Sustained impairment of α2A-adrenergic autoreceptor signaling mediates neurochemical and behavioral sensitization to amphetamine

Biological Psychiatry

Volumn 74, Issue 2, 2013, Pages 90-98

  Doucet, Emilie L ^a   Bobadilla, Ana Clara ^a   Houades, Vanessa ^a   Lanteri, Christophe ^a   Godeheu, Gérard ^a   Lanfumey, Laurence ^b   Sara, Susan J ^c   Tassin, Jean Pol ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b CENTRE DE PSYCHIATRIE ET NEUROSCIENCES   (France)

^c Collège de France ^*  (France)

Author keywords

G i proteins; in vivo microdialysis; locus coeruleus cell recording; neurochemical sensitization; norepinephrine; psychostimulants

Indexed keywords

ALPHA 2A ADRENERGIC RECEPTOR; AMPHETAMINE; AUTORECEPTOR; CLONIDINE; EFAROXAN; NORADRENALIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BEHAVIORAL SENSITIZATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; INTRACELLULAR SIGNALING; LOCUS CERULEUS; MALE; MICRODIALYSIS; MOUSE; NERVE CELL; NEUROCHEMISTRY; NONHUMAN; NORADRENERGIC NERVE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSITIZATION; WESTERN BLOTTING;

ADRENERGIC ALPHA-2 RECEPTOR ANTAGONISTS; AMPHETAMINE; ANIMALS; AUTORECEPTORS; CENTRAL NERVOUS SYSTEM SENSITIZATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; LOCUS COERULEUS; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; NEURONS; NOREPINEPHRINE; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-2;

EID: 84879506877     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2012.11.029     Document Type: Article

References (46)

