Nicotine and ethanol cooperate to enhance ventral tegmental area AMPA receptor function via α6-containing nicotinic receptors

Neuropharmacology

Volumn 91, Issue , 2015, Pages 13-22

  Engle, Staci E ^a   McIntosh, J Michael ^b,c   Drenan, Ryan M ^a  

^a PURDUE UNIVERSITY   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Addiction; Alcohol; Co exposure; Dopamine; Glutamate; Nicotine

Indexed keywords

ALCOHOL; ALPHA CONOTOXIN MII; AMPA RECEPTOR; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA6; UNCLASSIFIED DRUG; VARENICLINE; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN SLICE; CONTROLLED STUDY; EMBRYO; FEMALE; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; VENTRAL TEGMENTUM; AGONISTS; ANIMAL; C57BL MOUSE; DRUG EFFECTS; METABOLISM; NERVE CELL; PHYSIOLOGY; PROTEIN SUBUNIT;

ANIMALS; ETHANOL; FEMALE; MALE; MICE; MICE, INBRED C57BL; NEURONS; NICOTINE; PROTEIN SUBUNITS; RECEPTORS, AMPA; RECEPTORS, NICOTINIC; VENTRAL TEGMENTAL AREA;

EID: 84919667056     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.11.014     Document Type: Article

References (76)

1. E. Argilli, D.R. Sibley, R.C. Malenka, P.M. England, and A. Bonci Mechanism and time course of cocaine-induced long-term potentiation in the ventral tegmental area J. Neurosci. 28 37 2008 9092 9100 10.1523/JNEUROSCI.1001-08.2008
2. L. Azam, U. Maskos, J.P. Changeux, C.D. Dowell, S. Christensen, M. De Biasi, and J.M. McIntosh α-Conotoxin BuIA[T5A;P6O]: a novel ligand that discriminates between α6β4 and α6β2 nicotinic acetylcholine receptors and blocks nicotine-stimulated norepinephrine release FASEB J. 24 2010 5113 5123 10.1096/fj.10-166272
3. J.K. Bobo Nicotine dependence and alcoholism epidemiology and treatment J. Psychoact. Drugs 24 1992 123 129
4. S.L. Borgland, R.C. Malenka, and A. Bonci Acute and chronic cocaine-induced potentiation of synaptic strength in the ventral tegmental area: electrophysiological and behavioral correlates in individual rats J. Neurosci. 24 34 2004 7482 7490 10.1523/JNEUROSCI.1312-04.2004
5. P. Calabresi, M.G. Lacey, and R.A. North Nicotinic excitation of rat ventral tegmental neurones in vitro studied by intracellular recording Br. J. Pharmacol. 98 1989 135 140
6. R. Cannady, K.R. Fisher, B. Durant, J. Besheer, and C.W. Hodge Enhanced AMPA receptor activity increases operant alcohol self-administration and cue-induced reinstatement Addict. Biol. 18 2013 54 65 10.1111/adb.12000
7. R.A. Cardoso, S.J. Brozowski, L.E. Chavez-Noriega, M. Harpold, C.F. Valenzuela, and R.A. Harris Effects of ethanol on recombinant human neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes J. Pharmacol. Exp. Ther. 289 1999 774 780
8. N. Champtiaux, C. Gotti, M. Cordero-Erausquin, D.J. David, C. Przybylski, C. Lena, F. Clementi, M. Moretti, F.M. Rossi, N. Le Novere, J.M. McIntosh, A.M. Gardier, and J.P. Changeux Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice J. Neurosci. 23 2003 7820 7829
9. A. Clark, and H.J. Little Interactions between low concentrations of ethanol and nicotine on firing rate of ventral tegmental dopamine neurones Drug Alcohol Depend. 75 2004 199 206 10.1016/j.drugalcdep.2004.03.001 S0376871604000663
