Cholinergic modulation of locomotion and striatal dopamine release is mediated by α6α4* nicotinic acetylcholine receptors

Journal of Neuroscience

Volumn 30, Issue 29, 2010, Pages 9877-9889

  Drenan, Ryan M ^a   Grady, Sharon R ^b   Steele, Andrew D ^a   McKinney, Sheri ^a   Patzlaff, Natalie E ^b   McIntosh, J Michael ^c,d   Marks, Michael J ^b   Miwa, Julie M ^a   Lester, Henry A ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

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

^d UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE TRANSPORTER; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA6ALPHA4; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN SYNAPTOSOME; CHOLINERGIC SYSTEM; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE RELEASE; DOPAMINERGIC TRANSMISSION; DRINKING; ELECTROCHEMISTRY; FEMALE; GROOMING; HANGING; HYPERACTIVITY; IN VITRO STUDY; LOCOMOTION; MALE; MOBILIZATION; MOUSE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; REARING; WALKING;

ANIMALS; CORPUS STRIATUM; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; GANGLIONIC STIMULANTS; HYPERKINESIS; LOCOMOTION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; NICOTINE; RECEPTORS, DOPAMINE; RECEPTORS, NICOTINIC; SYNAPTOSOMES;

EID: 77954836905     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2056-10.2010     Document Type: Article

References (59)

