Synaptic effects of cannabinoids: Complexity, behavioral effects, and potential clinical implications

Neurology

Volumn 83, Issue 21, 2014, Pages 1958-1967

  Benarroch, Eduardo E ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 ARACHODONOYL GLYCEROL; ANANDAMIDE; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR; DOPAMINE; DRONABINOL; ENDOCANNABINOID; HUNTINGTIN; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; TRPV1 PROTEIN, HUMAN; VANILLOID RECEPTOR;

ANTINOCICEPTION; ARTICLE; BASAL GANGLION; DOPAMINERGIC SYSTEM; ENERGY BALANCE; GLIA; HIPPOCAMPUS; MESENCEPHALON; MOSAICISM; MOTOR DYSFUNCTION; MULTIPLE SCLEROSIS; NERVE CELL; NERVE CELL NETWORK; NONHUMAN; PAIN; PRIORITY JOURNAL; SEIZURE; SIGNAL TRANSDUCTION; STRESS; SYNAPSE; SYNTHESIS; ADDICTION; ANIMAL; DEGENERATIVE DISEASE; HUMAN; METABOLISM; PHYSIOLOGY; PSYCHOLOGY;

ANIMALS; BEHAVIOR, ADDICTIVE; ENDOCANNABINOIDS; HUMANS; NERVE NET; NEURODEGENERATIVE DISEASES; SIGNAL TRANSDUCTION; SYNAPSES; TRPV CATION CHANNELS;

EID: 84922480780     PISSN: 00283878     EISSN: 1526632X     Source Type: Journal    
DOI: 10.1212/WNL.0000000000001013     Document Type: Article

References (98)

1. Katona I, Freund TF. Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat Med 2008;14:923-930.
2. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M. Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 2009; 89:309-380.
3. Pertwee RG, Howlett AC, Abood ME, et al. International Union of Basic and Clinical Pharmacology: LXXIX: can-nabinoid receptors and their ligands: Beyond CB(1) and CB(2). Pharmacol Rev 2010;62:588-631.
4. Katona I, Freund TF. Multiple functions of endocannabi-noid signaling in the brain. Annu Rev Neurosci 2012;35: 529-558.
5. Castillo PE, Younts TJ, Chavez AE, Hashimotodani Y. Endocannabinoid signaling and synaptic function. Neuron 2012;76:70-81.
6. Iremonger KJ, Wamsteeker Cusulin JI, Bains JS. Changing the tune: plasticity and adaptation of retrograde signals. Trends Neurosci 2013;36:471-479.
7. Ohno-Shosaku T, Kano M. Endocannabinoid-mediated retrograde modulation of synaptic transmission. Curr Opin Neurobiol 2014;29C:1-8.
8. Piomelli D. More surprises lying ahead: the endocannabi-noids keep us guessing. Neuropharmacology 2014;76: 228-234.
9. Jung KM, Sepers M, Henstridge CM, et al. Uncoupling of the endocannabinoid signalling complex in a mouse model of fragile X syndrome. Nat Commun 2012;3:1080.
10. Dinh TP, Carpenter D, Leslie FM, et al. Brain monoglyc-eride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci USA 2002;99:10819-10824.
11. Marrs WR, Blankman JL, Horne EA, et al. The serine hydrolase ABHD6 controls the accumulation and efficacy of 2-AG at cannabinoid receptors. Nat Neurosci 2010;13: 951-957.
12. Ueda N, Tsuboi K, Uyama T. Metabolism of endocanna-binoids and related N-acylethanolamines: canonical and alternative pathways. FEBS J 2013;280:1874-1894.
13. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990;346: 561-564.
14. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993;365:61-65.
15. Herkenham M, Lynn AB, Little MD, et al. Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 1990;87:1932-1936.
16. Glass M, Dragunow M, Faull RL. Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience 1997;77:299-318.
17. Atwood BK, Mackie K. CB2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 2010;160:467-479.
18. Stella N. Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas. Glia 2010;58: 1017-1030.
19. Sanchez-Blazquez P, Rodriguez-Munoz M, Garzon J. The cannabinoid receptor 1 associates with NMDA receptors to produce glutamatergic hypofunction: implications in psychosis and schizophrenia. Front Pharmacol 2014;4:169.