10. B.N. Cohen, E.D. Mackey, S.R. Grady, S. McKinney, N.E. Patzlaff, C.R. Wageman, J.M. McIntosh, M.J. Marks, H.A. Lester, and R.M. Drenan Nicotinic cholinergic mechanisms causing elevated dopamine release and abnormal locomotor behavior Neuroscience 200 2012 31 41 10.1016/j.neuroscience.2011.10.047 S0306-4522(11)01240-1
11. M.C. Creed, N.R. Ntamati, and K.R. Tan VTA GABA neurons modulate specific learning behaviors through the control of dopamine and cholinergic systems Front. Behav. Neurosci. 8 2014 8 10.3389/fnbeh.2014.00008
12. DHHS The Health Consequences of Smoking: Nicotine Addiction: a Report of the Surgeon General 1988 Washington, D.C
13. G. Di Chiara, E. Acquas, and G. Tanda Ethanol as a neurochemical surrogate of conventional reinforcers: the dopamine-opioid link Alcohol 13 1996 13 17
14. J.R. DiFranza, and M.P. Guerrera Alcoholism and smoking J. Stud. Alcohol 51 1990 130 135
15. Y. Dong, D. Saal, M. Thomas, R. Faust, A. Bonci, T. Robinson, and R.C. Malenka Cocaine-induced potentiation of synaptic strength in dopamine neurons: behavioral correlates in GluRA(-/-) mice Proc. Natl. Acad. Sci. U. S. A. 101 2004 14282 14287 10.1073/pnas.0401553101
16. W.M. Doyon, Y. Dong, A. Ostroumov, A.M. Thomas, T.A. Zhang, and J.A. Dani Nicotine decreases ethanol-induced dopamine signaling and increases self-administration via stress hormones Neuron 79 2013 530 540 10.1016/j.neuron.2013.06.006
17. R.M. Drenan, S.R. Grady, P. Whiteaker, T. McClure-Begley, S. McKinney, J.M. Miwa, S. Bupp, N. Heintz, J.M. McIntosh, M. Bencherif, M.J. Marks, and H.A. Lester In vivo activation of midbrain dopamine neurons via sensitized, high-affinity α6∗ nicotinic acetylcholine receptors Neuron 60 2008 123 136
18. R.M. Drenan, S.R. Grady, A.D. Steele, S. McKinney, N.E. Patzlaff, J.M. McIntosh, M.J. Marks, J.M. Miwa, and H.A. Lester Cholinergic modulation of locomotion and striatal dopamine release is mediated by α6α4∗ nicotinic acetylcholine receptors J. Neurosci. 30 2010 9877 9889
19. R.M. Drenan, S.E. Engle, H.A. Lester, J.M. McIntosh, and D.H. Brunzell Activation of α6β2∗ Nicotinic Acetylcholine Receptors is Sufficient for Nicotine Reward. Program No. 455.03/P19 2012 Neuroscience Meeting Planner 2012 Society for Neuroscience New Orleans, LA Online
20. D. Engblom, A. Bilbao, C. Sanchis-Segura, L. Dahan, S. Perreau-Lenz, B. Balland, J.R. Parkitna, R. Lujan, B. Halbout, M. Mameli, R. Parlato, R. Sprengel, C. Luscher, G. Schutz, and R. Spanagel Glutamate receptors on dopamine neurons control the persistence of cocaine seeking Neuron 59 2008 497 508 10.1016/j.neuron.2008.07.010 S0896-6273(08)00582-5
21. S.E. Engle, H.J. Broderick, and R.M. Drenan Local application of drugs to study nicotinic acetylcholine receptor function in mouse brain slices J. Vis. Exp. 2012 e50034 10.3791/5003450034
22. S.E. Engle, P.Y. Shih, J.M. McIntosh, and R.M. Drenan α4α6β2∗ nicotinic acetylcholine receptor activation on ventral tegmental area dopamine neurons is sufficient to stimulate a depolarizing conductance and enhance surface AMPA receptor function Mol. Pharmacol. 84 2013 393 406 10.1124/mol.113.087346
