Nicotinic cholinergic mechanisms causing elevated dopamine release and abnormal locomotor behavior

Neuroscience

Volumn 200, Issue , 2012, Pages 31-41

  Cohen, B N ^a   Mackey, E D W ^a   Grady, S R ^b   Mckinney, S ^a   Patzlaff, N E ^b   Wageman, C R ^b   Mcintosh, J M ^c   Marks, M J ^b   Lester, H A ^a   Drenan, R M ^a,d  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF COLORADO   (United States)

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

^d PURDUE UNIVERSITY   (United States)

Author keywords

Acetylcholine; Cholinergic; Dopamine; Mouse; Nicotinic; Transgenic

Indexed keywords

DOPAMINE; LEUCINE; MUTANT PROTEIN; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA6; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SYNAPTOSOME; CHOLINERGIC SYSTEM; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE COURSE; DOPAMINE RELEASE; DOPAMINERGIC TRANSMISSION; GENE DUPLICATION; HYPERACTIVITY; HYPERSENSITIVITY; LOCOMOTION; MOTOR ACTIVITY; MOUSE; MOUSE STRAIN; MUSCLE CONTRACTION; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RUNNING; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CORPUS STRIATUM; DOPAMINE; EXPLORATORY BEHAVIOR; HYPERKINESIS; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; MUTATION; RECEPTORS, NICOTINIC; SYNAPTOSOMES; TIME FACTORS;

EID: 84855206570     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.10.047     Document Type: Article

References (40)