20. Smart D, Jerman JC. Anandamide: an endogenous activator of the vanilloid receptor. Trends Pharmacol Sci 2000;21:134.
21. Singla S, Kreitzer AC, Malenka RC. Mechanisms for synapse specificity during striatal long-term depression. J Neurosci 2007;27:5260-5264.
22. Bacci A, Huguenard JR, Prince DA. Long-lasting self-inhibition of neocortical interneurons mediated by endo-cannabinoids. Nature 2004;431:312-316.
23. Marinelli S, Pacioni S, Cannich A, Marsicano G, Bacci A. Self-modulation of neocortical pyramidal neurons by en-docannabinoids. Nat Neurosci 2009;12:1488-1490.
24. Kim J, Alger BE. Reduction in endocannabinoid tone is a homeostatic mechanism for specific inhibitory synapses. Nat Neurosci 2010;13:592-600.
25. Hill MN, McLaughlin RJ, Bingham B, et al. Endogenous cannabinoid signaling is essential for stress adaptation. Proc Natl Acad Sci USA 2010;107:9406-9411.
26. Grueter BA, Brasnjo G, Malenka RC. Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat Neurosci 2010;13:1519-1525.
27. Chavez AE, Chiu CQ, Castillo PE. TRPV1 activation by endogenous anandamide triggers postsynaptic long-term depression in dentate gyrus. Nat Neurosci 2010;13: 1511-1518.
28. Walter L, Dinh T, Stella N. ATP induces a rapid and pronounced increase in 2-arachidonoylglycerol production by astrocytes, a response limited by monoacylglycerol lipase. J Neurosci 2004;24:8068-8074.
29. Navarrete M, Araque A. Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron 2010;68:113-126.
30. Han J, Kesner P, Metna-Laurent M, et al. Acute cannab-inoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD. Cell 2012; 148:1039-1050.
31. Min R, Nevian T. Astrocyte signaling controls spike timing-dependent depression at neocortical synapses. Nat Neurosci 2012;15:746-753.
32. Xu JY, Chen C. Endocannabinoids in synaptic plasticity and neuroprotection. Neuroscientist Epub 2014 Feb 25.
33. Hashimotodani Y, Ohno-Shosaku T, Kano M. Ca(21)-assisted receptor-driven endocannabinoid release: mechanisms that associate presynaptic and postsynaptic activities. Curr Opin Neurobiol 2007;17:360-365.
34. Mathur BN, Lovinger DM. Endocannabinoid-dopamine interactions in striatal synaptic plasticity. Front Pharmacol 2012;3:66.
35. Lerner TN, Kreitzer AC. RGS4 is required for dopamin-ergic control of striatal LTD and susceptibility to parkin-sonian motor deficits. Neuron 2012;73:347-359.
36. Chiu CQ, Puente N, Grandes P, Castillo PE. Dopamin-ergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J Neurosci 2010;30:7236-7248.
37. Chaperon F, Thiebot MH. Behavioral effects of cannabinoid agents in animals. Crit Rev Neurobiol 1999;13:243-281.
38. Hillard CJ, Weinlander KM, Stuhr KL. Contributions of endocannabinoid signaling to psychiatric disorders in humans: genetic and biochemical evidence. Neuroscience 2012;204:207-229.
39. Fernandez-Ruiz J, Hernandez M, Ramos JA. Cannabi-noid-dopamine interaction in the pathophysiology and treatment of CNS disorders. CNS Neurosci Ther 2010; 16:e72-e91.
40. El Manira A, Kyriakatos A. The role of endocannabinoid signaling in motor control. Physiology2010;25:230-238.
41. Starowicz K, Przewlocka B. Modulation of neuropathic-pain-related behaviour by the spinal endocannabinoid/en-dovanilloid system. Philos Trans R Soc Lond B Biol Sci 2012;367:3286-3299.