23. M.R. Etherton, K. Tabuchi, M. Sharma, J. Ko, and T.C. Sudhof An autism-associated point mutation in the neuroligin cytoplasmic tail selectively impairs AMPA receptor-mediated synaptic transmission in hippocampus EMBO J. 30 2011 2908 2919 10.1038/emboj.2011.182
24. R. Exley, N. Maubourguet, V. David, R. Eddine, A. Evrard, S. Pons, F. Marti, S. Threlfell, P. Cazala, J.M. McIntosh, J.P. Changeux, U. Maskos, S.J. Cragg, and P. Faure Distinct contributions of nicotinic acetylcholine receptor subunit α4 and subunit α6 to the reinforcing effects of nicotine Proc. Natl. Acad. Sci. U. S. A. 108 2011 7577 7582 10.1073/pnas.1103000108
25. L.M. Fucito, B.A. Toll, R. Wu, D.M. Romano, E. Tek, and S.S. O'Malley A preliminary investigation of varenicline for heavy drinking smokers Psychopharmacology (Berl) 215 2011 655 663 10.1007/s00213-010-2160-9
26. M. Gao, Y. Jin, K. Yang, D. Zhang, R.J. Lukas, and J. Wu Mechanisms involved in systemic nicotine-induced glutamatergic synaptic plasticity on dopamine neurons in the ventral tegmental area J. Neurosci. 30 41 2010 13814 13825 10.1523/JNEUROSCI.1943-10.2010
27. S.R. Grady, R.M. Drenan, S.R. Breining, D. Yohannes, C.R. Wageman, N.B. Fedorov, S. McKinney, P. Whiteaker, M. Bencherif, H.A. Lester, and M.J. Marks Structural differences determine the relative selectivity of nicotinic compounds for native α4β2∗-, α6β2∗-, α3β4∗- and α7-nicotine acetylcholine receptors Neuropharmacology 58 2010 1054 1066
28. B.F. Grant, D.S. Hasin, S.P. Chou, F.S. Stinson, and D.A. Dawson Nicotine dependence and psychiatric disorders in the United States: results from the national epidemiologic survey on alcohol and related conditions Arch. Gen. Psychiatry 61 11 2004 1107 1115 10.1001/archpsyc.61.11.1107
29. A.W. Halff, D. Gomez-Varela, D. John, and D.K. Berg A novel mechanism for nicotinic potentiation of glutamatergic synapses J. Neurosci. 34 2014 2051 2064 10.1523/JNEUROSCI.2795-13.2014
30. E.L. Harrison, R.E. Hinson, and S.A. McKee Experimenting and daily smokers: episodic patterns of alcohol and cigarette use Addict. Behav. 34 2009 484 486 10.1016/j.addbeh.2008.12.013
31. L.M. Hendrickson, R. Zhao-Shea, X. Pang, P.D. Gardner, and A.R. Tapper Activation of α4∗ nAChRs is necessary and sufficient for varenicline-induced reduction of alcohol consumption J. Neurosci. 30 30 2010 10169 10176 10.1523/JNEUROSCI.2601-10.2010
32. J.E. Henningfield Nicotine medications for smoking cessation N. Engl. J. Med. 333 1995 1196 1203 10.1056/NEJM199511023331807
33. T.S. Hnasko, and R.H. Edwards Neurotransmitter corelease: mechanism and physiological role Annu. Rev. Physiol. 74 2012 225 243 10.1146/annurev-physiol-020911-153315
34. T.S. Hnasko, G.O. Hjelmstad, H.L. Fields, and R.H. Edwards Ventral tegmental area glutamate neurons: electrophysiological properties and projections J. Neurosci. 32 2012 15076 15085 10.1523/JNEUROSCI.3128-12.2012