1. Azam L., Winzer-Serhan U.H., Chen Y., Leslie F.M. Expression of neuronal nicotinic acetylcholine receptor subunit mRNAs within midbrain dopamine neurons. J Comp Neurol 2002, 444:260-274.
2. Ballester M., Castelló A., Ibáñez E., Sánchez A., Folch J.M. Real-time quantitative PCR-based system for determining transgene copy number in transgenic animals. BioTechniques 2004, 37:610-613.
3. Brunzell D.H., Boschen K.E., Hendrick E.S., Beardsley P.M., McIntosh J.M. α-conotoxin MII-sensitive nicotinic acetylcholine receptors in the nucleus accumbens shell regulate progressive ratio responding maintained by nicotine. Neuropsychopharmacology 2010, 35:665-673.
4. Cartier G.E., Yoshikami D., Gray W.R., Luo S., Olivera B.M., McIntosh J.M. A new alpha-conotoxin which targets α3β2 nicotinic acetylcholine receptors. J Biol Chem 1996, 271:7522-7528.
5. Champtiaux N., Gotti C., Cordero-Erausquin M., David D.J., Przybylski C., Léna C., Clementi F., Moretti M., Rossi F.M., Le Novère N., McIntosh J.M., Gardier A.M., Changeux J.P. Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J Neurosci 2003, 23:7820-7829.
6. Champtiaux N., Han Z.Y., Bessis A., Rossi F.M., Zoli M., Marubio L., McIntosh J.M., Changeux J.P. Distribution and pharmacology of α6-containing nicotinic acetylcholine receptors analyzed with mutant mice. J Neurosci 2002, 22:1208-1217.
7. Cui C., Booker T.K., Allen R.S., Grady S.R., Whiteaker P., Marks M.J., Salminen O., Tritto T., Butt C.M., Allen W.R., Stitzel J.A., McIntosh J.M., Boulter J., Collins A.C., Heinemann S.F. The β3 nicotinic receptor subunit: a component of α-conotoxin MII-binding nicotinic acetylcholine receptors that modulate dopamine release and related behaviors. J Neurosci 2003, 23:11045-11053.
8. Day J., Damsma G., Fibiger H.C. Cholinergic activity in the rat hippocampus, cortex and striatum correlates with locomotor activity: an in vivo microdialysis study. Pharmacol Biochem Behav 1991, 38:723-729.
9. Drenan R.M., Grady S.R., Steele A.D., McKinney S., Patzlaff N.E., McIntosh J.M., Marks M.J., Miwa J.M., Lester H.A. Cholinergic modulation of locomotion and striatal dopamine release is mediated by α6α4* nicotinic acetylcholine receptors. J Neurosci 2010, 30:9877-9889.
10. Drenan R.M., Grady S.R., Whiteaker P., McClure-Begley T., McKinney S., Miwa J.M., Bupp S., Heintz N., McIntosh J.M., Bencherif M., Marks M.J., Lester H.A. In vivo activation of midbrain dopamine neurons via sensitized, high-affinity α6* nicotinic acetylcholine receptors. Neuron 2008, 60:123-136.
11. Exley R., Maubourguet N., David V., Eddine R., Evrard A., Pons S., Marti F., Threlfell S., Cazala P., McIntosh J.M., Changeux J.P., Maskos U., Cragg S.J., Faure P. Distinct contributions of nicotinic acetylcholine receptor subunit α4 and subunit α6 to the reinforcing effects of nicotine. Proc Natl Acad Sci U S A 2011, 108:7577-7582.
12. Fonck C., Cohen B.N., Nashmi R., Whiteaker P., Wagenaar D.A., Rodrigues-Pinguet N., Deshpande P., McKinney S., Kwoh S., Munoz J., Labarca C., Collins A.C., Marks M.J., Lester H.A. Novel seizure phenotype and sleep disruptions in knock-in mice with hypersensitive α4* nicotinic receptors. J Neurosci 2005, 25:11396-11411.
13. Giros B., Jaber M., Jones S.R., Wightman R.M., Caron M.G. Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 1996, 379:606-612.
14. Gotti C., Guiducci S., Tedesco V., Corbioli S., Zanetti L., Moretti M., Zanardi A., Rimondini R., Mugnaini M., Clementi F., Chiamulera C., Zoli M. Nicotinic acetylcholine receptors in the mesolimbic pathway: primary role of ventral tegmental area α6β2* receptors in mediating systemic nicotine effects on dopamine release, locomotion, and reinforcement. J Neurosci 2010, 30:5311-5325.
15. Gotti C., Moretti M., Clementi F., Riganti L., McIntosh J.M., Collins A.C., Marks M.J., Whiteaker P. Expression of nigrostriatal α6-containing nicotinic acetylcholine receptors is selectively reduced, but not eliminated, by β3 subunit gene deletion. Mol Pharmacol 2005, 67:2007-2015.
16. Grady S.R., Drenan R.M., Breining S.R., Yohannes D., Wageman C.R., Fedorov N.B., McKinney S., Whiteaker P., Bencherif M., Lester H.A., Marks M.J. Structural differences determine the relative selectivity of nicotinic compounds for native α4β2*-, α6β2*-, α3β4*- and α7-nicotine acetylcholine receptors. Neuropharmacology 2010, 58:1054-1066.
17. Grady S.R., Murphy K.L., Cao J., Marks M.J., McIntosh J.M., Collins A.C. Characterization of nicotinic agonist-induced [3H]dopamine release from synaptosomes prepared from four mouse brain regions. J Pharmacol Exp Ther 2002, 301:651-660.
