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Science 15 January 1999:
Vol. 283. no. 5400, pp. 401 - 404
DOI: 10.1126/science.283.5400.401
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Reports

Unresponsiveness to Cannabinoids and Reduced Addictive Effects of Opiates in CB1 Receptor Knockout Mice

Catherine Ledent, Olga Valverde, Gregorio Cossu, François Petitet, Jean-François Aubert, Françoise Beslot, Georg A. Böhme, Assunta Imperato, Thierry Pedrazzini, Bernard P. Roques, Gilbert Vassart, Walter Fratta, Marc Parmentier *

The function of the central cannabinoid receptor (CB1) was investigated by invalidating its gene. Mutant mice did not respond to cannabinoid drugs, demonstrating the exclusive role of the CB1 receptor in mediating analgesia, reinforcement, hypothermia, hypolocomotion, and hypotension. The acute effects of opiates were unaffected, but the reinforcing properties of morphine and the severity of the withdrawal syndrome were strongly reduced. These observations suggest that the CB1 receptor is involved in the motivational properties of opiates and in the development of physical dependence and extend the concept of an interconnected role of CB1 and opiate receptors in the brain areas mediating addictive behavior.

C. Ledent and M. Parmentier, IRIBHN, Université libre de Bruxelles, B-1070 Brussels, Belgium. O. Valverde, F. Beslot, B. P. Roques, Département de Pharmacochimie Moléculaire et Structurale, INSERM U266, URA D1500 CNRS, Université René Descartes, 75270 Paris Cedex, France. G. Cossu and W. Fratta, "Bernard B. Brodie" Department of Neuroscience, University of Cagliari, 09124, Cagliari, Italy. F. Petitet, G. A. Böhme, A. Imperato, Rhône-Poulenc-Rorer S.A., Centre de Recherche de Vitry-Alfortville, 94403 Vitry sur Seine, France. J.-F. Aubert and T. Pedrazzini, Division of Hypertension, Lausanne University Medical School, CH-1011 Lausanne, Switzerland. G. Vassart, IRIBHN and Service de Génétique Médicale, Université libre de Bruxelles, B-1070 Brussels, Belgium.
*   To whom correspondence should be addressed. E-mail: mparment{at}ulb.ac.be

