The absence of VGLUT3 predisposes to cocaine abuse by increasing dopamine and glutamate signaling in the nucleus accumbens

Molecular Psychiatry

Volumn 20, Issue 11, 2015, Pages 1448-1459

  Sakae, D Y ^a,b,c   Marti, F ^a,b,c   Lecca, S ^a,d,e   Vorspan, F ^e,f,g   Martin Garcia E ^h   Morel, L J ^a,b,c   Henrion, A ^e,f,i,j   Gutierrez Cuesta J ^h   Besnard, A ^a,b   Heck, N ^a,b   Herzog, E ^a,b   Bolte, S ^a   Prado, V F ^k   Prado, M A M ^k   Bellivier, F ^e,f,g   Eap, C B ^l,m   Crettol, S ^l   Vanhoutte, P ^a,b   Caboche, J ^a,b   Gratton, A ^c   Moquin, L ^c   Giros, B ^a,b,c,f   Maldonado, R ^h   Daumas, S ^a,b   Mameli, M ^a,d,e   Jamain, S ^e,f,i,j   El Mestikawy, S ^a,b,c,f   more..

^a SORBONNE UNIVERSITÉ   (France)

^b and Centre National de la Recherche Scientifique Unité Mixte de Recherche 8246   (France)

^c MCGILL UNIVERSITY   (Canada)

^d INSTITUT DU FER À MOULIN   (France)

^e INSERM   (France)

^f FONDATION FONDAMENTAL   (France)

^g ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^h UNIVERSITAT POMPEU FABRA   (Spain)

ⁱ FACULTÉ DE MÉDECINE   (France)

^j HENRI MONDOR HOSPITAL   (France)

^k ROBARTS RESEARCH INSTITUTE   (Canada)

^l LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^m UNIVERSITY OF GENEVA   (Switzerland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

COCAINE; DOPAMINE; GLUTAMIC ACID; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR GLUTAMATE TRANSPORTER 3; DOPAMINE UPTAKE INHIBITOR; SLC17A8 PROTEIN, HUMAN; VESICULAR GLUTAMATE TRANSPORTER;

ACTION POTENTIAL; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COCAINE DEPENDENCE; CONDITIONED PLACE PREFERENCE TEST; CONTROLLED STUDY; DENDRITIC SPINE; DISEASE DURATION; ELECTROPHYSIOLOGICAL PROCEDURES; EXCITATORY POSTSYNAPTIC POTENTIAL; GENOTYPE; HUMAN; INTERNEURON; LOCOMOTION; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; OPIATE ADDICTION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TONICALLY ACTIVE CHOLINERGIC INTERNEURON; ANIMAL; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; DRUG SELF ADMINISTRATION; GENETIC PREDISPOSITION; GENETICS; INSTRUMENTAL CONDITIONING; METABOLISM; MIDDLE AGED; NERVE CELL; PATHOLOGY; PHYSIOLOGY; SYNAPTIC POTENTIAL; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ACTION POTENTIALS; ADULT; ANIMALS; COCAINE; COCAINE-RELATED DISORDERS; CONDITIONING, OPERANT; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; GENETIC PREDISPOSITION TO DISEASE; GLUTAMIC ACID; HUMANS; MICE; MICE, TRANSGENIC; MIDDLE AGED; NEURONS; NUCLEUS ACCUMBENS; OPIOID-RELATED DISORDERS; SELF ADMINISTRATION; SIGNAL TRANSDUCTION; SYNAPTIC POTENTIALS; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

EID: 84946496094     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2015.104     Document Type: Article

References (49)