18. Ikemoto S. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 2007, 56:27-78.
19. Kametani H., Kawamura H. Alterations in acetylcholine release in the rat hippocampus during sleep-wakefulness detected by intracerebral dialysis. Life Sci 1990, 47:421-426.
20. Kulak J.M., Nguyen T.A., Olivera B.M., McIntosh J.M. α-conotoxin MII blocks nicotine-stimulated dopamine release in rat striatal synaptosomes. J Neurosci 1997, 17:5263-5270.
21. Labarca C., Nowak M.W., Zhang H., Tang L., Deshpande P., Lester H.A. Channel gating governed symmetrically by conserved leucine residues in the M2 domain of nicotinic receptors. Nature 1995, 376:514-516.
22. Labarca C., Schwarz J., Deshpande P., Schwarz S., Nowak M.W., Fonck C., Nashmi R., Kofuji P., Dang H., Shi W., Fidan M., Khakh B.S., Chen Z., Bowers B.J., Boulter J., Wehner J.M., Lester H.A. Point mutant mice with hypersensitive α4 nicotinic receptors show dopaminergic deficits and increased anxiety. Proc Natl Acad Sci U S A 2001, 98:2786-2791.
23. Lee C., Kim J., Shin S.G., Hwang S. Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli. J Biotechnol 2006, 123:273-280.
24. Léna C., de Kerchove D'Exaerde A., Cordero-Erausquin M., Le Novère N., del Mar Arroyo-Jimenez M., Changeux J.P. Diversity and distribution of nicotinic acetylcholine receptors in the locus ceruleus neurons. Proc Natl Acad Sci U S A 1999, 96:12126-12131.
25. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
26. Mizuno T., Endo Y., Arita J., Kimura F. Acetylcholine release in the rat hippocampus as measured by the microdialysis method correlates with motor activity and exhibits a diurnal variation. Neuroscience 1991, 44:607-612.
27. Nashmi R., Xiao C., Deshpande P., McKinney S., Grady S.R., Whiteaker P., Huang Q., McClure-Begley T., Lindstrom J.M., Labarca C., Collins A.C., Marks M.J., Lester H.A. 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 2007, 27:8202-8218.
28. Picciotto M.R., Zoli M., Rimondini R., Léna C., Marubio L.M., Pich E.M., Fuxe K., Changeux J.P. Acetylcholine receptors containing the β2 subunit are involved in the reinforcing properties of nicotine. Nature 1998, 391:173-177.
29. Pons S., Fattore L., Cossu G., Tolu S., Porcu E., McIntosh J.M., Changeux J.P., Maskos U., Fratta W. Crucial role of α4 and α6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration. J Neurosci 2008, 28:12318-12327.
30. Quik M., McIntosh J.M. Striatal α6* nicotinic acetylcholine receptors: potential targets for Parkinson's disease therapy. J Pharmacol Exp Ther 2006, 316:481-489.
31. Rhodes J.S., Gammie S.C., Garland T. Neurobiology of mice selected for high voluntary wheel-running activity. Integr Comp Biol 2005, 45:438-455.
32. Salminen O., Drapeau J.A., McIntosh J.M., Collins A.C., Marks M.J., Grady S.R. Pharmacology of α-conotoxin MII-sensitive subtypes of nicotinic acetylcholine receptors isolated by breeding of null mutant mice. Mol Pharmacol 2007, 71:1563-1571.
33. Salminen O., Murphy K.L., McIntosh J.M., Drago J., Marks M.J., Collins A.C., Grady S.R. Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice. Mol Pharmacol 2004, 65:1526-1535.
34. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3:1101-1108.
35. Tapper A.R., McKinney S.L., Marks M.J., Lester H.A. Nicotine responses in hypersensitive and knockout α4 mice account for tolerance to both hypothermia and locomotor suppression in wild-type mice. Physiol Genomics 2007, 31:422-428.
36. Tsai H.C., Zhang F., Adamantidis A., Stuber G.D., Bonci A., de Lecea L., Deisseroth K. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 2009, 324:1080-1084.
37. Voorn P., Vanderschuren L.J., Groenewegen H.J., Robbins T.W., Pennartz C.M. Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci 2004, 27:468-474.
38. Whiteaker P., McIntosh J.M., Luo S., Collins A.C., Marks M.J. 125I-α-conotoxin MII identifies a novel nicotinic acetylcholine receptor population in mouse brain. Mol Pharmacol 2000, 57:913-925.
39. Yang K., Buhlman L., Khan G.M., Nichols R.A., Jin G., McIntosh J.M., Whiteaker P., Lukas R.J., Wu J. Functional nicotinic acetylcholine receptors containing α6 subunits are on GABAergic neuronal boutons adherent to ventral tegmental area dopamine neurons. J Neurosci 2011, 31:2537-2548.
40. Zhuang X., Oosting R.S., Jones S.R., Gainetdinov R.R., Miller G.W., Caron M.G., Hen R. Hyperactivity and impaired response habituation in hyperdopaminergic mice. Proc Natl Acad Sci U S A 2001, 98:1982-1987.