1. J.D. Steketee, and P.W. Kalivas Drug wanting: Behavioral sensitization and relapse to drug-seeking behavior Pharmacol Rev 63 2011 348 365
2. T.E. Robinson, and K.C. Berridge The neural basis of drug craving: An incentive-sensitization theory of addiction Brain Res Brain Res Rev 18 1993 247 291
3. C. Lanteri, S.J. Hernández Vallejo, L. Salomon, E.L. Doucet, G. Godeheu, and Y. Torrens Inhibition of monoamine oxidases desensitizes 5-HT1A autoreceptors and allows nicotine to induce a neurochemical and behavioral sensitization J Neurosci 29 2009 987 997
4. C. Lanteri, L. Salomon, Y. Torrens, J. Glowinski, and J.P. Tassin Drugs of abuse specifically sensitize noradrenergic and serotonergic neurons via a non-dopaminergic mechanism Neuropsychopharmacology 33 2008 1724 1734
5. L. Salomon, C. Lanteri, J. Glowinski, and J.P. Tassin Behavioral sensitization to amphetamine results from an uncoupling between noradrenergic and serotonergic neurons Proc Natl Acad Sci U S A 103 2006 7476 7481
6. S.E. Loughlin, S.L. Foote, and J.H. Fallon Locus coeruleus projections to cortex: Topography, morphology and collateralization Brain Res Bull 9 1982 287 294
7. J.M. Cedarbaum, and G.K. Aghajanian Catecholamine receptors on locus coeruleus neurons: Pharmacological characterization Eur J Pharmacol 44 1977 375 385
8. J.T. Williams, G. Henderson, and R.A. North Characterization of alpha 2-adrenoceptors which increase potassium conductance in rat locus coeruleus neurones Neuroscience 14 1985 95 101
9. G.K. Aghajanian, and C.P. VanderMaelen alpha 2-adrenoceptor-mediated hyperpolarization of locus coeruleus neurons: Intracellular studies in vivo Science 215 1982 1394 1396
10. J. Juhila, A. Honkanen, J. Sallinen, A. Haapalinna, E. Korpi, and M. Scheinin alpha(2A)-Adrenoceptors regulate d-amphetamine-induced hyperactivity and behavioural sensitization in mice Eur J Pharmacol 517 2005 74 83
11. G. Gobbi, T. Cassano, F. Radja, M.G. Morgese, V. Cuomo, and L. Santarelli Neurokinin 1 receptor antagonism requires norepinephrine to increase serotonin function Eur Neuropsychopharmacol 17 2007 328 338
12. A. Bortolozzi, M. Amargós-Bosch, A. Adell, L. Díaz-Mataix, J. Serrats, and S. Pons In vivo modulation of 5-hydroxytryptamine release in mouse prefrontal cortex by local 5-HT(2A) receptors: Effect of antipsychotic drugs Eur J Neurosci 18 2003 1235 1246
13. S. Bouret, A. Duvel, S. Onat, and S.J. Sara Phasic activation of locus ceruleus neurons by the central nucleus of the amygdala J Neurosci 23 2003 3491 3497
14. G. Paxinos, and K.B.J. Franklin The Mouse Brain in Stereotaxic Coordinates 2nd ed. 1997 Academic Press New York
15. S.J. Sara, and M. Segal Plasticity of sensory responses of locus coeruleus neurons in the behaving rat: Implications for cognition Prog Brain Res 88 1991 571 585
16. T.H. Svensson, B.S. Bunney, and G.K. Aghajanian Inhibition of both noradrenergic and serotonergic neurons in brain by the alpha-adrenergic agonist clonidine Brain Res 92 1975 291 306
17. C. Dyon-Laurent, A. Hervé, and S.J. Sara Noradrenergic hyperactivity in hippocampus after partial denervation: pharmacological, behavioral, and electrophysiological studies Exp Brain Res 99 1994 259 266
18. J. Albarrán-Juárez, R. Gilsbach, R.P. Piekorz, K. Pexa, N. Beetz, and J. Schneider Modulation of alpha2-adrenoceptor functions by heterotrimeric Galphai protein isoforms J Pharmacol Exp Ther 331 2009 35 44
19. J.P. Tassin Uncoupling between noradrenergic and serotonergic neurons as a molecular basis of stable changes in behavior induced by repeated drugs of abuse Biochem Pharmacol 75 2008 85 97
20. J. Jasper, J. Lesnick, L. Chang, S. Yamanishi, T. Chang, and S. Hsu Ligand efficacy and potency at recombinant alpha2 adrenergic receptors: Agonist-mediated [35S]GTPgammaS binding Biochem Pharmacol 55 1998 1035 1043
21. M. Gollasch, J. Hescheler, K. Spicher, F.J. Klinz, G. Schultz, and W. Rosenthal Inhibition of Ca2+ channels via alpha 2-adrenergic and muscarinic receptors in pheochromocytoma (PC-12) cells Am J Physiol 260 1991 C1282 C1289
22. S.Y. Song, K. Saito, K. Noguchi, and S. Konishi Adrenergic and cholinergic inhibition of Ca2+ channels mediated by different GTP-binding proteins in rat sympathetic neurones Pflugers Arch 418 1991 592 600