1. Kalivas PW, Volkow ND. The neural basis of addiction: A pathology of motivation and choice. Am J Psychiatry 2005; 162: 1403-1413.
2. Luscher C, Ungless MA. The mechanistic classification of addictive drugs. PLoS Med 2006; 3: e437.
3. Gras C, Amilhon B, Lepicard EM, Poirel O, Vinatier J, Herbin M et al. The vesicular glutamate transporter VGLUT3 synergizes striatal acetylcholine tone. Nat Neurosci 2008; 11: 292-300.
4. Higley MJ, Gittis AH, Oldenburg IA, Balthasar N, Seal RP, Edwards RH et al. Cholinergic interneurons mediate fast VGluT3-dependent glutamatergic transmission in the striatum. PLoS One 2011; 6: e19155.
5. Guzman MS, De Jaeger X, Raulic S, Souza IA, Li AX, Schmid S et al. Elimination of the vesicular acetylcholine transporter in the striatum reveals regulation of behaviour by cholinergic-glutamatergic co-transmission. PLoS Biol 2011; 9: e1001194.
6. Crettol S, Deglon JJ, Besson J, Croquette-Krokar M, Hammig R, Gothuey I et al. ABCB1 and cytochrome P450 genotypes and phenotypes: influence on methadone plasma levels and response to treatment. Clin Pharmacol Ther 2006; 80: 668-681.
7. Besnard A, Bouveyron N, Kappes V, Pascoli V, Pages C, Heck N et al. Alterations of molecular and behavioral responses to cocaine by selective inhibition of Elk-1 phosphorylation. J Neurosci 2011; 31: 14296-14307.
8. Martin-Garcia E, Barbano MF, Galeote L, Maldonado R. New operant model of nicotine-seeking behaviour in mice. Int J Neuropsychopharmacol 2009; 12: 343-356.
9. Soria G, Barbano MF, Maldonado R, Valverde O. A reliable method to study cue-, priming-, and stress-induced reinstatement of cocaine self-administration in mice. Psychopharmacology 2008; 199: 593-603.
10. Soria G, Mendizabal V, Tourino C, Robledo P, Ledent C, Parmentier M et al. Lack of CB1 cannabinoid receptor impairs cocaine self-administration. Neuropsychopharmacology 2005; 30: 1670-1680.
11. Richardson NR, Gratton A. Changes in nucleus accumbens dopamine transmission associated with fixed-and variable-time schedule-induced feeding. Eur J Neurosci 2008; 27: 2714-2723.
12. Tolu S, Eddine R, Marti F, David V, Graupner M, Pons S et al. Co-activation of VTA DA and GABA neurons mediates nicotine reinforcement. Mol Psychiatry 2013; 18: 382-393.
13. Grace AA, Bunney BS. Intracellular and extracellular electrophysiology of nigral dopaminergic neurons-1. Identification and characterization. Neuroscience 1983; 10: 301-315.
14. Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 1984; 4: 2877-2890.
15. Mameli M, Bellone C, Brown MT, Luscher C. Cocaine inverts rules for synaptic plasticity of glutamate transmission in the ventral tegmental area. Nat Neurosci 2011; 14: 414-416.
16. Mameli M, Halbout B, Creton C, Engblom D, Parkitna JR, Spanagel R et al. Cocaineevoked synaptic plasticity: persistence in the VTA triggers adaptations in the NAc. Nat Neurosci 2009; 12: 1036-1041.
17. Amilhon B, Lepicard E, Renoir T, Mongeau R, Popa D, Poirel O et al. VGLUT3 (vesicular glutamate transporter type 3) contribution to the regulation of serotonergic transmission and anxiety. J Neurosci 2010; 30: 2198-2210.
18. Bolte S, Cordelieres FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 2006; 224: 213-232.
19. Jaskolski F, Mulle C, Manzoni OJ. An automated method to quantify and visualize colocalized fluorescent signals. J Neurosci Methods 2005; 146: 42-49.
20. Heck N, Betuing S, Vanhoutte P, Caboche J. A deconvolution method to improve automated 3D-analysis of dendritic spines: application to a mouse model of Huntington's disease. Brain Structure Function 2012; 217: 421-434.
21. Rodriguez A, Ehlenberger DB, Dickstein DL, Hof PR, Wearne SL. Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS One 2008; 3: e1997.
22. Sanchis-Segura C, Spanagel R. Behavioural assessment of drug reinforcement and addictive features in rodents: an overview. Addict Biol 2006; 11: 2-38.
23. Carboni E, Vacca C. Conditioned place preference. A simple method for investigating reinforcing properties in laboratory animals. Methods Mol Med 2003; 79: 481-498.
24. Schmitz Y, Benoit-Marand M, Gonon F, Sulzer D. Presynaptic regulation of dopaminergic neurotransmission. J Neurochem 2003; 87: 273-289.
