Understanding the role α7 nicotinic receptors play in dopamine efflux in nucleus accumbens

ACS Chemical Neuroscience

Volumn 5, Issue 10, 2014, Pages 1032-1040

  Maex, Reinoud ^a   Grinevich, Vladimir P ^b,c   Grinevich, Valentina ^c   Budygin, Evgeny ^c,d   Bencherif, Merouane ^b   Gutkin, Boris ^a,e  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b TARGACEPT INC   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

^d ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^e NATIONAL RESEARCH UNIVERSITY HIGHER SCHOOL OF ECONOMICS   (Russian Federation)

Author keywords

Acetylcholine; Desensitization; Mesolimbic pathway; Modeling; Ventral tegmental area; 7 Nicotinic receptor agonist

Indexed keywords

BUNGAROTOXIN RECEPTOR; DOPAMINE; GLUTAMIC ACID; NICOTINIC RECEPTOR BLOCKING AGENT; PARTIAL AGONIST; PNU 120596; TC 7020; UNCLASSIFIED DRUG; 1-(5-CHLORO-2,4-DIMETHOXYPHENYL)-3-(5-METHYLISOXAZOL-3-YL)UREA; 4 AMINOBUTYRIC ACID; 5-METHYL-N-(2-(PYRIDIN-3-YLMETHYL)-1-AZABICYCLO(2.2.2)OCT-3-YL)THIOPHENE-2-CARBOXAMIDE; CARBANILAMIDE DERIVATIVE; CHOLINERGIC RECEPTOR STIMULATING AGENT; ISOXAZOLE DERIVATIVE; QUINUCLIDINE DERIVATIVE; THIOPHENE DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DESENSITIZATION; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DRUG EFFECT; ELECTROCHEMICAL ANALYSIS; IN VIVO STUDY; INTERNEURON; MALE; NONHUMAN; NUCLEUS ACCUMBENS; RAT; VENTRAL TEGMENTUM; ANIMAL; BIOLOGICAL MODEL; BRAIN CORTEX; DRUG EFFECTS; METABOLISM; NERVE CELL; NERVE TRACT; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPSE;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; CEREBRAL CORTEX; CHOLINERGIC AGENTS; DOPAMINE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; ISOXAZOLES; MALE; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; NEURONS; NUCLEUS ACCUMBENS; PHENYLUREA COMPOUNDS; QUINUCLIDINES; RATS, SPRAGUE-DAWLEY; SYNAPSES; THIOPHENES;

EID: 84907998272     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn500126t     Document Type: Article

References (73)

