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Role of Endogenous Cannabinoids in Synaptic Signaling

Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary; Department of Clinical Neurobiology, University Hospital of Neurology, Heidelberg, Germany; and Department of Pharmacology, University of California Irvine, Irvine, California

Freund, Tamás F., István Katona, and Daniele Piomelli. Role of Endogenous Cannabinoids in Synaptic Signaling. Physiol Rev 83: 1017–1066, 2003; 10.1152/physrev.00004.2003.—Research of cannabinoid actions was boosted in the 1990s by remarkable discoveries including identification of endogenous compounds with cannabimimetic activity (endocannabinoids) and the cloning of their molecular targets, the CB₁ and CB₂ receptors. Although the existence of an endogenous cannabinoid signaling system has been established for a decade, its physiological roles have just begun to unfold. In addition, the behavioral effects of exogenous cannabinoids such as delta-9-tetrahydrocannabinol, the major active compound of hashish and marijuana, await explanation at the cellular and network levels. Recent physiological, pharmacological, and high-resolution anatomical studies provided evidence that the major physiological effect of cannabinoids is the regulation of neurotransmitter release via activation of presynaptic CB₁ receptors located on distinct types of axon terminals throughout the brain. Subsequent discoveries shed light on the functional consequences of this localization by demonstrating the involvement of endocannabinoids in retrograde signaling at GABAergic and glutamatergic synapses. In this review, we aim to synthesize recent progress in our understanding of the physiological roles of endocannabinoids in the brain. First, the synthetic pathways of endocannabinoids are discussed, along with the putative mechanisms of their release, uptake, and degradation. The fine-grain anatomical distribution of the neuronal cannabinoid receptor CB₁ is described in most brain areas, emphasizing its general presynaptic localization and role in controlling neurotransmitter release. Finally, the possible functions of endocannabinoids as retrograde synaptic signal molecules are discussed in relation to synaptic plasticity and network activity patterns.

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				C. G. Reich, M. A. Karson, S. V. Karnup, L. M. Jones, and B. E. Alger Regulation of IPSP Theta Rhythm by Muscarinic Receptors and Endocannabinoids in Hippocampus J Neurophysiol, December 1, 2005; 94(6): 4290 - 4299. [Abstract] [Full Text] [PDF]

				H. Schuel and L. J. Burkman A Tale of Two Cells: Endocannabinoid-Signaling Regulates Functions of Neurons and Sperm Biol Reprod, December 1, 2005; 73(6): 1078 - 1086. [Abstract] [Full Text] [PDF]

				S. M. Thompson, J. P. Y. Kao, R. H. Kramer, K. E. Poskanzer, R. A. Silver, D. Digregorio, and S. S.-H. Wang Flashy Science: Controlling Neural Function with Light J. Neurosci., November 9, 2005; 25(45): 10358 - 10365. [Full Text] [PDF]

				B. E. Alger Endocannabinoid Identification in the Brain: Studies of Breakdown Lead to Breakthrough, and There May Be NO Hope Sci. Signal., November 8, 2005; 2005(309): pe51 - pe51. [Abstract] [Full Text] [PDF]

				K.-M. Jung, R. Mangieri, C. Stapleton, J. Kim, D. Fegley, M. Wallace, K. Mackie, and D. Piomelli Stimulation of Endocannabinoid Formation in Brain Slice Cultures through Activation of Group I Metabotropic Glutamate Receptors Mol. Pharmacol., November 1, 2005; 68(5): 1196 - 1202. [Abstract] [Full Text] [PDF]

				T. Klausberger, L. F. Marton, J. O'Neill, J. H. J. Huck, Y. Dalezios, P. Fuentealba, W. Y. Suen, E. Papp, T. Kaneko, M. Watanabe, et al. Complementary Roles of Cholecystokinin- and Parvalbumin-Expressing GABAergic Neurons in Hippocampal Network Oscillations J. Neurosci., October 19, 2005; 25(42): 9782 - 9793. [Abstract] [Full Text] [PDF]

				M. D. Van Sickle, M. Duncan, P. J. Kingsley, A. Mouihate, P. Urbani, K. Mackie, N. Stella, A. Makriyannis, D. Piomelli, J. S. Davison, et al. Identification and Functional Characterization of Brainstem Cannabinoid CB2 Receptors Science, October 14, 2005; 310(5746): 329 - 332. [Abstract] [Full Text] [PDF]

				T. Heinbockel, D. H. Brager, C. G. Reich, J. Zhao, S. Muralidharan, B. E. Alger, and J. P. Y. Kao Endocannabinoid Signaling Dynamics Probed with Optical Tools J. Neurosci., October 12, 2005; 25(41): 9449 - 9459. [Abstract] [Full Text] [PDF]

				N. Wettschureck and S. Offermanns Mammalian G Proteins and Their Cell Type Specific Functions Physiol Rev, October 1, 2005; 85(4): 1159 - 1204. [Abstract] [Full Text] [PDF]

				M. Isokawa and B. E Alger Retrograde endocannabinoid regulation of GABAergic inhibition in the rat dentate gyrus granule cell J. Physiol., September 15, 2005; 567(3): 1001 - 1010. [Abstract] [Full Text] [PDF]

				S. Ambrosi, L. Ragni, A. Ambrosini, L. Paccamiccio, P. Mariani, R. Fiorini, E. Bertoli, and G. Zolese On the importance of anandamide structural features for its interactions with DPPC bilayers: effects on PLA2 activity J. Lipid Res., September 1, 2005; 46(9): 1953 - 1961. [Abstract] [Full Text] [PDF]

				Y. Zilberter, T. Harkany, and C. D. Holmgren Dendritic Release of Retrograde Messengers Controls Synaptic Transmission in Local Neocortical Networks Neuroscientist, August 1, 2005; 11(4): 334 - 344. [Abstract] [PDF]

				A. L. Bodor, I. Katona, G. Nyiri, K. Mackie, C. Ledent, N. Hajos, and T. F. Freund Endocannabinoid Signaling in Rat Somatosensory Cortex: Laminar Differences and Involvement of Specific Interneuron Types J. Neurosci., July 20, 2005; 25(29): 6845 - 6856. [Abstract] [Full Text] [PDF]

				P. J. Zhu and D. M. Lovinger Retrograde Endocannabinoid Signaling in a Postsynaptic Neuron/Synaptic Bouton Preparation from Basolateral Amygdala J. Neurosci., June 29, 2005; 25(26): 6199 - 6207. [Abstract] [Full Text] [PDF]

				C. Bernard, M. Milh, Y. M. Morozov, Y. Ben-Ari, T. F. Freund, and H. Gozlan Altering cannabinoid signaling during development disrupts neuronal activity PNAS, June 28, 2005; 102(26): 9388 - 9393. [Abstract] [Full Text] [PDF]

				Z. Justinova, M. Solinas, G. Tanda, G. H. Redhi, and S. R. Goldberg The Endogenous Cannabinoid Anandamide and Its Synthetic Analog R(+)-Methanandamide Are Intravenously Self-Administered by Squirrel Monkeys J. Neurosci., June 8, 2005; 25(23): 5645 - 5650. [Abstract] [Full Text] [PDF]

				D. J. Rademacher, S. Patel, W.-S. V. Ho, A. M. Savoie, N. J. Rusch, K. M. Gauthier, and C. J. Hillard U-46619 but not serotonin increases endocannabinoid content in middle cerebral artery: evidence for functional relevance Am J Physiol Heart Circ Physiol, June 1, 2005; 288(6): H2694 - H2701. [Abstract] [Full Text] [PDF]