Dopamine activation of endogenous cannabinoid signaling in dorsal striatum

We measured endogenous cannabinoid release in dorsal striatum of freely moving rats by microdialysis and gas chromatography/mass spectrometry. Neural activity stimulated the release of anandamide, but not of other endogenous cannabinoids such as 2-arachidonylglycerol. Moreover, anandamide release was increased eightfold over baseline after local administration of the D2-like (D2, D3, D4) dopamine receptor agonist quinpirole, a response that was prevented by the D2-like receptor antagonist raclopride. Administration of the D1-like (D1, D5) receptor agonist SKF38393 had no such effect. These results suggest that functional interactions between endocannabinoid and dopaminergic systems may contribute to striatal signaling. In agreement with this hypothesis, pretreatment with the cannabinoid antagonist SR141716A enhanced the stimulation of motor behavior elicited by systemic administration of quinpirole. The endocannabinoid system therefore may act as an inhibitory feedback mechanism countering dopamine-induced facilitation of motor activity.

[1]  G. Pryor,et al.  Interactions of Δ 9-tetrahydrocannabinol with d-Amphetamine, cocaine, and nicotine in rats , 1978, Pharmacology Biochemistry and Behavior.

[2]  A. Gough,et al.  Catalepsy induced by intrastriatal injections of Δ9-THC and 11-OH-Δ9-THC in the rat , 1978, Neuropharmacology.

[3]  D. Proud,et al.  Identification and Partial Characterization , 1986 .

[4]  D. Eilam,et al.  Biphasic effect of D-2 agonist quinpirole on locomotion and movements. , 1989, European journal of pharmacology.

[5]  M. Herkenham,et al.  Cannabinoid receptor localization in brain. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[6]  S. Cooper,et al.  The Neurobiology of Stereotyped Behaviour , 1991 .

[7]  T. Bonner,et al.  Structure of a cannabinoid receptor and functional expression of the cloned cDNA , 1990, Nature.

[8]  M. Herkenham,et al.  Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  D. Gibson,et al.  Isolation and structure of a brain constituent that binds to the cannabinoid receptor. , 1992, Science.

[10]  C. Gerfen.  The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. , 1992, Annual review of neuroscience.

[11]  C. Gerfen.  The neostriatal mosaic: multiple levels of compartmental organization , 1992, Trends in Neurosciences.

[12]  M. Cebeira,et al.  Motor disturbances induced by an acute dose of Δ 9-tetrahydrocannabinol: Possible involvement of nigrostriatal dopaminergic alterations , 1993, Pharmacology Biochemistry and Behavior.

[13]  R. Mechoulam,et al.  Pharmacological activity of the cannabinoid receptor agonist, anandamide, a brain constituent. , 1993, European journal of pharmacology.

[14]  P. Yellowlees,et al.  Effective treatment of Tourette's syndrome with marijuana , 1993, Journal of psychopharmacology.

[15]  P. Soubrié,et al.  SR141716A, a potent and selective antagonist of the brain cannabinoid receptor , 1994, FEBS letters.

[16]  L. Parsons,et al.  Quantitative approaches to in vivo brain microdialysis. , 1994, Critical reviews in neurobiology.

[17]  J. Schwartz,et al.  Formation and inactivation of endogenous cannabinoid anandamide in central neurons , 1994, Nature.

[18]  A M Graybiel,et al.  The basal ganglia and adaptive motor control. , 1994, Science.

[19]  W. Campbell,et al.  Characterization of the kinetics and distribution of N-arachidonylethanolamine (anandamide) hydrolysis by rat brain. , 1995, Biochimica et biophysica acta.

[20]  A. Buriani,et al.  Mast cells express a peripheral cannabinoid receptor with differential sensitivity to anandamide and palmitoylethanolamide. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[21]  P. Soubrié,et al.  Intrastriatal injection of cannabinoid receptor agonists induced turning behavior in mice , 1995, Pharmacology Biochemistry and Behavior.

[22]  Z. Vogel,et al.  Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. , 1995, Biochemical pharmacology.

[23]  A. Yamashita,et al.  2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. , 1995, Biochemical and biophysical research communications.

[24]  F. Bloom,et al.  Psychopharmacology: The Fourth Generation of Progress , 1995 .

[25]  D. Piomelli,et al.  Anandamide Amidohydrolase Activity in Rat Brain Microsomes , 1995, The Journal of Biological Chemistry.

[26]  N. Ueda,et al.  Partial Purification and Characterization of the Porcine Brain Enzyme Hydrolyzing and Synthesizing Anandamide (*) , 1995, The Journal of Biological Chemistry.

