Cocaine-induced endocannabinoid release modulates behavioral and neurochemical sensitization in mice

Addiction Biology

Volumn 20, Issue 1, 2015, Pages 91-103

  Mereu, Maddalena ^a   Tronci, Valeria ^a   Chun, Lauren E ^a,b   Thomas, Alexandra M ^a,c   Green, Jennifer L ^a,d   Katz, Jonathan L ^a   Tanda, Gianluigi ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d University of North Carolina at Chapel Hill   (United States)

Author keywords

Behavioral sensitization; cannabinoid CB1 receptors; cocaine addiction; endocannabinoids; in vivo dopamine microdialysis; nucleus accumbens

Indexed keywords

CANNABINOID 1 RECEPTOR; COCAINE; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; DOPAMINE; ENDOCANNABINOID; FATTY ACID AMIDASE; NEUROTRANSMITTER; RIMONABANT; CANNABINOID RECEPTOR ANTAGONIST; DOPAMINE UPTAKE INHIBITOR; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROCHEMICAL DETECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIGHT DARK CYCLE; LOCOMOTION; MALE; MICRODIALYSIS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; SENSITIZATION; SWISS WEBSTER MOUSE; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; BRAIN; CENTRAL NERVOUS SYSTEM SENSITIZATION; COCAINE DEPENDENCE; DRUG EFFECTS; METABOLISM; MOTOR ACTIVITY; NUCLEUS ACCUMBENS;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CANNABINOID RECEPTOR ANTAGONISTS; CENTRAL NERVOUS SYSTEM SENSITIZATION; COCAINE; COCAINE-RELATED DISORDERS; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; ENDOCANNABINOIDS; MICE; MICRODIALYSIS; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; PIPERIDINES; PYRAZOLES; RECEPTOR, CANNABINOID, CB1;

EID: 84919839249     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/adb.12080     Document Type: Article

References (63)