1. Geerts, H. (2012) α7 Nicotinic receptor modulators for cognitive deficits in schizophrenia and Alzheimer's disease. Expert Opin. Invest. Drugs 21, 59-65.
2. Kucinski, A. J., Stachowiak, M. K., Wersinger, S. R., Lippiello, P. M., and Bencherif, M. (2011) Alpha7 neuronal nicotinic receptors as targets for novel therapies to treat multiple domains of schizophrenia. Curr. Pharm. Biotechnol. 12, 437-448.
3. Wallace, T. L., and Bertrand, D. (2013) Alpha7 neuronal nicotinic receptors as a drug target in schizophrenia. Expert Opin. Ther. Targets 17, 139-155.
4. Quik, M., and Wonnacott, S. (2011) α6β2∗ and α4β2∗ Nicotinic acetylcholine receptors as drug targets for Parkinson's disease. Pharmacol. Rev. 63, 938-966.
5. Zhou, F. M., Liang, Y., and Dani, J. A. (2001) Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum. Nat. Neurosci. 4, 1224-1229.
6. Brazell, M. P., Mitchell, S. N., Joseph, M. H., and Gray, J. A. (1990) Acute administration of nicotine increases the in vivo extracellular levels of dopamine, 3,4-dihydroxyphenylacetic acid and ascorbic acid preferentially in the nucleus accumbens of the rat: comparison with caudate-putamen. Neuropharmacology 29, 1177-1185.
7. Cheer, J. F., Wassum, K. M., Sombers, L. A., Heien, M. L., Ariansen, J. L., Aragona, B. J., Phillips, P. E., and Wightman, R. M. (2007) Phasic dopamine release evoked by abused substances requires cannabinoid receptor activation. J. Neurosci. 27, 791-795.
8. Mameli-Engvall, M., Evrard, A., Pons, S., Maskos, U., Svensson, T. H., Changeux, J. P., and Faure, P. (2006) Hierarchical control of dopamine neuron-firing patterns by nicotinic receptors. Neuron 50, 911-921.
9. Schilström, B., Svensson, H. M., Svensson, T. H., and Nomikos, G. G. (1998) Nicotine and food induced dopamine release in the nucleus accumbens of the rat: putative role of α7 nicotinic receptors in the ventral tegmental area. Neuroscience 85, 1005-1009.
10. Good, C. H., and Lupica, C. R. (2009) Properties of distinct ventral tegmental area synapses activated via pedunculopontine or ventral tegmental area stimulation in vitro. J. Physiol. 587, 1233-1247.
11. Taylor, D. H., Burman, P. N., Hansen, M. D., Wlcox, R. S., Larsen, B. R., Blanchard, J. K., Merrill, C. B., Edwards, J. G., Sudweeks, S. N., Wu, J., Arias, H. R., and Steffensen, S. C. (2013) Nicotine enhances the excitability of Gaba neurons in the ventral tegmental area via activation of alpha 7 nicotinic receptors on glutamate terminals. Biochem. Pharmacol. S1, No. 007.
12. Tolu, S., Eddine, R., Marti, F., David, V., Graupner, M., Pons, S., Baudonnat, M., Husson, M., Besson, M., Reperant, C., Zemdegs, J., Pages, C., Hay, Y. A., Lambolez, B., Caboche, J., Gutkin, B., Gardier, A. M., Changeux, J. P., Faure, P., and Maskos, U. (2013) Co-activation of VTA DA and GABA neurons mediates nicotine reinforcement. Mol. Psychiatry 18, 382-393.
13. Forster, G. L., and Blaha, C. D. (2000) Laterodorsal tegmental stimulation elicits dopamine efflux in the rat nucleus accumbens by activation of acetylcholine and glutamate receptors in the ventral tegmental area. Eur. J. Neurosci. 12, 3596-3604.
14. Schilström, B., Fagerquist, M. V., Zhang, X., Hertel, P., Panagis, G., Nomikos, G. G., and Svensson, T. H. (2000) Putative role of presynaptic alpha7∗ nicotinic receptors in nicotine stimulated increases of extracellular levels of glutamate and aspartate in the ventral tegmental area. Synapse 38, 375-383.
15. Cachope, R., Mateo, Y., Mathur, B. N., Irving, J., Wang, H. L., Morales, M., Lovinger, D. M., and Cheer, J. F. (2012) Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: Setting the tone for reward processing. Cell Rep. 2, 33-41.
16. Threlfell, S., Lalic, T., Platt, N. J., Jennings, K. A., Deisseroth, K., and Cragg, S. J. (2012) Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75, 58-64.
17. Koranda, J. L., Cone, J. J., McGehee, D. S., Roitman, M. F., Beeler, J. A., and Zhuang, X. (2014) Nicotinic receptors regulate the dynamic range of dopamine release in vivo. J. Neurophysiol. 111, 103-111.