[27]  L. Venance,et al.  Biosynthesis of an Endogenous Cannabinoid Precursor in Neurons and its Control by Calcium and cAMP , 1996, The Journal of Neuroscience.

[28]  D. R. Compton,et al.  Evaluation of binding in a transfected cell line expressing a peripheral cannabinoid receptor (CB2): identification of cannabinoid receptor subtype selective ligands. , 1996, The Journal of pharmacology and experimental therapeutics.

[29]  Stephen P. Mayfield,et al.  Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides , 1996, Nature.

[30]  R. Coppola,et al.  Tourette Syndrome: Prediction of Phenotypic Variation in Monozygotic Twins by Caudate Nucleus D2 Receptor Binding , 1996, Science.

[31]  D. Surmeier,et al.  Coordinated Expression of Dopamine Receptors in Neostriatal Medium Spiny Neurons , 1996, The Journal of Neuroscience.

[32]  L. Parsons,et al.  Neurochemical Evidence that Postsynaptic Nucleus Accumbens D3 Receptor Stimulation Enhances Cocaine Reinforcement , 1996, Journal of neurochemistry.

[33]  J. Lowe,et al.  In vivo characterization of a specific cannabinoid receptor antagonist (SR141716A): inhibition of delta 9-tetrahydrocannabinol-induced responses and apparent agonist activity. , 1996, The Journal of pharmacology and experimental therapeutics.

[34]  V. Natarajan,et al.  The N-acylation-phosphodiesterase pathway and cell signalling. , 1996, Chemistry and physics of lipids.

[35]  D. Selley,et al.  Differences in G-protein activation by μ-and δ-opioid, and cannabinoid, receptors in rat striatum , 1996 .

[36]  S. L. Patrick,et al.  Effects of intranigral cannabinoids on rotational behavior in rats: interactions with the dopaminergic system , 1996, Neuroscience Letters.

[37]  A. Yamashita,et al.  Transacylase-mediated and phosphodiesterase-mediated synthesis of N-arachidonoylethanolamine, an endogenous cannabinoid-receptor ligand, in rat brain microsomes. Comparison with synthesis from free arachidonic acid and ethanolamine. , 1996, European journal of biochemistry.

[38]  A. Yamashita,et al.  Enzymatic synthesis of anandamide, an endogenous cannabinoid receptor ligand, through N-acylphosphatidylethanolamine pathway in testis: involvement of Ca(2+)-dependent transacylase and phosphodiesterase activities. , 1996, Biochemical and biophysical research communications.

[39]  T. Engber,et al.  Contribution of dopaminergic and glutamatergic mechanisms to the pathogenesis of motor response complications in Parkinson's disease. , 1996, Advances in neurology.

[40]  A. Antonini,et al.  The metabolic anatomy of Tourette's syndrome , 1997, Neurology.

[41]  H. Yamamura,et al.  SR141716A is an inverse agonist at the human cannabinoid CB1 receptor. , 1997, European journal of pharmacology.

[42]  D. Piomelli,et al.  Occurrence and Biosynthesis of Endogenous Cannabinoid Precursor,N-Arachidonoyl Phosphatidylethanolamine, in Rat Brain , 1997, The Journal of Neuroscience.

[43]  D. Piomelli,et al.  Functional role of high-affinity anandamide transport, as revealed by selective inhibition. , 1997, Science.

[44]  C. Routledge,et al.  Evidence to Suggest that Agonist Modulation of Hyperlocomotion is Via Post-synaptic Dopamine D2 or D3 Receptors , 1997, Neuropharmacology.

[45]  L. Matsuda,et al.  Molecular aspects of cannabinoid receptors. , 1997, Critical reviews in neurobiology.

[46]  D. Piomelli,et al.  A second endogenous cannabinoid that modulates long-term potentiation , 1997, Nature.

[47]  K. Waku,et al.  2‐Arachidonoylglycerol, an endogenous cannabinoid receptor agonist: identification as one of the major species of monoacylglycerols in various rat tissues, and evidence for its generation through Ca2+‐dependent and ‐independent mechanisms , 1998, FEBS letters.

[48]  D. Piomelli,et al.  Isotope dilution GC/MS determination of anandamide and other fatty acylethanolamides in rat blood plasma , 1998, FEBS letters.

[49]  D. Surmeier,et al.  Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. , 1998, Advances in pharmacology.

[50]  D. Piomelli,et al.  Control of pain initiation by endogenous cannabinoids , 1998, Nature.

[51]  K. Starke,et al.  Inhibition of GABAergic inhibitory postsynaptic currents by cannabinoids in rat corpus striatum , 1998, Neuroscience.