The necessity of α4 nicotinic receptors in nicotine-driven behaviors: Dissociation between reinforcing and motor effects of nicotine

Neuropsychopharmacology

Volumn 36, Issue 7, 2011, Pages 1505-1517

  Cahir, Elizabeth ^a   Pillidge, Katie ^a   Drago, John ^a,b   Lawrence, Andrew J ^a,b  

^a FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

4 subunit; locomotor; nicotine; operant self administration; reinforcement

Indexed keywords

MECAMYLAMINE; NICOTINE; NICOTINE RECEPTOR ALPHA 4; NICOTINIC RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG SELF ADMINISTRATION; GENE DELETION; HYPERACTIVITY; LOCOMOTION; MALE; MOTOR ACTIVITY; MOUSE; NONHUMAN; PLACE PREFERENCE; POINT MUTATION; PRIORITY JOURNAL; PSYCHOMOTOR ACTIVITY; REINFORCEMENT; WILD TYPE;

ANIMALS; CONDITIONING, OPERANT; CUES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; EXCITATORY AMINO ACID ANTAGONISTS; KETAMINE; LOCOMOTION; MECAMYLAMINE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; RECEPTORS, NICOTINIC; REINFORCEMENT (PSYCHOLOGY); SELF ADMINISTRATION;

EID: 79956016650     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2011.35     Document Type: Article

References (61)

