 receptors in delta 9-tetrahydrocannabinol-induced expression of Fos protein in the rat brain. Brain Res. 710:1996;234-240.
42. Moratalla R., Xu M., Tonegawa S., Graybiel A.M. Cellular responses to psychomotor stimulant and neuroleptic drugs are abnormal in mice lacking the D1 dopamine receptor. Proc. natn. Acad. Sci. U.S.A. 93:1996;14,928-14,933.
43. Morgan J.I., Curran T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. A. Rev. Neurosci. 14:1991;421-451.
44. Munro S., Thomas K.L., Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature. 365:1993;61-65.
45. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic, New York.
46. Perio A., Rinaldi-Carmona M., Maruani J., Barth F., Le Fur G., Soubrie P. Central mediation of the cannabinoid cue: activity of a selective CB1 antagonist, SR141716A. Behav. Pharmac. 7:1996;65-71.
47. Pinna A., Wardas J., Cristalli G., Morelli M. Adenosine A2A receptor agonists increase Fos-like immunoreactivity in mesolimbic areas. Brain Res. 759:1997;41-49.
48. Richardson J.D., Aanonsen L., Hargreaves K.M. Hypoactivity of the spinal cannabinoid system results in NMDA-dependent hyperalgesia. J. Neurosci. 18:1998;451-457.
49. Rinaldi-Carmona M., Barth F., Heaulme M., Alonso R., Shire D., Congy C., Soubrie P., Breliere J.C., Le Fur G. Biochemical and pharmacological characterisation of SR141716A, the first potent and selective brain cannabinoid receptor antagonist. Life Sci. 56:1995;1941-1947.
50. Rinaldi-Carmona M., Barth F., Heaulme M., Shire D., Calandra B., Congy C., Martinez S., Maruani J., Neliat G., Caput D., Ferrara P., Soubrie P., Le Fur G. SR141716A, a potent and selective antagonist of the brain cannabinoid receptor. Fedn Eur. biochem. Socs Lett. 350:1994;240-244.
51. Robertson G.S., Fibiger H.C. Neuroleptics increase c-fos expression on the forebrain: contrasting effects of haloperidol and clozapine. Neuroscience. 46:1992;315-328.
52. Robertson G.S., Jian M. D1 and D2 dopamine receptors differentially increase Fos-like immunoreactivity in accumbal projections to the ventral pallidum and midbrain. Neuroscience. 64:1995;1019-1034.
53. Robertson G.S., Matsumura H., Fibiger H.C. Induction patterns of Fos-like immunoreactivity in the forebrain as predictors of atypical antipsychotic activity. J. Pharmac. exp. Ther. 271:1994;1058-1066.
54. Robertson G.S., Vincent S.R., Fibiger H.C. D1 and D2 dopamine receptors differentially regulate c-fos expression in striatonigral and striatopallidal neurons. Neuroscience. 49:1992;285-296.
55. Rodriguez de Fonseca F., Carrera M.R.A., Navarro M., Koob G.F., Weiss F. Activation of corticotropin-releasing factor in the limbic system during cannabinoid withdrawal. Science. 276:1997;2050-2054.
56. Santucci V., Gueudet C., Steinberg R., Le F.G., Soubrie P. Involvement of cortical neurotensin in the regulation of rat meso-cortico-limbic dopamine neurons: evidence from changes in the number of spontaneously active A10 cells after neurotensin receptor blockade. Synapse. 26:1997;370-380.
57. Santucci V., Storme J.J., Soubrie P., Le Fur G. Arousal-enhancing properties of the CB1 cannabinoid receptor antagonist SR141716A in rats as assessed by electroencephalographic spectral and sleep-waking cycle analysis. Life Sci. 58:1996;PL103-PL110.
58. Sebens J.B., Koch T., Ter Horst G.J., Korf J. Differential Fos-protein induction in rat forebrain regions after acute and long-term haloperidol and clozapine treatment. Eur. J. Pharmac. 273:1995;175-182.
59. Semba J., Sakai M., Miyoshi R., Mataga N., Fukamauchi F., Kito S. Differential expression of c-fos mRNA in rat prefrontal cortex, striatum, N. accumbens and lateral septum after typical and atypical antipsychotics: an in situ hybridization study. Neurochem. Int. 29:1996;435-442.
60. Senger B., Brog J.S., Zahm D.S. Subsets of neurotensin-immunoreactive neurons in the rat striatal complex following antagonism of the dopamine D2 receptor: an immunohistochemical double-labeling study using antibodies against Fos. Neuroscience. 57:1993;649-660.
61. Sokoloff P., Schwartz J.C. Novel dopamine receptors half a decade later. Trends pharmac. Sci. 16:1995;270-275.
62. Steinberg R., Marco N., Voutsinos B., Bensaid N., Rodier D., Souilhac J., Alonso R., Oury-Donat F., Le Fur G., Soubrie P. Expression and presence of septal neurokinin-2 receptors controlling hippocampal acetylcholine release during sensory stimulation in rat. Eur. J. Neurosci. 10:1998;2337-2345.
63. Stella N., Schweitzer P., Piomelli D. A second endogenous cannabinoid that modulates long-term potentiation. Nature. 388:1997;773-778.
64. Tanda G., Pontieri F.E., Di Chiara G. Cannabinoid and heroin activation of mesolimbic dopamine transmission by a common mu1 opioid receptor mechanism. Science. 276:1997;2048-2050.
65. Terranova J.P., Storme J.J., Lafon N., Perio A., Rinaldi-Carmona M., Le Fu G., Soubrie P. Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR141716. Psychopharmacologia. 126:1996;165-172.
66. Thierry A.M., Le Douarin C., Ferron J., Glowinski J. Variation of the ability of neuroleptics to block the inhibitory influence of dopaminergic neurons on the activity of cells in the rat prefrontal cortex. Brain Res. Bull. 16:1986;155-160.
67. Tsou K., Brown S., Sanudo-Pena M.C., Mackie K., Walker J.M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience. 83:1998;393-411.
68. Wan W., Ennulat D.J., Cohen B.M. Acute administration of typical and atypical antipsychotic drugs induces distinctive patterns of Fos expression in the rat forebrain. Brain Res. 688:1995;95-104.
69. West M., Michael A. J., Knowles S. E., Chapin J. K. and Woodward D. J. (1998) In Basal Ganglia and Behavior: Sensory Aspects of Motor Functioning (eds Schneider S. and Lidsky T.), p. 27.35. Hans Huber Hogrefe.
70. Zahm D.S., Brog J.S. On the significance of subterritories in the "accumbens" part of the rat ventral striatum. Neuroscience. 50:1992;751-767.