18. Grilli, M., Summa, M., Salamone, A., Olivero, G., Zappettini, S., Di Prisco, S., Feligioni, M., Usai, C., Pittaluga, A., and Marchi, M. (2012) In vitro exposure to nicotine induces endocytosis of presynaptic AMPA receptors modulating dopamine release in rat nucleus accumbens nerve terminals. Neuropharmacology 63, 916-926.
19. 3H]dopamine release in rat striatal slices via glutamate release. Mol. Pharmacol. 58, 312-318.
20. Marrero, M. B., Lucas, R., Salet, C., Hauser, T. A., Mazurov, A., Lippiello, P. M., and Bencherif, M. (2010) An α7 nicotinic acetylcholine receptor-selective agonist reduces weight gain and metabolic changes in a mouse model of diabetes. J. Pharmacol. Exp. Ther. 332, 173-180.
21. Narla, S., Klejbor, I., Birkaya, B., Lee, Y. W., Morys, J., Stachowiak, E. K., Terranova, C., Bencherif, M., and Stachowiak, M. K. (2013) α7 Nicotinic receptor agonist reactivates neurogenesis in adult brain. Biochem. Pharmacol. 86, 1099-1104.
22. Kucinski, A., Syposs, C., Wersinger, S., Bencherif, M., Stachowiak, M. K., and Stachowiak, E. K. (2012) α7 Neuronal nicotinic receptor agonist (TC-7020) reverses increased striatal dopamine release during acoustic PPI testing in a transgenic mouse model of schizophrenia. Schizophr. Res. 136 82-87.
23. Garzón, M., Duffy, A. M., Chan, J., Lynch, M. K., Mackie, K., and Pickel, V. M. (2013) Dopamine D2 and acetylcholine α7 nicotinic receptors have subcellular distributions favoring mediation of convergent signaling in the mouse ventral tegmental area. Neuroscience 252, 126-143.
24. Jones, I. W., and Wonnacott, S. (2004) Precise localization of α7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area. J. Neurosci. 24, 11244-11252.
25. Livingstone, P. D., Dickinson, J. A., Srinivasan, J., Kew, J. N., and Wonnacott, S. (2010) Glutamate-dopamine crosstalk in the rat prefrontal cortex is modulated by alpha7 nicotinic receptors and potentiated by PNU-120596. J. Mol. Neurosci. 40, 172-176.
26. Yang, Y., Paspalas, C. D., Jin, L. E., Picciotto, M. R., Arnsten, A. F., and Wang, M. (2013) Nicotinic α7 receptors enhance NMDA cognitive circuits in dorsolateral prefrontal cortex. Proc. Natl. Acad. Sci. U. S. A. 110, 12078-12083.
27. Jin, Y., Yang, K., Wang, H., and Wu, J. (2011) Exposure of nicotine to ventral tegmental area slices induces glutamatergic synaptic plasticity on dopamine neurons. Synapse 65, 332-338.
28. Melis, M., Scheggi, S., Carta, G., Madeddu, C., Lecca, S., Luchicchi, A., Cadeddu, F., Frau, R., Fattore, L., Fadda, P., Ennas, M. G., Castelli, M. P., Fratta, W., Schilstrom, B., Banni, S., De Montis, M. G., and Pistis, M. (2013) PPARα regulates cholinergic-driven activity of midbrain dopamine neurons via a novel mechanism involving α7 nicotinic acetylcholine receptors. J. Neurosci. 33, 6203-6211.
29. Hurst, R. S., Hajós, M., Raggenbass, M., Wall, T. M., Higdon, N. R., Lawson, J. A., Rutherford-Root, K. L., Berkenpas, M. B., Hoffmann, W. E., Piotrowski, D. W., Groppi, V. E., Allaman, G., Ogier, R., Bertrand, S., Bertrand, D., and Arneric, S. P. (2005) A novel positive allosteric modulator of the α7 neuronal nicotinic acetylcholine receptor: in vitro and in vivo characterization. J. Neurosci. 25, 4396-4405.
30. Schilström, B., Rawal, N., Mameli-Engvall, M., Nomikos, G. G., and Svensson, T. H. (2003) Dual effects of nicotine on dopamine neurons mediated by different nicotinic receptor subtypes. Int. J. Neuropsychopharmacol. 6, 1-11.
31. Wu, J., George, A. A., Schroeder, K. M., Xu, L., Marxer-Miller, S., Lucero, L., and Lukas, R. J. (2004) Electrophysiological, pharmacological, and molecular evidence for α7-nicotinic acetylcholine receptors in rat midbrain dopamine neurons. J. Pharmacol. Exp. Ther. 311, 80-91.
32. Klink, R., de Kerchove d'Exaerde, A., Zoli, M., and Changeux, J. P. (2001) Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J. Neurosci. 21, 1452-1463.
33. Yang, K., Hu, J., Lucero, L., Liu, Q., Zheng, C., Zhen, X., Jin, G., Lukas, R. J., and Wu, J. (2009) Distinctive nicotinic acetylcholine receptor functional phenotypes of rat ventral tegmental area dopaminergic neurons. J. Physiol. 587, 345-361.
34. Grady, S. R., Salminen, O., Laverty, D. C., Whiteaker, P., McIntosh, J. M., Collins, A. C., and Marks, M. J. (2007) The subtypes of nicotinic acetylcholine receptors on dopaminergic terminals of mouse striatum. Biochem. Pharmacol. 74, 1235-1246.