1. Azam L, Winzer-Serhan UH, Chen Y, Leslie FM (2002). Expression of neuronal nicotinic acetylcholine receptor subunit mRNAs within midbrain dopamine neurons. J Comp Neurol 444: 260-274. (Pubitemid 34117090)
2. Bilkei-Gorzo A, Racz I, Michel K, Darvas M, Maldonado R, Zimmer A (2008). A common genetic predisposition to stress sensitivity and stress-induced nicotine craving. Biol Psychiatry 63: 164-171. (Pubitemid 350299314)
3. Brown RM, Short JL, Cowen MS, Ledent C, Lawrence AJ (2009). A differential role for the adenosine A(2A) receptor in opiate reinforcement vs opiate-seeking behavior. Neuropsychopharma-cology 34: 844-856.
4. Brunzell DH, Boschen KE, Hendrick ES, Beardsley PM, McIntosh JM (2010). alpha-Conotoxin MII-sensitive nicotinic acetylcholine receptors in the nucleus accumbens shell regulate progressive ratio responding maintained by nicotine. Neuropsychopharma-cology 35: 665-673.
5. Brunzell DH, Chang JR, Schneider B, Olausson P, Taylor JR, Picciotto MR (2006). beta2-Subunit-containing nicotinic acetylcholine receptors are involved in nicotine-induced increases in conditioned reinforcement but not progressive ratio responding for food in C57BL/6 mice. Psychopharmacology (Berl) 184: 328-338. (Pubitemid 43255849)
6. Champtiaux N, Gotti C, Cordero-Erausquin M, David DJ, Przybylski C, Lena C et al (2003). Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J Neurosci 23: 7820-7829. (Pubitemid 37055453)
7. Champtiaux N, Han ZY, Bessis A, Rossi FM, Zoli M, Marubio L et al (2002). Distribution and pharmacology of alpha 6-contain-ing nicotinic acetylcholine receptors analyzed with mutant mice. J Neurosci 22: 1208-1217. (Pubitemid 34163722)
8. Changeux JP (2010). Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat Rev Neurosci 11: 389-401.
9. Corrigall WA (1999). Nicotine self-administration in animals as a dependence model. Nicotine Tob Res 1: 11-20.
10. Corrigall WA, Coen KM, Adamson KL (1994). Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res 653: 278-284. (Pubitemid 24252850)
11. Corrigall WA, Franklin KB, Coen KM, Clarke PB (1992). The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine. Psychopharmacology (Berl) 107: 285-289.
12. Criswell HE, Ridings A (1983). Intravenous self-administration of morphine by naive mice. Pharmacol Biochem Behav 18: 467-470. (Pubitemid 13146908)
13. Dani JA, Bertrand D (2007). Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu Rev Pharmacol Toxicol 47: 699-729.
14. Debruyne D, Sobrio F, Hinschberger A, Camsonne R, Coquerel A, Barre L (2003). Short-term pharmacokinetics and brain distribution of mecamylamine as a preliminary to carbon-11 labeling for nicotinic receptor investigation. J Pharm Sci 92: 1051-1057. (Pubitemid 36523451)
15. Doggrell SA (2007). Which is the best primary medication for long-term smoking cessation-nicotine replacement therapy, bupropion or varenicline? Expert Opin Pharmacother 8: 2903-2915. (Pubitemid 350285009)
16. Drago J, McColl CD, Horne MK, Finkelstein DI, Ross SA (2003). Neuronal nicotinic receptors: insights gained from gene knockout and knockin mutant mice. Cell Mol Life Sci 60: 1267-1280. (Pubitemid 36900512)
17. Drenan RM, Grady SR, Steele AD, McKinney S, Patzlaff NE, McIntosh JM et al (2010). Cholinergic modulation of locomotion and striatal dopamine release is mediated by alpha6alpha4* nicotinic acetylcholine receptors. J Neurosci 30: 9877-9889.
18. Drenan RM, Grady SR, Whiteaker P, McClure-Begley T, McKinney S, Miwa JM et al (2008). In vivo activation of midbrain dopamine neurons via sensitized, high-affinity alpha 6 nicotinic acetylcho-line receptors. Neuron 60: 123-136.
19. Epping-Jordan MP, Picciotto MR, Changeux JP, Pich EM (1999). Assessment of nicotinic acetylcholine receptor subunit contributions to nicotine self-administration in mutant mice. Psychopharmacology (Berl) 147: 25-26. (Pubitemid 30010017)
20. Fowler CD, Lu Q, Johnson PM, Marks MJ, Kenny PJ (2011). Habenular alpha5 nicotinic receptor subunit signalling controls nicotine intake. Nature (e-pub ahead of print).
21. George O, Lloyd A, Carroll FI, Damaj MI, Koob GF (2010). Varenicline blocks nicotine intake in rats with extended access to nicotine self-administration. Psychopharmacology (Berl) 213: 715-722.