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J. Physiol. 558, 647-657
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Differential Effects of {Delta}9-Tetrahydrocannabinol and Methanandamide in CB1 Knockout and Wild-Type Mice.
C. Y. Baskfield, B. R. Martin, and J. L. Wiley (2004)
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M. Begg, F.-M. Mo, L. Offertaler, S. Batkai, P. Pacher, R. K. Razdan, D. M. Lovinger, and G. Kunos (2003)
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B. L. F. Kaplan, C. E. Rockwell, and N. E. Kaminski (2003)
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T. F. FREUND, I. KATONA, and D. PIOMELLI (2003)
Physiol Rev 83, 1017-1066
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J. Neurosci. 23, 4815-4820
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D. L. Cichewicz and S. P. Welch (2003)
J. Pharmacol. Exp. Ther. 305, 812-817
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L. Iversen (2003)
Brain 126, 1252-1270
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Increased Seizure Susceptibility and Proconvulsant Activity of Anandamide in Mice Lacking Fatty Acid Amide Hydrolase.
A. B. Clement, E. G. Hawkins, A. H. Lichtman, and B. F. Cravatt (2003)
J. Neurosci. 23, 3916-3923
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The Role of Several Kinases in Mice Tolerant to Delta 9-Tetrahydrocannabinol.
M. C. Lee, F. L. Smith, D. L. Stevens, and S. P. Welch (2003)
J. Pharmacol. Exp. Ther. 305, 593-599
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Regulation of Extracellular Signal-Regulated Kinase by Cannabinoids in Hippocampus.
P. Derkinderen, E. Valjent, M. Toutant, J.-C. Corvol, H. Enslen, C. Ledent, J. Trzaskos, J. Caboche, and J.-A. Girault (2003)
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Activation of the Cannabinoid Receptor Type 1 Decreases Glutamatergic and GABAergic Synaptic Transmission in the Lateral Amygdala of the Mouse.
S. C. Azad, M. Eder, G. Marsicano, B. Lutz, W. Zieglgansberger, and G. Rammes (2003)
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Selective Ligands and Cellular Effectors of a G Protein-Coupled Endothelial Cannabinoid Receptor.
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Neurobiology of addiction and implications for treatment.
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Anti-obesity effect of SR141716, a CB1 receptor antagonist, in diet-induced obese mice.
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Activation of Muscarinic Acetylcholine Receptors Enhances the Release of Endogenous Cannabinoids in the Hippocampus.
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Increased Severity of Stroke in CB1 Cannabinoid Receptor Knock-Out Mice.
S. Parmentier-Batteur, K. Jin, X. O. Mao, L. Xie, and D. A. Greenberg (2002)
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Inhibition of Improgan Antinociception by the Cannabinoid (CB)1 Antagonist N-(Piperidin-1-yl)-5-(4-chlorophenyl)-1-(2,4-dichlorophenyl)-4-methyl-1H-pyrazole-3-carboxamide (SR141716A): Lack of Obligatory Role for Endocannabinoids Acting at CB1 Receptors.
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J. Pharmacol. Exp. Ther. 303, 314-322
   Abstract »    Full Text »    PDF »
N-Methyl-D-aspartate Antagonists and WIN 55212-2 [4,5-Dihydro-2-methyl-4(4-morpholinylmethyl)-1-(1-naphthalenyl-carbonyl)-6H-pyrrolo[3,2,1-i,j]quinolin-6-one], a Cannabinoid Agonist, Interact to Produce Synergistic Hypothermia.
S. M. Rawls, A. Cowan, R. J. Tallarida, E. B. Geller, and M. W. Adler (2002)
J. Pharmacol. Exp. Ther. 303, 395-402
   Abstract »    Full Text »    PDF »
A missense mutation in human fatty acid amide hydrolase associated with problem drug use.
J. C. Sipe, K. Chiang, A. L. Gerber, E. Beutler, and B. F. Cravatt (2002)
PNAS 99, 8394-8399
   Abstract »    Full Text »    PDF »
Identification of the Endogenous Cannabinoid System through Integrative Pharmacological Approaches.
B. R. Martin (2002)
J. Pharmacol. Exp. Ther. 301, 790-796
   Abstract »    Full Text »    PDF »
CB1 Receptors in the Preoptic Anterior Hypothalamus Regulate WIN 55212-2 [(4,5-Dihydro-2-methyl-4(4-morpholinylmethyl)-1-(1-naphthalenyl-carbonyl)-6H-pyrrolo[3,2,1ij]quinolin-6-one]-Induced Hypothermia.
S. M. Rawls, J. Cabassa, E. B. Geller, and M. W. Adler (2002)
J. Pharmacol. Exp. Ther. 301, 963-968
   Abstract »    Full Text »    PDF »