35. Livingstone, P. D., and Wonnacott, S. (2009) Nicotinic acetylcholine receptors and the ascending dopamine pathways. Biochem. Pharmacol. 78, 744-755.
36. Zhang, H., and Sulzer, D. (2003) Glutamate spillover in the striatum depresses dopaminergic transmission by activating group I metabotropic glutamate receptors. J. Neurosci. 23, 10585-10592.
37. Papke, R. L., Kem, W. R., Soti, F., Lopez-Hernandez, G. Y., and Horenstein, N. A. (2009) Activation and desensitization of nicotinic α7-type acetylcholine receptors by benzylidene anabaseines and nicotine. J. Pharmacol. Exp. Ther. 329, 791-807.
38. Kalappa, B. I., and Uteshev, V. V. (2013) The dual effect of PNU-120596 on α7 nicotinic acetylcholine receptor channels. Eur. J. Pharmacol. 718, 226-234.
39. Hu, G., Duffy, P., Swanson, C., Ghasemzadeh, M. B., and Kalivas, P. W. (1999) The regulation of dopamine transmission by metabotropic glutamate receptors. J. Pharmacol. Exp. Ther. 289, 412-416.
40. van Zessen, R., Phillips, J. L., Budygin, E. A., and Stuber, G. D. (2012) Activation of VTA GABA neurons disrupts reward consumption. Neuron 73, 1184-1194.
41. Wang, Y., Sherwood, J. L., Miles, C. P., Whiffin, G., and Lodge, D. (2006) TC-2559 excites dopaminergic neurones in the ventral tegmental area by stimulating α4β2-like nicotinic acetylcholine receptors in anaesthetised rats. Br. J. Pharmacol. 147, 379-390.
42. Glowinski, J., Cheramy, A., Romo, R., and Barbeito, L. (1988) Presynaptic regulation of dopaminergic transmission in the striatum. Cell. Mol. Neurobiol. 8, 7-17.
43. Cheramy, A., Desce, J. M., Godeheu, G., and Glowinski, J. (1994) Presynaptic control of dopamine synthesis and release by excitatory amino acids in rat striatal synaptosomes. Neurochem. Int. 25, 145-154.
44. Marchi, M., Risso, F., Viola, C., Cavazzani, P., and Raiteri, M. (2002) Direct evidence that release-stimulating α7∗ nicotinic cholinergic receptors are localized on human and rat brain glutamatergic axon terminals. J. Neurochem. 80, 1071-1078.
45. Garcao, P., Oliveira, C. R., Cunha, R. A., and Agostinho, P. (2014) Subsynaptic localization of nicotinic acetylcholine receptor subunits: A comparative study in the mouse and rat striatum. Neurosci. Lett. 566, 106-110.
46. Lenoir, M., and Kiyatkin, E. A. (2013) Intravenous nicotine injection induces rapid, experience-dependent sensitization of glutamate release in the ventral tegmental area and nucleus accumbens. J. Neurochem. 127, 541-551.
47. Goldberg, J. A., and Reynolds, J. N. (2011) Spontaneous firing and evoked pauses in the tonically active cholinergic interneurons of the striatum. Neuroscience 198, 27-43.
48. Albuquerque, E. X., Pereira, E. F. R., and Alkondon, M. (2013) Tonic activation of α7 nicotinic acetylcholine receptors (nAChRs) controls glutamatergic inputs to striatal and parietal cortical neurons in guinea pig brain slices, in Society for Neuroscience Annual Meeting, p 224.01, Society for Neuroscience, San Diego, CA.
49. Wu, H. Q., Rassoulpour, A., and Schwarcz, R. (2007) Kynurenic acid leads, dopamine follows: A new case of volume transmission in the brain? J. Neural Transm. 114, 33-41.
50. Kulagina, N. V., Zigmond, M. J., and Michael, A. C. (2001) Glutamate regulates the spontaneous and evoked release of dopamine in the rat striatum. Neuroscience 102, 121-128.
51. Wang, Y., Moquin, K. F., and Michael, A. C. (2010) Evidence for coupling between steady-state and dynamic extracellular dopamine concentrations in the rat striatum. J. Neurochem. 114, 150-159.
52. Besson, M., David, V., Baudonnat, M., Cazala, P., Guilloux, J. P., Reperant, C., Cloez-Tayarani, I., Changeux, J. P., Gardier, A. M., and Granon, S. (2012) Alpha7-nicotinic receptors modulate nicotine-induced reinforcement and extracellular dopamine outflow in the mesolimbic system in mice. Psychopharmacology (Berlin, Ger.) 220, 1-14.
53. Wu, Y., Pearl, S. M., Zigmond, M. J., and Michael, A. C. (2000) Inhibitory glutamatergic regulation of evoked dopamine release in striatum. Neuroscience 96, 65-72.