22. Gotti C, Clementi F, Fornari A, Gaimarri A, Guiducci S, Manfredi I et al (2009). Structural and functional diversity of native brain neuronal nicotinic receptors. Biochem Pharmacol 78: 703-711.
23. Gotti C, Moretti M, Clementi F, Riganti L, McIntosh JM, Collins AC et al (2005). Expression of nigrostriatal alpha 6-containing nicotinic acetylcholine receptors is selectively reduced, but not eliminated, by beta 3 subunit gene deletion. Mol Pharmacol 67: 2007-2015. (Pubitemid 41007782)
24. Gotti C, Zoli M, Clementi F (2006). Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmacol Sci 27: 482-491. (Pubitemid 44251225)
25. Grady SR, Salminen O, Laverty DC, Whiteaker P, McIntosh JM, Collins AC et al (2007). The subtypes of nicotinic acetylcholine receptors on dopaminergic terminals of mouse striatum. Biochem Pharmacol 74: 1235-1246. (Pubitemid 47417935)
26. Grady SR, Salminen O, McIntosh JM, Marks MJ, Collins AC (2009). Mouse striatal dopamine nerve terminals express alpha4alpha5-beta2 and two stoichiometric forms of alpha4beta2*-nicotinic acetylcholine receptors. J Mol Neurosci 40: 91-95.
27. Jackson KJ, McIntosh JM, Brunzell DH, Sanjakdar SS, Damaj MI (2009). The role of alpha6-containing nicotinic acetylcholine receptors in nicotine reward and withdrawal. J Pharmacol Exp Ther 331: 547-554.
28. Klink R, de Kerchove d'Exaerde A, Zoli M, Changeux JP (2001). Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 21: 1452-1463. (Pubitemid 32182187)
29. Lam S, Patel PN (2007). Varenicline: a selective alpha4beta2 nicotinic acetylcholine receptor partial agonist approved for smoking cessation. Cardiol Rev 15: 154-161. (Pubitemid 46626069)
30. Le Novere N, Zoli M, Changeux JP (1996). Neuronal nicotinic receptor alpha 6 subunit mRNA is selectively concentrated in catecholaminergic nuclei of the rat brain. Eur J Neurosci 8: 2428-2439. (Pubitemid 26387904)
31. le Novere N, Zoli M, Lena C, Ferrari R, Picciotto MR, Merlo-Pich E et al (1999). Involvement of alpha6 nicotinic receptor subunit in nicotine-elicited locomotion, demonstrated by in vivo antisense oligonucleotide infusion. Neuroreport 10: 2497-2501. (Pubitemid 29418126)
32. Li MD, Beuten J, Ma JZ, Payne TJ, Lou XY, Garcia V et al (2005). Ethnic- and gender-specific association of the nicotinic acet-ylcholine receptor alpha4 subunit gene (CHRNA4) with nicotine dependence. Hum Mol Genet 14: 1211-1219. (Pubitemid 40613909)
33. Martin-Garcia E, Barbano MF, Galeote L, Maldonado R (2008). New operant model of nicotine-seeking behaviour in mice. Int J Neuropsychopharmacol 12: 343-356.
34. Marubio LM, del Mar Arroyo-Jimenez M, Cordero-Erausquin M, Lena C, Le Novere N, de Kerchove d'Exaerde A et al (1999). Reduced antinociception in mice lacking neuronal nicotinic receptor subunits. Nature 398: 805-810.
35. Marubio LM, Gardier AM, Durier S, David D, Klink R, Arroyo-Jimenez MM et al (2003). Effects of nicotine in the dopaminergic system of mice lacking the alpha4 subunit of neuronal nicotinic acetylcholine receptors. Eur J Neurosci 17: 1329-1337. (Pubitemid 36560833)
36. Maskos U, Molles BE, Pons S, Besson M, Guiard BP, Guilloux JP et al (2005). Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 436: 103-107. (Pubitemid 40966193)
37. McCallum SE, Collins AC, Paylor R, Marks MJ (2006). Deletion of the beta 2 nicotinic acetylcholine receptor subunit alters development of tolerance to nicotine and eliminates receptor upregulation. Psychopharmacology (Berl) 184: 314-327. (Pubitemid 43255848)
38. McGehee DS, Role LW (1995). Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu Rev Physiol 57: 521-546.
39. McPherson CS, Mantamadiotis T, Tan SS, Lawrence AJ (2010). Deletion of CREB1 from the dorsal telencephalon reduces motivational properties of cocaine. Cereb Cortex 20: 941-952.
40. Metaxas A, Bailey A, Barbano MF, Galeote L, Maldonado R, Kitchen I (2010). Differential region-specific regulation of alpha4beta2* nAChRs by self-administered and non-contingent nicotine in C57BL/6J mice. Addict Biol 15: 464-479.
41. Nashmi R, Xiao C, Deshpande P, McKinney S, Grady SR, Whiteaker P et al (2007). Chronic nicotine cell specifically upregulates functional alpha 4* nicotinic receptors: basis for both tolerance in midbrain and enhanced long-term potentiation in perforant path. J Neurosci 27: 8202-8218. (Pubitemid 47219619)