35. N.R. Hoft, R.P. Corley, M.B. McQueen, D. Huizinga, S. Menard, and M.A. Ehringer SNPs in CHRNA6 and CHRNB3 are associated with alcohol consumption in a nationally representative sample Genes Brain Behav. 8 2009 631 637 10.1111/j.1601-183X.2009.00495.x GBB495
36. N.R. Hoft, R.P. Corley, M.B. McQueen, I.R. Schlaepfer, D. Huizinga, and M.A. Ehringer Genetic association of the CHRNA6 and CHRNB3 genes with tobacco dependence in a nationally representative sample Neuropsychopharmacology 34 2009 698 706 10.1038/npp.2008.122
37. Y. Jin, K. Yang, H. Wang, and J. Wu Exposure of nicotine to ventral tegmental area slices induces glutamatergic synaptic plasticity on dopamine neurons Synapse 65 2011 332 338 10.1002/syn.20850
38. J.A. Kauer, and R.C. Malenka Synaptic plasticity and addiction Nat. Rev. Neurosci. 8 2007 844 858 10.1038/nrn2234
39. A.C. King, and A.M. Epstein Alcohol dose-dependent increases in smoking urge in light smokers Alcohol Clin. Exp. Res. 29 2005 547 552
40. S. Lammel, A. Hetzel, O. Hackel, I. Jones, B. Liss, and J. Roeper Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system Neuron 57 2008 760 773
41. A. Larsson, E. Jerlhag, L. Svensson, B. Soderpalm, and J.A. Engel Is an α-conotoxin MII-sensitive mechanism involved in the neurochemical, stimulatory, and rewarding effects of ethanol? Alcohol 34 2004 239 250
42. A. Larsson, L. Edstrom, L. Svensson, B. Soderpalm, and J.A. Engel Voluntary ethanol intake increases extracellular acetylcholine levels in the ventral tegmental area in the rat Alcohol Alcohol. 40 2005 349 358 10.1093/alcalc/agh180
43. N. le Novere, M. Zoli, C. Lena, R. Ferrari, M.R. Picciotto, E. Merlo-Pich, and J.P. Changeux Involvement of α6 nicotinic receptor subunit in nicotine-elicited locomotion, demonstrated by in vivo antisense oligonucleotide infusion Neuroreport 10 1999 2497 2501
44. C. Lena, A. de Kerchove D'Exaerde, M. Cordero-Erausquin, N. Le Novere, M. del Mar Arroyo-Jimenez, and J.P. Changeux Diversity and distribution of nicotinic acetylcholine receptors in the locus ceruleus neurons Proc. Natl. Acad. Sci. U. S. A. 96 1999 12126 12131
45. L. Liu, R. Zhao-Shea, J.M. McIntosh, P. Gardner, and A. Tapper Nicotine persistently activates ventral tegmental area dopaminergic neurons via nicotinic acetylcholine receptors containing α4 and α6 subunits Mol. Pharmacol. 2012 10.1124/mol.111.076661
46. L. Liu, L.M. Hendrickson, M.J. Guildford, R. Zhao-Shea, P.D. Gardner, and A.R. Tapper Nicotinic acetylcholine receptors containing the α4 subunit modulate alcohol reward Biol. Psychiatry 73 2013 738 746 10.1016/j.biopsych.2012.09.019
47. E. Lof, P. Olausson, A. deBejczy, R. Stomberg, J.M. McIntosh, J.R. Taylor, and B. Soderpalm Nicotinic acetylcholine receptors in the ventral tegmental area mediate the dopamine activating and reinforcing properties of ethanol cues Psychopharmacology (Berl) 195 2007 333 343 10.1007/s00213-007-0899-4
48. C. Luscher, and R.C. Malenka Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling Neuron 69 2011 650 663 10.1016/j.neuron.2011.01.017 S0896-6273(11)00065-1