Delta 9-Tetrahydrocannabinol and Cannabinol Activate Capsaicin-Sensitive Sensory Nerves via a CB1 and CB2 Cannabinoid Receptor-Independent Mechanism.
P. M. Zygmunt, D. A. Andersson, and E. D. Hogestatt (2002)
J. Neurosci. 22, 4720-4727
   Abstract »    Full Text »    PDF »
International Union of Pharmacology. XXVII. Classification of Cannabinoid Receptors.
A. C. Howlett, F. Barth, T. I. Bonner, G. Cabral, P. Casellas, W. A. Devane, C. C. Felder, M. Herkenham, K. Mackie, B. R. Martin, et al. (2002)
Pharmacol. Rev. 54, 161-202
   Abstract »    Full Text »    PDF »
Neural Systems Underlying Opiate Addiction.
T. J. De Vries and T. S. Shippenberg (2002)
J. Neurosci. 22, 3321-3325
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Cannabinoid Addiction: Behavioral Models and Neural Correlates.
R. Maldonado and F. Rodriguez de Fonseca (2002)
J. Neurosci. 22, 3326-3331
   Abstract »    Full Text »    PDF »
Characterization of vasorelaxant responses to anandamide in the rat mesenteric arterial bed.
D. Harris, A. I McCulloch, D. A Kendall, and M. D Randall (2002)
J. Physiol. 539, 893-902
   Abstract »    Full Text »    PDF »
Motivational Effects of Cannabinoids Are Mediated by {micro}-Opioid and kappa -Opioid Receptors.
S. Ghozland, H. W. D. Matthes, F. Simonin, D. Filliol, B. L. Kieffer, and R. Maldonado (2002)
J. Neurosci. 22, 1146-1154
   Abstract »    Full Text »    PDF »
Prevention of Cannabinoid Withdrawal Syndrome by Lithium: Involvement of Oxytocinergic Neuronal Activation.
S.-S. Cui, R. C. Bowen, G.-B. Gu, D. K. Hannesson, P. H. Yu, and X. Zhang (2001)
J. Neurosci. 21, 9867-9876
   Abstract »    Full Text »    PDF »
Absence of Delta -9-Tetrahydrocannabinol Dysphoric Effects in Dynorphin-Deficient Mice.
A. Zimmer, E. Valjent, M. Konig, A. M. Zimmer, P. Robledo, H. Hahn, O. Valverde, and R. Maldonado (2001)
J. Neurosci. 21, 9499-9505
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Distribution of CB1 Cannabinoid Receptors in the Amygdala and their Role in the Control of GABAergic Transmission.
I. Katona, E. A. Rancz, L. Acsady, C. Ledent, K. Mackie, N. Hajos, and T. F. Freund (2001)
J. Neurosci. 21, 9506-9518
   Abstract »    Full Text »    PDF »
Mouse Strain Differences in Opiate Reward Learning Are Explained by Differences in Anxiety, Not Reward or Learning.
C. L. Dockstader and D. van der Kooy (2001)
J. Neurosci. 21, 9077-9081
   Abstract »    Full Text »    PDF »
Opioid and Cannabinoid Modulation of Precipitated Withdrawal in Delta 9-Tetrahydrocannabinol and Morphine-Dependent Mice.
A. H. Lichtman, S. M. Sheikh, H. H. Loh, and B. R. Martin (2001)
J. Pharmacol. Exp. Ther. 298, 1007-1014
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Functional Interaction between Opioid and Cannabinoid Receptors in Drug Self-Administration.
M. Navarro, M. R. A. Carrera, W. Fratta, O. Valverde, G. Cossu, L. Fattore, J. A. Chowen, R. Gomez, I. del Arco, M. A. Villanua, et al. (2001)
J. Neurosci. 21, 5344-5350
   Abstract »    Full Text »    PDF »
G{alpha}olf Levels Are Regulated by Receptor Usage and Control Dopamine and Adenosine Action in the Striatum.
D. Herve, C. Le Moine, J.-C. Corvol, L. Belluscio, C. Ledent, A. A. Fienberg, M. Jaber, J.-M. Studler, and J.-A. Girault (2001)
J. Neurosci. 21, 4390-4399
   Abstract »    Full Text »    PDF »
Blockade of Effects of Smoked Marijuana by the CB1-Selective Cannabinoid Receptor Antagonist SR141716.
M. A. Huestis, D. A. Gorelick, S. J. Heishman, K. L. Preston, R. A. Nelson, E. T. Moolchan, and R. A. Frank (2001)
Arch Gen Psychiatry 58, 322-328
   Abstract »    Full Text »    PDF »
How might cannabinoids influence sexual behavior?.
N. Stella (2001)
PNAS 98, 793-795
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Systemic and portal hemodynamic effects of anandamide.
N. Garcia Jr., Z. Jarai, F. Mirshahi, G. Kunos, and A. J. Sanyal (2001)
Am J Physiol Gastrointest Liver Physiol 280, G14-G20
   Abstract »    Full Text »    PDF »
Cannabinoid Withdrawal Syndrome Is Reduced in Pre-Proenkephalin Knock-Out Mice.
O. Valverde, R. Maldonado, E. Valjent, A. M. Zimmer, and A. Zimmer (2000)
J. Neurosci. 20, 9284-9289
   Abstract »    Full Text »    PDF »
The Cannabinoid System and Cytokine Network.
T. W. Klein, B. Lane, C. A. Newton, and H. Friedman (2000)
Experimental Biology and Medicine 225, 1-8
   Abstract »    Full Text »


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