1. Adamczyk P, Miszkiel J, McCreary AC, Filip M, Papp M, Przegalinski E, (2012) The effects of cannabinoid CB1, CB2 and vanilloid TRPV1 receptor antagonists on cocaine addictive behavior in rats. Brain Res 1444: 45-54.
2. Arnold JC, (2005) The role of endocannabinoid transmission in cocaine addiction. Pharmacol Biochem Behav 81: 396-406.
3. Belin D, Everitt BJ, (2008) Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 57: 432-441.
4. Bowers MS, Chen BT, Bonci A, (2010) AMPA receptor synaptic plasticity induced by psychostimulants: the past, present, and therapeutic future. Neuron 67: 11-24.
5. Cadoni C, Solinas M, Di Chiara G, (2000) Psychostimulant sensitization: differential changes in accumbal shell and core dopamine. Eur J Pharmacol 388: 69-76.
6. Caille S, Alvarez-Jaimes L, Polis I, Stouffer DG, Parsons LH, (2007) Specific alterations of extracellular endocannabinoid levels in the nucleus accumbens by ethanol, heroin, and cocaine self-administration. J Neurosci 27: 3695-3702.
7. Caprioli A, Coccurello R, Rapino C, Di Serio S, Di Tommaso M, Vertechy M, Vacca V, Battista N, Pavone F, Maccarrone M, Borsini F, (2012) The novel reversible fatty acid amide hydrolase inhibitor ST4070 increases endocannabinoid brain levels and counteracts neuropathic pain in different animal models. J Pharmacol Exp Ther 342: 188-195.
8. Centonze D, Battista N, Rossi S, Mercuri NB, Finazzi-Agro A, Bernardi G, Calabresi P, Maccarrone M, (2004) A critical interaction between dopamine D2 receptors and endocannabinoids mediates the effects of cocaine on striatal gabaergic transmission. Neuropsychopharmacology 29: 1488-1497.
9. Cheer JF, Wassum KM, Sombers LA, Heien ML, Ariansen JL, Aragona BJ, Phillips PE, Wightman RM, (2007) Phasic dopamine release evoked by abused substances requires cannabinoid receptor activation. J Neurosci 27: 791-795.
10. Corbille AG, Valjent E, Marsicano G, Ledent C, Lutz B, Herve D, Girault JA, (2007) Role of cannabinoid type 1 receptors in locomotor activity and striatal signaling in response to psychostimulants. J Neurosci 27: 6937-6947.
11. Cossu G, Ledent C, Fattore L, Imperato A, Bohme GA, Parmentier M, Fratta W, (2001) Cannabinoid CB1 receptor knockout mice fail to self-administer morphine but not other drugs of abuse. Behav Brain Res 118: 61-65.
12. Di Chiara G, (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 137: 75-114.
13. Di Chiara G, Acquas E, Tanda G, Cadoni C, (1993) Drugs of abuse: biochemical surrogates of specific aspects of natural reward? Biochem Soc Symp 59: 65-81.
14. Di Chiara G, Tanda G, Bassareo V, Pontieri F, Acquas E, Fenu S, Cadoni C, Carboni E, (1999) Drug addiction as a disorder of associative learning. Role of nucleus accumbens shell/extended amygdala dopamine. Ann N Y Acad Sci 877: 461-485.
15. Di Chiara G, Tanda G, Cadoni C, Acquas E, Bassareo V, Carboni E, (1998) Homologies and differences in the action of drugs of abuse and a conventional reinforcer (food) on dopamine transmission: an interpretative framework of the mechanism of drug dependence. Adv Pharmacol 42: 983-987.
16. Eisenstein SA, Holmes PV, Hohmann AG, (2009) Endocannabinoid modulation of amphetamine sensitization is disrupted in a rodent model of lesion-induced dopamine dysregulation. Synapse 63: 941-950.
17. Everitt BJ, Robbins TW, (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8: 1481-1489.
18. Fernandez-Espejo E, Ramiro-Fuentes S, Rodriguez de Fonseca F, (2009) The absence of a functional peroxisome o proliferator-activated receptor-alpha gene in mice enhances motor sensitizing effects of morphine, but not cocaine. Neuroscience 164: 667-675.
19. Ferrer B, Asbrock N, Kathuria S, Piomelli D, Giuffrida A, (2003) Effects of levodopa on endocannabinoid levels in rat basal ganglia: implications for the treatment of levodopa-induced dyskinesias. Eur J Neurosci 18: 1607-1614.
20. Filip M, Golda A, Zaniewska M, McCreary AC, Nowak E, Kolasiewicz W, Przegalinski E, (2006) Involvement of cannabinoid CB1 receptors in drug addiction: effects of rimonabant on behavioral responses induced by cocaine. Pharmacol Rep 58: 806-819.