25. Karasawa J, Yoshimizu T, Chaki S. A metabotropic glutamate 2/3 receptor antagonist, MGS0039, increases extracellular dopamine levels in the nucleus accumbens shell. Neurosci Lett 2006; 393: 127-130.
26. Fitzjohn SM, Bortolotto ZA, Palmer MJ, Doherty AJ, Ornstein PL, Schoepp DD et al. The potent mGlu receptor antagonist LY341495 identifies roles for both cloned and novel mGlu receptors in hippocampal synaptic plasticity. Neuropharmacology 1998; 37: 1445-1458.
27. Bertran-Gonzalez J, Bosch C, Maroteaux M, Matamales M, Herve D, Valjent E et al. Opposing patterns of signaling activation in dopamine D1 and D2 receptorexpressing striatal neurons in response to cocaine and haloperidol. J Neurosci 2008; 28: 5671-5685.
28. Robinson TE, Kolb B. Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur J Neurosci 1999; 11: 1598-1604.
29. Russo SJ, Dietz DM, Dumitriu D, Morrison JH, Malenka RC, Nestler EJ. The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci 2010; 33: 267-276.
30. Heck N, Dos Santos M, Amairi B, Salery M, Besnard A, Herzog E et al. A new automated 3D detection of synaptic contacts reveals the formation of cortico-striatal synapses upon cocaine treatment in vivo. Brain Structure Function 2014.
31. Sesack SR, Grace AA. Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 2010; 35: 27-47.
32. Kourrich S, Rothwell PE, Klug JR, Thomas MJ. Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J Neurosci 2007; 27: 7921-7928.
33. Pascoli V, Turiault M, Luscher C. Reversal of cocaine-evoked synaptic potentiation resets drug-induced adaptive behaviour. Nature 2012; 481: 71-75.
34. Genomes Project C, Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM et al. An integrated map of genetic variation from 1,092 human genomes. Nature 2012; 491: 56-65.
35. Brown MT, Tan KR, O'Connor EC, Nikonenko I, Muller D, Luscher C. Ventral tegmental area GABA projections pause accumbal cholinergic interneurons to enhance associative learning. Nature 2012; 492: 452-456.
36. Tepper JM, Bolam JP. Functional diversity and specificity of neostriatal interneurons. Curr Opin Neurobiol 2004; 14: 685-692.
37. Hikida T, Kaneko S, Isobe T, Kitabatake Y, Watanabe D, Pastan I et al. Increased sensitivity to cocaine by cholinergic cell ablation in nucleus accumbens. Proc Natl Acad Sci USA 2001; 98: 13351-13354.
38. Kitabatake Y, Hikida T, Watanabe D, Pastan I, Nakanishi S. Impairment of rewardrelated learning by cholinergic cell ablation in the striatum. Proc Natl Acad Sci USA 2003; 100: 7965-7970.
39. Surmeier DJ, Graybiel AM. A feud that wasn't: acetylcholine evokes dopamine release in the striatum. Neuron 2012; 75: 1-3.
40. Exley R, Cragg SJ. Presynaptic nicotinic receptors: A dynamic and diverse cholinergic filter of striatal dopamine neurotransmission. Br J Pharmacol 2008; 153: S283-S297.
41. Nelson AB, Bussert TG, Kreitzer AC, Seal RP. Striatal cholinergic neurotransmission requires VGLUT3. J Neurosci 2014; 34: 8772-8777.
42. Hikida T, Kimura K, Wada N, Funabiki K, Nakanishi S. Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior. Neuron 2010; 66: 896-907.
43. Hikida T, Yawata S, Yamaguchi T, Danjo T, Sasaoka T, Wang Y et al. Pathwayspecific modulation of nucleus accumbens in reward and aversive behavior via selective transmitter receptors. Proc Natl Acad Sci USA 2013; 110: 342-347.
44. Lobo MK, Nestler EJ. The striatal balancing act in drug addiction: distinct roles of direct and indirect pathway medium spiny neurons. Front Neuroanat 2011; 5: 41.
45. Kravitz AV, Tye LD, Kreitzer AC. Distinct roles for direct and indirect pathway striatal neurons in reinforcement. Nat Neurosci 2012; 15: 816-818.
46. Berridge KC. The debate over dopamine's role in reward: The case for incentive salience. Psychopharmacology 2007; 191: 391-431.
47. Berridge KC, Robinson TE, Aldridge JW. Dissecting components of reward: 'liking', 'wanting', and learning. Curr Opin Pharmacol 2009; 9: 65-73.
48. Kalivas PW, Volkow N, Seamans J. Unmanageable motivation in addiction: A pathology in prefrontal-accumbens glutamate transmission. Neuron 2005; 45: 647-650.
49. Wagner FA, Anthony JC. From first drug use to drug dependence; developmental periods of risk for dependence upon marijuana, cocaine, and alcohol. Neuropsychopharmacology 2002; 26: 479-488.