1. Akopian G, Crawford C, Beal MF, Cappelletti M, Jakowec MW, Petzinger GM, Zheng L, Gheorghe SL, Reichel CM, Chow R, Walsh JP (2008) Decreased striatal dopamine release underlies increased expression of long-term synaptic potentiation at corticostriatal synapses 24 h after 3-nitropropionic-acid- induced chemical hypoxia. J Neurosci 28:9585-9597.
2. 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.
3. Bayer HM, Glimcher PW (2005) Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 47:129-141.
4. Bordia T, Campos C, McIntosh JM, Quik M (2010) Nicotinic receptor-mediated reduction in L-dopa-induced dyskinesias may occur via desensitization. J Pharmacol Exp Ther 333:929-938.
5. Brown RW, Collins AC, Lindstrom JM, Whiteaker P (2007) Nicotinic α5 subunit deletion locally reduces high-affinity agonist activation without altering nicotinic receptor numbers. J Neurochem 103:204-215.
6. Cartier GE, Yoshikami D, Gray WR, Luo S, Olivera BM, McIntosh JM (1996) A new α-conotoxin which targets α3β2 nicotinic acetylcholine receptors. J Biol Chem 271:7522-7528.
7. Champtiaux N, Han ZY, Bessis A, Rossi FM, Zoli M, Marubio L, McIntosh JM, Changeux JP (2002) Distribution and pharmacology of α6-containing nicotinic acetylcholine receptors analyzed with mutant mice. J Neurosci 22:1208-1217.
8. Champtiaux N, Gotti C, Cordero-Erausquin M, David DJ, Przybylski C, Léna C, Clementi F, Moretti M, Rossi FM, Le Novère N, McIntosh JM, Gardier AM, Changeux JP (2003) Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J Neurosci 23:7820-7829.
9. Chergui K, Suaud-Chagny MF, Gonon F (1994) Nonlinear relationship between impulse flow, dopamine release and dopamine elimination in the rat brain in vivo. Neuroscience 62:641-645. (Pubitemid 2143081)
10. Coe JW, Brooks PR, Vetelino MG, Wirtz MC, Arnold EP, Huang J, Sands SB, Davis TI, Lebel LA, Fox CB, Shrikhande A, Heym JH, Schaeffer E, Rollema H, Lu Y, Mansbach RS, Chambers LK, Rovetti CC, Schulz DW, Tingley FD 3rd, et al. (2005) Varenicline: an α4β2 nicotinic receptor partial agonist for smoking cessation. J Med Chem 48:3474-3477.
11. Cragg SJ (2003) Variable dopamine release probability and short-term plasticity between functional domains of the primate striatum. J Neurosci 23:4378-4385.
12. Cui C, Booker TK, Allen RS, Grady SR, Whiteaker P, Marks MJ, Salminen O, Tritto T, Butt CM, Allen WR, Stitzel JA, McIntosh JM, Boulter J, Collins AC, Heinemann SF (2003) The β3 nicotinic receptor subunit: a component of α-Conotoxin MII-binding nicotinic acetylcholine receptors that modulate dopamine release and related behaviors. J Neurosci 23:11045-11053.
13. Drenan RM, Nashmi R, Imoukhuede P, Just H, McKinney S, Lester HA (2008a) Subcellular trafficking, pentameric assembly, and subunit stoichiometry of neuronal nicotinic acetylcholine receptors containing fluorescently labeled α6 and β3 subunits. Mol Pharmacol 73:27-41.
14. Drenan RM, Grady SR, Whiteaker P, McClure-Begley T, McKinney S, Miwa JM, Bupp S, Heintz N, McIntosh JM, Bencherif M, Marks MJ, Lester HA (2008b) In vivo activation of midbrain dopamine neurons via sensitized, high-affinity α6* nicotinic acetylcholine receptors. Neuron 60:123-136.
15. Exley R, Cragg SJ (2008) Presynaptic nicotinic receptors: a dynamic and diverse cholinergic filter of striatal dopamine neurotransmission. Br J Pharmacol 153 [Suppl 1]:S283-S297.
16. Exley R, Clements MA, Hartung H, McIntosh JM, Cragg SJ (2008) α6-containing nicotinic acetylcholine receptors dominate the nicotine control of dopamine neurotransmission in nucleus accumbens. Neuropsychopharmacology 33:2158-2166. (Pubitemid 351992087)
17. Gahring LC, Persiyanov K, Rogers SW (2004) Neuronal and astrocyte expression of nicotinic receptor subunit β4 in the adult mouse brain. J Comp Neurol 468:322-333.
18. Giros B, Jaber M, Jones SR, Wightman RM, Caron MG (1996) Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379:606-612.
19. Gotti C, Moretti M, Clementi F, Riganti L, McIntosh JM, Collins AC, Marks MJ, Whiteaker P (2005) Expression of nigrostriatal α6-containing nicotinic acetylcholine receptors is selectively reduced, but not eliminated, by β3 subunit gene deletion. Mol Pharmacol 67:2007-2015.
20. 3H]dopamine release from synaptosomes prepared from four mouse brain regions. J Pharmacol Exp Ther 301:651-660.
21. Huang CL, Chen HC, Huang NK, Yang DM, Kao LS, Chen JC, Lai HL, Chern Y (1999) Modulation of dopamine transporter activity by nicotinic acetylcholine receptors and membrane depolarization in rat pheochromocytoma PC12 cells. J Neurochem 72:2437-2444.
22. Hyland BI, Reynolds JN, Hay J, Perk CG, Miller R (2002) Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 114:475-492.
23. Ikemoto S (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56:27-78.
24. 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.
25. Kole MH, Letzkus JJ, Stuart GJ (2007) Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 55:633-647.
26. Labarca C, Nowak MW, Zhang H, Tang L, Deshpande P, Lester HA (1995) Channel gating governed symmetrically by conserved leucine residues in the M2 domain of nicotinic receptors. Nature 376:514-516.
27. Lammel S, Hetzel A, Häckel O, Jones I, Liss B, Roeper J (2008) Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57:760-773. (Pubitemid 351335346)
28. Lança AJ, Adamson KL, Coen KM, Chow BL, Corrigall WA (2000) The pedunculopontine tegmental nucleus and the role of cholinergic neurons in nicotine self-administration in the rat: a correlative neuroanatomical and behavioral study. Neuroscience 96:735-742.
29. 3H]epibatidine. Mol Pharmacol 70:947-959.
30. Marubio LM, Gardier AM, Durier S, David D, Klink R, Arroyo-Jimenez MM, McIntosh JM, Rossi F, Champtiaux N, Zoli M, Changeux JP (2003) Effects of nicotine in the dopaminergic system of mice lacking the α4 subunit of neuronal nicotinic acetylcholine receptors. Eur J Neurosci 17:1329-1337.