49. E.D. Mackey, S.E. Engle, M.R. Kim, H.C. O'Neill, C.R. Wageman, N.E. Patzlaff, Y. Wang, S.R. Grady, J.M. McIntosh, M.J. Marks, H.A. Lester, and R.M. Drenan α6∗ nicotinic acetylcholine receptor expression and function in a visual salience circuit J. Neurosci. 32 30 2012 10226 10237 10.1523/JNEUROSCI.0007-12.2012
50. D. Mao, K. Gallagher, and D.S. McGehee Nicotine potentiation of excitatory inputs to ventral tegmental area dopamine neurons J. Neurosci. 31 18 2011 6710 6720 10.1523/JNEUROSCI.5671-10.2011
51. L.M. Marubio, A.M. Gardier, S. Durier, D. David, R. Klink, M.M. Arroyo-Jimenez, J.M. McIntosh, F. Rossi, N. Champtiaux, M. Zoli, and J.P. Changeux Effects of nicotine in the dopaminergic system of mice lacking the α4 subunit of neuronal nicotinic acetylcholine receptors Eur. J. Neurosci. 17 2003 1329 1337
52. S.A. McKee, E.L. Harrison, S.S. O'Malley, S. Krishnan-Sarin, J. Shi, J.M. Tetrault, M.R. Picciotto, I.L. Petrakis, N. Estevez, and E. Balchunas Varenicline reduces alcohol self-administration in heavy-drinking smokers Biol. Psychiatry 66 2009 185 190 10.1016/j.biopsych.2009.01.029
53. A.K. Mehta, and M.K. Ticku Ethanol potentiation of GABAergic transmission in cultured spinal cord neurons involves gamma-aminobutyric acidA-gated chloride channels J. Pharmacol. Exp. Ther. 246 1988 558 564
54. N.S. Miller, and M.S. Gold Comorbid cigarette and alcohol addiction: epidemiology and treatment J. Addict. Dis. 17 1998 55 66 10.1300/J069v17n01-06
55. S.H. Mitchell, H. de Wit, and J.P. Zacny Effects of varying ethanol dose on cigarette consumption in healthy normal volunteers Behav. Pharmacol. 6 1995 359 365
56. J.M. Mitchell, C.H. Teague, A.S. Kayser, S.E. Bartlett, and H.L. Fields Varenicline decreases alcohol consumption in heavy-drinking smokers Psychopharmacology (Berl) 223 2012 299 306 10.1007/s00213-012-2717-x
57. R. Nashmi, C. Xiao, P. Deshpande, S. McKinney, S.R. Grady, P. Whiteaker, Q. Huang, T. McClure-Begley, J.M. Lindstrom, C. Labarca, A.C. Collins, M.J. Marks, and H.A. Lester Chronic nicotine cell specifically upregulates functional α4∗ nicotinic receptors: basis for both tolerance in midbrain and enhanced long-term potentiation in perforant path J. Neurosci. 27 2007 8202 8218
58. S. Pons, L. Fattore, G. Cossu, S. Tolu, E. Porcu, J.M. McIntosh, J.P. Changeux, U. Maskos, and W. Fratta Crucial role of α4 and α6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration J. Neurosci. 28 2008 12318 12327
59. M.S. Powers, H.J. Broderick, R.M. Drenan, and J.A. Chester Nicotinic acetylcholine receptors containing α6 subunits contribute to alcohol reward-related behaviours Genes Brain Behav. 12 2013 543 553 10.1111/gbb.12042
60. H. Rollema, L.K. Chambers, J.W. Coe, J. Glowa, R.S. Hurst, L.A. Lebel, Y. Lu, R.S. Mansbach, R.J. Mather, C.C. Rovetti, S.B. Sands, E. Schaeffer, D.W. Schulz, F.D. Tingley 3rd, and K.E. Williams Pharmacological profile of the α4β2 nicotinic acetylcholine receptor partial agonist varenicline, an effective smoking cessation aid Neuropharmacology 52 2007 985 994 10.1016/j.neuropharm.2006.10.016
61. J.E. Rose, L.H. Brauer, F.M. Behm, M. Cramblett, K. Calkins, and D. Lawhon Psychopharmacological interactions between nicotine and ethanol Nicotine Tob. Res. 6 2004 133 144 10.1080/14622200310001656957