21. Fourgeaud L, Mato S, Bouchet D, Hemar A, Worley PF, Manzoni OJ, (2004) A single in vivo exposure to cocaine abolishes endocannabinoid-mediated long-term depression in the nucleus accumbens. J Neurosci 24: 6939-6945.
22. Gerdeman GL, Ronesi J, Lovinger DM, (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5: 446-451.
23. Gerdeman GL, Schechter JB, French ED, (2008) Context-specific reversal of cocaine sensitization by the CB1 cannabinoid receptor antagonist rimonabant. Neuropsychopharmacology 33: 2747-2759.
24. Giuffrida A, Parsons LH, Kerr TM, Rodriguez de Fonseca F, Navarro M, Piomelli D, (1999) Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nat Neurosci 2: 358-363.
25. Gonzalez S, Cascio MG, Fernandez-Ruiz J, Fezza F, Di Marzo V, Ramos JA, (2002) Changes in endocannabinoid contents in the brain of rats chronically exposed to nicotine, ethanol or cocaine. Brain Res 954: 73-81.
26. Grueter BA, Brasnjo G, Malenka RC, (2010) Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat Neurosci 13: 1519-1525.
27. Kalivas PW, Duffy P, (1993) Time course of extracellular dopamine and behavioral sensitization to cocaine. I. Dopamine axon terminals. J Neurosci 13: 266-275.
28. Kathuria S, Gaetani S, Fegley D, Valino F, Duranti A, Tontini A, Mor M, Tarzia G, La Rana G, Calignano A, Giustino A, Tattoli M, Palmery M, Cuomo V, Piomelli D, (2003) Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 9: 76-81.
29. Kauer JA, Malenka RC, (2007) Synaptic plasticity and addiction. Nat Rev Neurosci 8: 844-858.
30. Koob GF, Volkow ND, (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35: 217-238.
31. Lesscher HM, Hoogveld E, Burbach JP, van Ree JM, Gerrits MA, (2005) Endogenous cannabinoids are not involved in cocaine reinforcement and development of cocaine-induced behavioural sensitization. Eur Neuropsychopharmacol 15: 31-37.
32. Li X, Hoffman AF, Peng XQ, Lupica CR, Gardner EL, Xi ZX, (2009) Attenuation of basal and cocaine-enhanced locomotion and nucleus accumbens dopamine in cannabinoid CB1-receptor-knockout mice. Psychopharmacology (Berl) 204: 1-11.
33. Li Y, Acerbo MJ, Robinson TE, (2004) The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur J Neurosci 20: 1647-1654.
34. Loland CJ, Mereu M, Okunola OM, Cao J, Prisinzano TE, Mazier S, Kopajtic T, Shi L, Katz JL, Tanda G, Newman AH, (2012) R-modafinil (armodafinil): a unique dopamine uptake inhibitor and potential medication for psychostimulant abuse. Biol Psychiatry 72: 405-413.
35. Luchicchi A, Lecca S, Carta S, Pillolla G, Muntoni AL, Yasar S, Goldberg SR, Pistis M, (2010) Effects of fatty acid amide hydrolase inhibition on neuronal responses to nicotine, cocaine and morphine in the nucleus accumbens shell and ventral tegmental area: involvement of PPAR-alpha nuclear receptors. Addict Biol 15: 277-288.
36. Luque-Rojas MJ, Galeano P, Suarez J, Araos P, Santin LJ, de Fonseca FR, Calvo EB, (2013) Hyperactivity induced by the dopamine D2/D3 receptor agonist quinpirole is attenuated by inhibitors of endocannabinoid degradation in mice. Int J Neuropsychopharmacol 16: 661-676.
37. Pan B, Hillard CJ, Liu QS, (2008a) D2 dopamine receptor activation facilitates endocannabinoid-mediated long-term synaptic depression of GABAergic synaptic transmission in midbrain dopamine neurons via cAMP-protein kinase A signaling. J Neurosci 28: 14018-14030.
38. Pan B, Hillard CJ, Liu QS, (2008b) Endocannabinoid signaling mediates cocaine-induced inhibitory synaptic plasticity in midbrain dopamine neurons. J Neurosci 28: 1385-1397.
39. Paxinos G, Franklin KBJ, (2001) The Mouse Brain in Stereotaxic Coordinates, 2nd edn. New York: Academic Press.
40. Pierce RC, Bell K, Duffy P, Kalivas PW, (1996) Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization. J Neurosci 16: 1550-1560.
41. Pierce RC, Vanderschuren LJ, (2010) Kicking the habit: the neural basis of ingrained behaviors in cocaine addiction. Neurosci Biobehav Rev 35: 212-219.