42. Olsen CM, Winder DG (2009). Operant sensation seeking engages similar neural substrates to operant drug seeking in C57 mice. Neuropsychopharmacology 34: 1685-1694.
43. Papke RL, Dwoskin LP, Crooks PA, Zheng G, Zhang Z, McIntosh JM et al (2008). Extending the analysis of nicotinic receptor antagonists with the study of alpha6 nicotinic receptor subunit chimeras. Neuropharmacology 54: 1189-1200.
44. Papke RL, Sanberg PR, Shytle RD (2001). Analysis of mecamy-lamine stereoisomers on human nicotinic receptor subtypes. J Pharmacol Exp Ther 297: 646-656. (Pubitemid 32377996)
45. Papke RL, Wecker L, Stitzel JA (2010). Activation and inhibition of mouse muscle and neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes. J Pharmacol Exp Ther 333: 501-518.
46. Petersen DR, Norris KJ, Thompson JA (1984). A comparative study of the disposition of nicotine and its metabolites in three inbred strains of mice. Drug Metab Dispos 12: 725-731. (Pubitemid 15222677)
47. Picciotto MR, Zoli M, Lena C, Bessis A, Lallemand Y, Le Novere N et al (1995). Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain. Nature 374: 65-67.
48. Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, Pich EM et al (1998). Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 391: 173-177. (Pubitemid 28092475)
49. Pons S, Fattore L, Cossu G, Tolu S, Porcu E, McIntosh JM et al (2008). Crucial role of {alpha}4 and {alpha}6 nicotinic acetylcho-line receptor subunits from ventral tegmental area in systemic nicotine self-administration. J Neurosci 28: 12318-12327.
50. Rasmussen T, Swedberg MD (1998). Reinforcing effects of nicotinic compounds: intravenous self-administration in drug-naive mice. Pharmacol Biochem Behav 60: 567-573. (Pubitemid 28282700)
51. Robinson TE, Berridge KC (2008). Review. The incentive sensitization theory of addiction: some current issues. Philos Trans R Soc Lond B Biol Sci 363: 3137-3146.
52. Rollema H, Coe JW, Chambers LK, Hurst RS, Stahl SM, Williams KE (2007). Rationale, pharmacology and clinical efficacy of partial agonists of alpha(4)beta(2) nACh receptors for smoking cessation. Trends Pharmacol Sci 28: 316-325. (Pubitemid 47016686)
53. Ross SA, Wong JY, Clifford JJ, Kinsella A, Massalas JS, Horne MK et al (2000). Phenotypic characterization of an alpha 4 neuronal nicotinic acetylcholine receptor subunit knock-out mouse. J Neurosci 20: 6431-6441.
54. Scheffer IE, Bhatia KP, Lopes-Cendes I, Fish DR, Marsden CD, Andermann E et al (1995). Autosomal dominant nocturnal frontal lobe epilepsy. A distinctive clinical disorder. Brain 118(Part 1): 61-73.
55. Tapper AR, McKinney SL, Marks MJ, Lester HA (2007). Nicotine responses in hypersensitive and knockout {alpha}4 mice account for tolerance to both hypothermia and locomotor suppression in wild-type mice. Physiol Genomics 31: 422-428. (Pubitemid 350127782)
56. Tapper AR, McKinney SL, Nashmi R, Schwarz J, Deshpande P, Labarca C et al (2004). Nicotine activation of alpha4* receptors: sufficient for reward, tolerance, and sensitization. Science 306: 1029-1032. (Pubitemid 39482905)
57. Teper Y, Whyte D, Cahir E, Lester HA, Grady SR, Marks MJ et al (2007). Nicotine-induced dystonic arousal complex in a mouse line harboring a human autosomal-dominant nocturnal frontal lobe epilepsy mutation. J Neurosci 27: 10128-10142. (Pubitemid 47450462)
58. Tritto T, McCallum SE, Waddle SA, Hutton SR, Paylor R, Collins AC et al (2004). Null mutant analysis of responses to nicotine: deletion of beta2 nicotinic acetylcholine receptor subunit but not alpha7 subunit reduces sensitivity to nicotine-induced locomo-tor depression and hypothermia. Nicotine Tob Res 6: 145-158.
59. Walters CL, Brown S, Changeux JP, Martin B, Damaj MI (2006). The beta2 but not alpha7 subunit of the nicotinic acetylcholine receptor is required for nicotine-conditioned place preference in mice. Psychopharmacology (Berl) 184: 339-344. (Pubitemid 43255850)
60. WHO (2008). MPOWER: A policy package to reverse the tobacco epidemic. World Health Organization. WHO: Geneva, Switzerland.
61. Xiao C, Nashmi R, McKinney S, Cai H, McIntosh JM, Lester HA (2009). Chronic nicotine selectively enhances alpha4beta2* nicotinic acetylcholine receptors in the nigrostriatal dopamine pathway. J Neurosci 29: 12428-12439.