62. S.A. Ross, J.Y. Wong, J.J. Clifford, A. Kinsella, J.S. Massalas, M.K. Horne, I.E. Scheffer, I. Kola, J.L. Waddington, S.F. Berkovic, and J. Drago Phenotypic characterization of an α4 neuronal nicotinic acetylcholine receptor subunit knock-out mouse J. Neurosci. 20 2000 6431 6441
63. D. Saal, Y. Dong, A. Bonci, and R.C. Malenka Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons Neuron 37 2003 577 582 S0896627303000217
64. O. Salminen, K.L. Murphy, J.M. McIntosh, J. Drago, M.J. Marks, A.C. Collins, and S.R. Grady Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice Mol. Pharmacol. 65 2004 1526 1535
65. O. Salminen, J.A. Drapeau, J.M. McIntosh, A.C. Collins, M.J. Marks, and S.R. Grady Pharmacology of α-conotoxin MII-sensitive subtypes of nicotinic acetylcholine receptors isolated by breeding of null mutant mice Mol. Pharmacol. 71 2007 1563 1571
66. G.J. Schaefer, and R.P. Michael Interactions between alcohol and nicotine on intracranial self-stimulation and locomotor activity in rats Drug Alcohol Depend. 30 1992 37 47
67. R. Spanagel, A. Herz, and T.S. Shippenberg Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway Proc. Natl. Acad. Sci. U. S. A. 89 1992 2046 2050
68. P. Steensland, J.A. Simms, J. Holgate, J.K. Richards, and S.E. Bartlett Varenicline, an α4β2 nicotinic acetylcholine receptor partial agonist, selectively decreases ethanol consumption and seeking Proc. Natl. Acad. Sci. U. S. A. 104 2007 12518 12523 10.1073/pnas.0705368104
69. G.D. Stuber, F.W. Hopf, J. Hahn, S.L. Cho, A. Guillory, and A. Bonci Voluntary ethanol intake enhances excitatory synaptic strength in the ventral tegmental area Alcohol Clin. Exp. Res. 32 2008 1714 1720 10.1111/j.1530-0277.2008.00749.x
70. D. Sulzer, M.P. Joyce, L. Lin, D. Geldwert, S.N. Haber, T. Hattori, and S. Rayport Dopamine neurons make glutamatergic synapses in vitro J. Neurosci. 18 1998 4588 4602
71. A.R. Tapper, S.L. McKinney, R. Nashmi, J. Schwarz, P. Deshpande, C. Labarca, P. Whiteaker, M.J. Marks, A.C. Collins, and H.A. Lester Nicotine activation of α4∗ receptors: sufficient for reward, tolerance, and sensitization Science 306 2004 1029 1032
72. Y. Tizabi, R.L. Copeland Jr., V.A. Louis, and R.E. Taylor Effects of combined systemic alcohol and central nicotine administration into ventral tegmental area on dopamine release in the nucleus accumbens Alcohol Clin. Exp. Res. 26 2002 394 399
73. 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 10.1038/3507907735079077
74. 125I]-α-Conotoxin MII identifies a novel nicotinic acetylcholine receptor population in mouse brain Mol. Pharmacol. 57 2000 913 925
75. WHO Department of Mental Health and Substance Abuse, Global Status Report on Alcohol 2011 2011 World Health Organization Department of Mental Health and Substance Abuse Geneva
76. Y. Zuo, K. Nagata, J.Z. Yeh, and T. Narahashi Single-channel analyses of ethanol modulation of neuronal nicotinic acetylcholine receptors Alcohol Clin. Exp. Res. 28 2004 688 696 00000374-200405000-00002