42. Pontieri FE, Tanda G, Di Chiara G, (1995) Intravenous cocaine, morphine, and amphetamine preferentially increase extracellular dopamine in the 'shell' as compared with the 'core' of the rat nucleus accumbens. Proc Natl Acad Sci U S A 92: 12304-12308.
43. Robinson TE, Berridge KC, (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18: 247-291.
44. Robinson TE, Berridge KC, (2003) Addiction. Annu Rev Psychol 54: 25-53.
45. Ross RA, Gibson TM, Brockie HC, Leslie M, Pashmi G, Craib SJ, Di Marzo V, Pertwee RG, (2001) Structure-activity relationship for the endogenous cannabinoid, anandamide, and certain of its analogues at vanilloid receptors in transfected cells and vas deferens. Br J Pharmacol 132: 631-640.
46. Saal D, Dong Y, Bonci A, Malenka RC, (2003) Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37: 577-582.
47. Seif T, Makriyannis A, Kunos G, Bonci A, Hopf FW, (2011) The endocannabinoid 2-arachidonoylglycerol mediates D1 and D2 receptor cooperative enhancement of rat nucleus accumbens core neuron firing. Neuroscience 193: 21-33.
48. Solinas M, Justinova Z, Goldberg SR, Tanda G, (2006) Anandamide administration alone and after inhibition of fatty acid amide hydrolase (FAAH) increases dopamine levels in the nucleus accumbens shell in rats. J Neurochem 98: 408-419.
49. Solinas M, Tanda G, Wertheim CE, Goldberg SR, (2010) Dopaminergic augmentation of delta-9-tetrahydrocannabinol (THC) discrimination: possible involvement of D(2)-induced formation of anandamide. Psychopharmacology (Berl) 209: 191-202.
50. Soria G, Mendizabal V, Tourino C, Robledo P, Ledent C, Parmentier M, Maldonado R, Valverde O, (2005) Lack of CB1 cannabinoid receptor impairs cocaine self-administration. Neuropsychopharmacology 30: 1670-1680.
51. Tanda G, (2007) Modulation of the endocannabinoid system: therapeutic potential against cocaine dependence. Pharmacol Res 56: 406-417.
52. Tanda G, Ebbs A, Newman AH, Katz JL, (2005) Effects of 4'-chloro-3 alpha-(diphenylmethoxy)-tropane on mesostriatal, mesocortical, and mesolimbic dopamine transmission: comparison with effects of cocaine. J Pharmacol Exp Ther 313: 613-620.
53. Tanda G, Newman AH, Ebbs AL, Tronci V, Green JL, Tallarida RJ, Katz JL, (2009) Combinations of cocaine with other dopamine uptake inhibitors: assessment of additivity. J Pharmacol Exp Ther 330: 802-809.
54. Thiemann G, van der Stelt M, Petrosino S, Molleman A, Di Marzo V, Hasenohrl RU, (2008) The role of the CB1 cannabinoid receptor and its endogenous ligands, anandamide and 2-arachidonoylglycerol, in amphetamine-induced behavioural sensitization. Behav Brain Res 187: 289-296.
55. Toth A, Blumberg PM, Boczan J, (2009) Anandamide and the vanilloid receptor (TRPV1). Vitam Horm 81: 389-419.
56. Tronci V, Tanda G, (2007) Involvement of CB1 cannabinoid receptors in cocaine-induced locomotor sensitization after single pre-exposure in mice. FASEB J 21: A410-A410.
57. Ungless MA, Whistler JL, Malenka RC, Bonci A, (2001) Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411: 583-587.
58. Vanderschuren LJ, Kalivas PW, (2000) Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology (Berl) 151: 99-120.
59. Wilson RI, Nicoll RA, (2002) Endocannabinoid signaling in the brain. Science 296: 678-682.
60. Wiskerke J, Irimia C, Cravatt BF, De Vries TJ, Schoffelmeer AN, Pattij T, Parsons LH, (2012) Characterization of the effects of reuptake and hydrolysis inhibition on interstitial endocannabinoid levels in the brain: an in vivo microdialysis study. ACS Chem Neurosci 3: 407-417.
61. Wiskerke J, Pattij T, Schoffelmeer AN, De Vries TJ, (2008) The role of CB1 receptors in psychostimulant addiction. Addict Biol 13: 225-238.
62. Xi ZX, Gilbert JG, Peng XQ, Pak AC, Li X, Gardner EL, (2006) Cannabinoid CB1 receptor antagonist AM251 inhibits cocaine-primed relapse in rats: role of glutamate in the nucleus accumbens. J Neurosci 26: 8531-8536.
63. Zocchi A, Girlanda E, Varnier G, Sartori I, Zanetti L, Wildish GA, Lennon M, Mugnaini M, Heidbreder CA, (2003) Dopamine responsiveness to drugs of abuse: a shell-core investigation in the nucleus accumbens of the mouse. Synapse 50: 293-302.