42. Skaper SD, Di Marzo V. Endocannabinoids in nervous system health and disease: the big picture in a nutshell. Philos Trans R Soc Lond B Biol Sci 2012;367: 3193-3200.
43. Hoffman AF, Lupica CR. Synaptic targets of Delta9-tetrahydrocannabinol in the central nervous system. Cold Spring Harb Perspect Med 2013;3.
44. Riedel G, Davies SN. Cannabinoid function in learning, memory and plasticity. Handb Exp Pharmacol 2005;168: 445-477.
45. Robbe D, Montgomery SM, Thome A, Rueda-Orozco PE, McNaughton BL, Buzsaki G. Cannabinoids reveal importance of spike timing coordination in hippo-campal function. Nat Neurosci 2006;9:1526-1533.
46. Kucewicz MT, Tricklebank MD, Bogacz R, Jones MW. Dysfunctional prefrontal cortical network activity and interactions following cannabinoid receptor activation. J Neurosci 2011;31:15560-15568.
47. Tortoriello G, Morris CV, Alpar A, et al. Miswiring the brain: delta9-tetrahydrocannabinol disrupts cortical development by inducing an SCG10/stathmin-2 degradation pathway. EMBO J 2014;33:668-685.
48. Zalesky A, Solowij N, Yucel M, et al. Effect of long-term cannabis use on axonal fibre connectivity. Brain 2012;135: 2245-2255.
49. Filbey F, Yezhuvath U. Functional connectivity in inhibitory control networks and severity of cannabisuse disorder. Am J Drug Alcohol Abuse 2013;39: 382-391.
50. Sales-Carbonell C, Rueda-Orozco PE, Soria-Gomez E, Buzsaki G, Marsicano G, Robbe D. Striatal GABAergic and cortical glutamatergic neurons mediate contrasting effects of cannabinoids on cortical network synchrony. Proc Natl Acad Sci USA 2013;110:719-724.
51. Lovinger DM, Mathur BN. Endocannabinoids in striatal plasticity. Parkinsonism Relat Disord 2012;18(suppl 1): S132-S134.
52. Morera-Herreras T, Miguelez C, Aristieta A, Ruiz- Ortega JA, Ugedo L. Endocannabinoid modulation of dopaminergic motor circuits. Front Pharmacol 2012;3:110.
53. Freestone PS, Guatteo E, Piscitelli F, di Marzo V, Lipski J, Mercuri NB. Glutamate spillover drives endocannabinoid production and inhibits GABAergic transmission in the substantia nigra pars compacta. Neuropharmacology 2014;79:467-475.
54. Kyriakatos A, El Manira A. Long-term plasticity of the spinal locomotor circuitry mediated by endocannabinoid and nitric oxide signaling. J Neurosci 2007;27: 12664-12674.
55. Song J, Kyriakatos A, El Manira A. Gating the polarity of endocannabinoid-mediated synaptic plasticity by nitric oxide in the spinal locomotor network. J Neurosci 2012; 32:5097-5105.
56. Cravatt BF, Lichtman AH. The endogenous cannabinoid system and its role in nociceptive behavior. J Neurobiol 2004;61:149-160.
57. Hohmann AG, Suplita RL II. Endocannabinoid mechanisms of pain modulation. AAPS J 2006;8:E693-E708.
58. Zogopoulos P, Vasileiou I, Patsouris E, Theocharis SE. The role of endocannabinoids in pain modulation. Fun-dam Clin Pharmacol 2013;27:64-80.
59. Pernia-Andrade AJ, Kato A, Witschi R, et al. Spinal endo-cannabinoids and CB1 receptors mediate C-fiber-induced heterosynaptic pain sensitization. Science 2009;325: 760-764.
60. Harkany T, Keimpema E, Barabas K, Mulder J. Endocan-nabinoid functions controlling neuronal specification during brain development. Mol Cell Endocrinol 2008;286: S84-S90.