54. Grinevich, V. P., O'Connor, J. A., Bencherif, M., and Budygin, E. A. (2009) Effects of nicotine on real time dopamine dynamics in rat nucleus accumbens: In vivo voltammetric study, in Society for Neuroscience Annual Meeting, p 226.12, Society for Neuroscience, Chicago.
55. Campling, B. G., Kuryatov, A., and Lindstrom, J. (2013) Acute activation, desensitization and smoldering activation of human acetylcholine receptors. PLoS One 8, No. e79653.
56. Vinson, P. N., and Justice, J. B., Jr. (1997) Effect of neostigmine on concentration and extraction fraction of acetylcholine using quantitative microdialysis. J. Neurosci. Methods 73, 61-67.
57. Arroyo, S., Bennett, C., and Hestrin, S. (2014) Nicotinic modulation of cortical circuits. Front. Neural Circuits 8, 30.
58. Owesson-White, C. A., Roitman, M. F., Sombers, L. A., Belle, A. M., Keithley, R. B., Peele, J. L., Carelli, R. M., and Wightman, R. M. (2012) Sources contributing to the average extracellular concentration of dopamine in the nucleus accumbens. J. Neurochem. 121, 252-262.
59. Zuo, P. L., Yao, W., Sun, L., Kuo, S. T., Li, Q., Wang, S. R., Dou, H. Q., Xu, H. D., Zhang, C. X., Kang, X. J., Zhou, Z., and Zhang, B. (2013) Impulse-dependent extracellular resting dopamine concentration in rat striatum in vivo. Neurochem. Int. 62, 50-57.
60. Chen, K. C., and Budygin, E. A. (2007) Extracting the basal extracellular dopamine concentrations from the evoked responses: Reanalysis of the dopamine kinetics. J. Neurosci. Methods 164, 27-42.
61. Shu, Z., Taylor, I. M., and Michael, A. C. (2013) The dopamine patchwork of the rat nucleus accumbens core. Eur. J. Neurosci. 38, 3221-3229.
62. McLean, S. L., Idris, N. F., Grayson, B., Gendle, D. F., Mackie, C., Lesage, A. S., Pemberton, D. J., and Neill, J. C. (2012) PNU-120596, a positive allosteric modulator of α7 nicotinic acetylcholine receptors, reverses a sub-chronic phencyclidine-induced cognitive deficit in the attentional set-shifting task in female rats. J. Psychopharmacol. 26, 1265-1270.
63. Turek, J. W., Kang, C. H., Campbell, J. E., Arneric, S. P., and Sullivan, J. P. (1995) A sensitive technique for the detection of the α7 neuronal nicotinic acetylcholine receptor antagonist, methyllycaconitine, in rat plasma and brain. J. Neurosci. Methods 61, 113-118.
64. Graupner, M., Maex, R., and Gutkin, B. (2013) Endogenous cholinergic inputs and local circuit mechanisms govern the phasic mesolimbic dopamine response to nicotine. PLoS Comput. Biol. 9, No. e1003183.
65. Grady, S. R., Grun, E. U., Marks, M. J., and Collins, A. C. (1997) Pharmacological comparison of transient and persistent [3H]-dopamine release from mouse striatal synaptosomes and response to chronic L-nicotine treatment. J. Pharmacol. Exp. Ther. 282, 32-43.
66. Fenster, C. P., Rains, M. F., Noerager, B., Quick, M. W., and Lester, R. A. (1997) Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentrations of nicotine. J. Neurosci. 17, 5747-5759.
67. Buisson, B., and Bertrand, D. (2001) Chronic exposure to nicotine upregulates the human α4β2 nicotinic acetylcholine receptor function. J. Neurosci. 21, 1819-1829.
68. Salminen, O., Drapeau, J. A., McIntosh, J. M., Collins, A. C., Marks, M. J., and Grady, S. R. (2007) Pharmacology of α-conotoxin MII-sensitive subtypes of nicotinic acetylcholine receptors isolated by breeding of null mutant mice. Mol. Pharmacol. 71, 1563-1571.
69. Engelman, H. S., and MacDermott, A. B. (2004) Presynaptic ionotropic receptors and control of transmitter release. Nat. Rev. Neurosci. 5, 135-145.
70. Fiorillo, C. D., and Williams, J. T. (1998) Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature 394, 78-82.
71. Grace, A. A. (1991) Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: A hypothesis for the etiology of schizophrenia. Neuroscience 41, 1-24.
72. Papke, R. L., Dwoskin, L. P., and Crooks, P. A. (2007) The pharmacological activity of nicotine and nornicotine on nAChRs subtypes: Relevance to nicotine dependence and drug discovery. J. Neurochem. 101, 160-167.
73. 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., and Marks, M. J. (2010) Structural differences determine the relative selectivity of nicotinic compounds for native α4β2∗-, α6β2∗-, α3β4∗- and α7-nicotine acetylcholine receptors. Neuropharmacology 58, 1054-1066.