23. E.J. Nestler, R.Z. Terwilliger, J.R. Walker, K.A. Sevarino, and R.S. Duman Chronic cocaine treatment decreases levels of the G protein subunits Gi alpha and Go alpha in discrete regions of rat brain J Neurochem 55 1990 1079 1082
24. C.D. Striplin, and P.W. Kalivas Robustness of G protein changes in cocaine sensitization shown with immunoblotting Synapse 14 1993 10 15
25. C.A. Crawford, F.Y. Choi, J.L. Kohutek, S.T. Yoshida, and S.A. McDougall Changes in PKA activity and Gs alpha and Golf alpha levels after amphetamine- and cocaine-induced behavioral sensitization Synapse 51 2004 241 248
26. E.R. McLeman, J.J. Warsh, L. Ang, P.P. Li, K.S. Kalasinsky, and B.M. Ross The human nucleus accumbens is highly susceptible to G protein down-regulation by methamphetamine and heroin J Neurochem 74 2000 2120 2126
27. M. Nishio, Y. Kanda, K. Mizuno, and Y. Watanabe Methamphetamine increases the hippocampal alpha(2A)-adrenergic receptor and Galpha(o) in mice Neurosci Lett 334 2002 145 148
28. E.J. Nestler, J.J. Erdos, R. Terwilliger, R.S. Duman, and J.F. Tallman Regulation of G proteins by chronic morphine in the rat locus coeruleus Brain Res 476 1989 230 239
29. H. Iwasa, S. Kikuchi, S. Hasegawa, K. Suzuki, and T. Sato Alteration of G protein subclass mRNAs in methamphetamine-induced behavioral sensitization Ann N Y Acad Sci 801 1996 110 115
30. Q.H. Li, K. Nakadate, S. Tanaka-Nakadate, D. Nakatsuka, Y. Cui, and Y. Watanabe Unique expression patterns of 5-HT2A and 5-HT2C receptors in the rat brain during postnatal development: Western blot and immunohistochemical analyses J Comp Neurol 469 2004 128 140
31. N. Haddjeri, C. de Montigny, and P. Blier Modulation of the firing activity of noradrenergic neurones in the rat locus coeruleus by the 5-hydroxtryptamine system Br J Pharmacol 120 1997 865 875
32. K.S. Murthy, J.R. Grider, and G.M. Makhlouf Heterologous desensitization of response mediated by selective PKC-dependent phosphorylation of G(i-1) and G(i-2) Am J Physiol Cell Physiol 279 2000 C925 C934
33. V. Di Marzo, D. Vial, P. Sokoloff, J.C. Schwartz, and D. Piomelli Selection of alternative G-mediated signaling pathways at the dopamine D2 receptor by protein kinase C J Neurosci 13 1993 4846 4853
34. K. Sasaki, S. Kawasaki, S. Kimura, R. Fujita, K. Takashima, and M. Matsumoto Functional uncoupling between the receptor and G-protein as the result of PKC activation, observed in Aplysia neurons Jpn J Physiol 47 1997 241 249
35. T.M. Quinton, S. Kim, C. Dangelmaier, R.T. Dorsam, J. Jin, and J.L. Daniel Protein kinase C- and calcium-regulated pathways independently synergize with Gi pathways in agonist-induced fibrinogen receptor activation Biochem J 368 2002 535 543
36. J.D. Elsworth, B.A. Morrow, V.T. Nguyen, J. Mitra, M.R. Picciotto, and R.H. Roth Prenatal cocaine exposure enhances responsivity of locus coeruleus norepinephrine neurons: Role of autoreceptors Neuroscience 147 2007 419 427
37. C.A. Jiménez-Rivera, M. Feliu-Mojer, and R. Vázquez-Torres Alpha-noradrenergic receptors modulate the development and expression of cocaine sensitization Ann N Y Acad Sci 1074 2006 390 402
38. S.J. Sara, and A. Hervé-Minvielle Inhibitory influence of frontal cortex on locus coeruleus neurons Proc Natl Acad Sci U S A 92 1995 6032 6036
39. E. Jodo, C. Chiang, and G. Aston-Jones Potent excitatory influence of prefrontal cortex activity on noradrenergic locus coeruleus neurons Neuroscience 83 1998 63 79
40. G. Aston-Jones, M. Ennis, V.A. Pieribone, W.T. Nickell, and M.T. Shipley The brain nucleus locus coeruleus: Restricted afferent control of a broad efferent network Science 234 1986 734 737
41. P.W. Kalivas, N. Volkow, and J. Seamans Unmanageable motivation in addiction: A pathology in prefrontal-accumbens glutamate transmission Neuron 45 2005 647 650
42. D.G. Winder, R.E. Egli, N.L. Schramm, and R.T. Matthews Synaptic plasticity in drug reward circuitry Curr Mol Med 2 2002 667 676
43. K.L. Conrad, K.Y. Tseng, J.L. Uejima, J.M. Reimers, L.J. Heng, and Y. Shaham Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving Nature 454 2008 118 121
44. M.A. Ungless, J.L. Whistler, R.C. Malenka, and A. Bonci Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons Nature 411 2001 583 587
45. J.A. Kauer, and R.C. Malenka Synaptic plasticity and addiction Nat Rev Neurosci 8 2007 844 858
46. M.E. Wolf, X. Sun, S. Mangiavacchi, and S.Z. Chao Psychomotor stimulants and neuronal plasticity Neuropharmacology 47 suppl 1 2004 61 79