31. Maskos U, Molles BE, Pons S, Besson M, Guiard BP, Guilloux JP, Evrard A, Cazala P, Cormier A, Mameli-Engvall M, Dufour N, Cloëz-Tayarani I, Bemelmans AP, Mallet J, Gardier AM, David V, Faure P, Granon S, Changeux JP (2005) Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 436:103-107.
32. Michael DJ, Wightman RM (1999) Electrochemical monitoring of biogenic amine neurotransmission in real time. J Pharm Biomed Anal 19:33-46.
33. Nashmi R, Xiao C, Deshpande P, McKinney S, Grady SR, Whiteaker P, Huang Q, McClure-Begley T, Lindstrom JM, Labarca C, Collins AC, Marks MJ, Lester HA (2007) 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 27:8202-8218.
34. Parish CL, Nunan J, Finkelstein DI, McNamara FN, Wong JY, Waddington JL, Brown RM, Lawrence AJ, Horne MK, Drago J (2005) Mice lacking the α4 nicotinic receptor subunit fail to modulate dopaminergic neuronal arbors and possess impaired dopamine transporter function. Mol Pharmacol 68:1376-1386.
35. Picciotto MR, Zoli M, Rimondini R, Léna C, Marubio LM, Pich EM, Fuxe K, Changeux JP (1998) Acetylcholine receptors containing the β2 subunit are involved in the reinforcing properties of nicotine. Nature 391:173-177.
36. Quik M, McIntosh JM (2006) Striatal α6* nicotinic acetylcholine receptors: potential targets for Parkinson's disease therapy. J Pharmacol Exp Ther 316:481-489.
37. Quik M, O'Leary K, Tanner CM (2008) Nicotine and Parkinson's disease: implications for therapy. Mov Disord 23:1641-1652.
38. Rice ME, Cragg SJ (2004) Nicotine amplifies reward-related dopamine signals in striatum. Nat Neurosci 7:583-584.
39. Rice ME, Cragg SJ (2008) Dopamine spillover after quantal release: rethinking dopamine transmission in the nigrostriatal pathway. Brain Res Rev 58:303-313.
40. Ross SA, Wong JY, Clifford JJ, Kinsella A, Massalas JS, Horne MK, Scheffer IE, Kola I, Waddington JL, Berkovic SF, Drago J (2000) Phenotypic characterization of an α4 neuronal nicotinic acetylcholine receptor subunit knock-out mouse. J Neurosci 20:6431-6441.
41. Salminen O, Murphy KL, McIntosh JM, Drago J, Marks MJ, Collins AC, Grady SR (2004) Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice. Mol Pharmacol 65:1526-1535.
42. Salminen O, Whiteaker P, Grady SR, Collins AC, McIntosh JM, Marks MJ (2005) The subunit composition and pharmacology of α-Conotoxin MII-binding nicotinic acetylcholine receptors studied by a novel membrane-binding assay. Neuropharmacology 48:696-705. (Pubitemid 40462409)
43. Salminen O, Drapeau JA, McIntosh JM, Collins AC, Marks MJ, Grady SR (2007) Pharmacology of α-conotoxin MII-sensitive subtypes of nicotinic acetylcholine receptors isolated by breeding of null mutant mice. Mol Pharmacol 71:1563-1571.
44. Schmitz Y, Schmauss C, Sulzer D (2002) Altered dopamine release and uptake kinetics in mice lacking D2 receptors. J Neurosci 22:8002-8009.
45. Schulte A, Chow RH (1996) A simple method for insulating carbon-fiber microelectrodes using anodic electrophoretic deposition of paint. Anal Chem 68:3054-3058. (Pubitemid 126462435)
46. Senior SL, Ninkina N, Deacon R, Bannerman D, Buchman VL, Cragg SJ, Wade-Martins R (2008) Increased striatal dopamine release and hyperdopaminergic-like behaviour in mice lacking both alpha-synuclein and gamma-synuclein. Eur J Neurosci 27:947-957.
47. Shu Y, Hasenstaub A, Duque A, Yu Y, McCormick DA (2006) Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature 441:761-765.
48. Steele AD, Jackson WS, King OD, Lindquist S (2007) The power of automated high-resolution behavior analysis revealed by its application to mouse models of Huntington's and prion diseases. Proc Natl Acad Sci U S A 104:1983-1988.
49. Steele AD, Hutter G, Jackson WS, Heppner FL, Borkowski AW, King OD, Raymond GJ, Aguzzi A, Lindquist S (2008) Heat shock factor 1 regulates lifespan as distinct from disease onset in prion disease. Proc Natl Acad Sci U S A 105:13626-13631.
50. Tapper AR, McKinney SL, Marks MJ, Lester HA (2007) Nicotine responses in hypersensitive and knockout α4 mice account for tolerance to both hypothermia and locomotor suppression in wild-type mice. Physiol Genomics 31:422-428.
51. Threlfell S, Clements MA, Khodai T, Pienaar IS, Exley R, Wess J, Cragg SJ (2010) Striatal muscarinic receptors promote activity dependence of dopamine transmission via distinct receptor subtypes on cholinergic interneurons in ventral versus dorsal striatum. J Neurosci 30:3398-3408.
52. Tsai HC, Zhang F, Adamantidis A, Stuber GD, Bonci A, de Lecea L, Deisseroth K (2009) Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324:1080-1084.
53. Xiao C, Nashmi R, McKinney S, Cai H, McIntosh JM, Lester HA (2009) Chronic nicotine selectively enhances α4β2* nicotinic acetylcholine receptors in the nigrostriatal dopamine pathway. J Neurosci 29:12428-12439.
54. Zhang H, Sulzer D (2004) Frequency-dependent modulation of dopamine release by nicotine. Nat Neurosci 7:581-582.
55. Zhang T, Zhang L, Liang Y, Siapas AG, Zhou FM, Dani JA (2009) Dopamine signaling differences in the nucleus accumbens and dorsal striatum exploited by nicotine. J Neurosci 29:4035-4043.
56. Zhou FM, Liang Y, Dani JA (2001) Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat Neurosci 4:1224-1229.
57. Zhou FM, Liang Y, Salas R, Zhang L, De Biasi M, Dani JA (2005) Corelease of dopamine and serotonin from striatal dopamine terminals. Neuron 46:65-74.
58. Zhuang X, Oosting RS, Jones SR, Gainetdinov RR, Miller GW, Caron MG, Hen R (2001) Hyperactivity and impaired response habituation in hyperdopaminergic mice. Proc Natl Acad Sci U S A 98:1982-1987.
59. Zweifel LS, Parker JG, Lobb CJ, Rainwater A, Wall VZ, Fadok JP, Darvas M, Kim MJ, Mizumori SJ, Paladini CA, Phillips PE, Palmiter RD (2009) Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc Natl Acad Sci U S A 106:7281-7288.