61. Zhu PJ, Lovinger DM. Developmental alteration of endo-cannabinoid retrograde signaling in the hippocampus. J Neurophysiol 2010;103:1123-1129.
62. Yasuda H, Huang Y, Tsumoto T. Regulation of excitability and plasticity by endocannabinoids and PKA in developing hippocampus. Proc Natl Acad Sci USA 2008;105: 3106-3111.
63. Chen K, Ratzliff A, Hilgenberg L, et al. Long-term plasticity of endocannabinoid signaling induced by developmental febrile seizures. Neuron 2003;39:599-611.
64. Riebe CJ, Wotjak CT. Endocannabinoids and stress. Stress 2011;14:384-397.
65. Wamsteeker JI, Kuzmiski JB, Bains JS. Repeated stress impairs endocannabinoid signaling in the paraven-tricular nucleus of the hypothalamus. J Neurosci 2010;30: 11188-11196.
66. Wang W, Sun D, Pan B, et al. Deficiency in endocanna-binoid signaling in the nucleus accumbens induced by chronic unpredictable stress. Neuropsychopharmacology 2010;35:2249-2261.
67. Patel S, Kingsley PJ, Mackie K, Marnett LJ, Winder DG. Repeated homotypic stress elevates 2-arachidonoylglycerol levels and enhances short-term endocannabinoid signaling at inhibitory synapses in basolateral amygdala. Neuropsy-chopharmacology 2009;34:2699-2709.
68. Wang M, Hill MN, Zhang L, Gorzalka BB, Hillard CJ, Alger BE. Acute restraint stress enhances hippocampal en-docannabinoid function via glucocorticoid receptor activation. J Psychopharmacol 2012;26:56-70.
69. Banni S, Di Marzo V. Effect of dietary fat on endocanna-binoids and related mediators: consequences on energy homeostasis, inflammation and mood. Mol Nutr Food Res 2010;54:82-92.
70. DiPatrizio NV, Piomelli D. The thrifty lipids: endocanna-binoids and the neural control of energy conservation. Trends Neurosci 2012;35:403-411.
71. Massa F, Mancini G, Schmidt H, et al. Alterations in the hippocampal endocannabinoid system in diet-induced obese mice. J Neurosci 2010;30:6273-6281.
72. Crosby KM, Inoue W, Pittman QJ, Bains JS. Endocanna-binoids gate state-dependent plasticity of synaptic inhibition in feeding circuits. Neuron 2011;71:529-541.
73. Mato S, Chevaleyre V, Robbe D, Pazos A, Castillo PE, Manzoni OJ. A single in-vivo exposure to delta 9THC blocks endocannabinoid-mediated synaptic plasticity. Nat Neurosci 2004;7:585-586.
74. Hoffman AF, Oz M, Caulder T, Lupica CR. Functional tolerance and blockade of long-term depression at synapses in the nucleus accumbens after chronic cannabinoid exposure. J Neurosci 2003;23:4815-4820.
75. Volkow ND, Baler RD, Compton WM, Weiss SR. Adverse health effects of marijuana use. N Engl J Med 2014;370:2219-2227.
76. Baker D, Pryce G, Croxford JL, et al. Cannabinoids control spasticity and tremor in a multiple sclerosis model. Nature 2000; 404: 84-87.
77. Robson PJ. Therapeutic potential of cannabinoid medicines. Drug Test Anal 2014;6:24-30.
78. Koppel BS, Brust JC, Fife T, et al. Systematic review: efficacy and safety of medical marijuana in selected neurologic disorders: report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology 2014;82:1556-1563.
79. Garcia-Ovejero D, Arevalo-Martin A, Petrosino S, et al. The endocannabinoid system is modulated in response to spinal cord injury in rats. Neurobiol Dis 2009;33:57-71.
80. Pryce G, Ahmed Z, Hankey DJ, et al. Cannabinoids inhibit neurodegeneration in models of multiple sclerosis. Brain 2003;126:2191-2202.
81. Pryce G, Visintin C, Ramagopalan SV, et al. Control of spasticity in a multiple sclerosis model using central nervous system-excluded CB1 cannabinoid receptor agonists. FASEB J 2014;28:117-130.
82. Baker D, Pryce G. The endocannabinoid system and multiple sclerosis. Curr Pharm Des 2008; 14: 2326-2336.
83. Wallace MJ, Blair RE, Falenski KW, Martin BR, DeLorenzo RJ. The endogenous cannabinoid system regulates seizure frequency and duration in a model of temporal lobe epilepsy. J Pharmacol Exp Ther 2003; 307:129-137.
84. Monory K, Massa F, Egertova M, et al. The endocanna-binoid system controls key epileptogenic circuits in the hippocampus. Neuron 2006;51:455-466.
85. Deshpande LS, Sombati S, Blair RE, Carter DS, Martin BR, DeLorenzo RJ. Cannabinoid CB1 receptor antagonists cause status epilepticus-like activity in the hip-pocampal neuronal culture model of acquired epilepsy. Neurosci Lett 2007;411:11-16.
86. Ludanyi A, Eross L, Czirjak S, et al. Downregulation of the CB1 cannabinoid receptor and related molecular elements of the endocannabinoid system in epileptic human hippocampus. J Neurosci 2008;28:2976-2990.
87. Jones NA, Glyn SE, Akiyama S, et al. Cannabidiol exerts anti-convulsant effects in animal models of temporal lobe and partial seizures. Seizure 2012;21:344-352.
88. Cilio MR, Thiele EA, Devinsky O. The case for assessing cannabidiol in epilepsy. Epilepsia 2014;55:787-790.
89. Gloss D, Vickrey B. Cannabinoids for epilepsy. Cochrane Database Syst Rev 2014;3:CD009270.
90. Devinsky O, Cilio MR, Cross H, et al. Cannabidiol: pharmacology and potential therapeutic role in epilepsy and other neuropsychiatric disorders. Epilepsia 2014;55:791-802.
91. Di Filippo M, Picconi B, Tozzi A, Ghiglieri V, Rossi A, Calabresi P. The endocannabinoid system in Parkinson's disease. Curr Pharm Des 2008;14:2337-2347.
92. Fox SH, Henry B, Hill M, Crossman A, Brotchie J. Stimulation of cannabinoid receptors reduces levodopa-induced dyskinesia in the MPTP-lesioned nonhuman primate model of Parkinson's disease. Mov Disord 2002;17: 1180-1187.
93. Pazos MR, Sagredo O, Fernandez-Ruiz J. The endocanna-binoid system in Huntington's disease. Curr Pharm Des 2008;14:2317-2325.
94. de Lago E, Fernandez-Ruiz J, Ortega-Gutierrez S, et al. UCM707, an inhibitor of the anandamide uptake, behaves as a symptom control agent in models of Huntington's disease and multiple sclerosis, but fails to delay/arrest the progression of different motor-related disorders. Eur Neu-ropsychopharmacol 2006;16:7-18.
95. Di Marzo V, Hill MP, Bisogno T, Crossman AR, Brotchie JM. Enhanced levels of endogenous cannabinoids in the globus pallidus are associated with a reduction in movement in an animal model of Parkinson's disease. FA-SEB J 2000;14:1432-1438.
96. Van Laere K, Casteels C, Lunskens S, et al. Regional changes in type 1 cannabinoid receptor availability in Parkinson's disease in vivo. Neurobiol Aging 2012;33: e621-e628.
97. Blazquez C, Chiarlone A, Sagredo O, et al. Loss of striatal type 1 cannabinoid receptors is a key pathogenic factor in Huntington's disease. Brain 2011;134:119-136.
98. Mievis S, Blum D, Ledent C. Worsening of Huntington disease phenotype in CB1 receptor knockout mice. Neuro-biol Dis 2011;42:524-529.