Nicotinic and dopamine D2 receptors mediate nicotine-induced changes in ventral tegmental area neurotensin system

European Journal of Pharmacology

Volumn 573, Issue 1-3, 2007, Pages 124-132

  Alburges, Mario E ^a   Hoonakker, Amanda J ^a   Hanson, Glen R ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

Dopamine; Mecamylamine; Metenkephalin; Neurotensin; Nicotine; Non alpha 7 nicotinic receptor; Substance P; Ventral tegmental area

Indexed keywords

8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; DOPAMINE 1 RECEPTOR BLOCKING AGENT; DOPAMINE 2 RECEPTOR; DOPAMINE 2 RECEPTOR BLOCKING AGENT; ETICLOPRIDE; MECAMYLAMINE; NEUROPEPTIDE; NEUROTENSIN; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR BLOCKING AGENT; DOPAMINE 1 RECEPTOR; NEUROTENSIN-LIKE IMMUNOREACTIVITY; SALICYLAMIDE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINE RELEASE; DRUG ABUSE; DRUG MEGADOSE; IMMUNOREACTIVITY; LIMBIC CORTEX; MALE; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUCLEUS ACCUMBENS; PEPTIDE ANALYSIS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; STRIATE CORTEX; SUBSTANTIA NIGRA; TOBACCO DEPENDENCE; VENTRAL TEGMENTUM; ANIMAL; BASAL GANGLION; CORPUS STRIATUM; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; INTRAPERITONEAL DRUG ADMINISTRATION; NEUROTENSIN LIKE ACTIVITY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SUBCUTANEOUS DRUG ADMINISTRATION; TEGMENTUM;

(R)-2,3,4,5-TETRAHYDRO-8-CHLORO-3-METHYL-5-PHENYL-1H-3-BENZAZEPIN-7-OL; ANIMALS; BASAL GANGLIA; CORPUS STRIATUM; DOSE-RESPONSE RELATIONSHIP, DRUG; INJECTIONS, INTRAPERITONEAL; INJECTIONS, SUBCUTANEOUS; MALE; MECAMYLAMINE; NEUROPEPTIDES; NEUROTENSIN; NICOTINE; NICOTINIC ANTAGONISTS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; SALICYLAMIDES; TEGMENTUM MESENCEPHALI;

EID: 34648844243     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2007.06.063     Document Type: Article

References (68)

1. Aghajanian G.K., and Bunney B.S. Dopamine 'autoreceptors': pharmacological characterization by microiontophoretic single cell recording studies. Naunyn-Schmiedeberg's Arch. Pharmacol. 297 (1977) 1-7
2. Alburges M.E., Keefe K.A., and Hanson G.R. Unique responses of limbic met-enkephalin systems to low and high doses of methamphetamine. Brain Res. 905 (2001) 120-126
3. Alburges M.E., Keefe K.A., and Hanson G.R. Contrasting response by basal ganglia metenkephalin systems to low and high doses of methamphetamine in a rat model. J. Neurochem. 76 (2001) 721-729
4. Boules M., Iversen I., Oliveros A., Shaw A., Williams K., Robinson J., Fredrickson P., and Richelson E. The neurotensin receptor agonist NT69L suppresses sucrose-reinforced operate behavior in the rat. Brain Res. 1127 (2007) 90-98
5. Bradford M.M. A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
6. Cador M., Rivet J., Kelley A., Le Moal M., and Stinus L. Substance P, neurotensin and enkephalin injections into the ventral tegmental area: comparative study on dopamine turnover in several forebrain structures. Brain Res. 486 (1989) 357-363
7. Cao Y.J., Surowy C.S., and Puttfarcken P.S. Different nicotinic acetylcholine receptor subtypes mediating striatal and prefrontal cortical [3H]dopamine release. Neuropharmacology 48 (2005) 72-79
8. Chen Y., Sharples T.J., Phillips K.G., Benedetti G., Broad L.N., Zwart R., and Shor E. The nicotine alpha 4 beta 2 receptor selective agonist, TC-2559, increases DA neuronal activity in VTA of rat midbrain slices. Neuropharmacology 45 (2003) 334-344
9. David V., Besson M., Changeux J., Granon S., and Cazala P. Reinforcing effects of nicotine microinjections into the ventral tegmental area of mice: dependence on cholinergic nicotinic and dopaminergic D1 receptors. Neuropharmacology 50 (2006) 1030-1040
10. Di Chiara G., and Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 5272-5278
11. Dearry A., Gingrich J., Falardeau R., Bates M., and Caron M. Molecular cloning and expression of the genes for a human D1 dopamine receptor. Nature (Lond.) 347 (1990) 72-76
12. Emmett S., and Greenfield S. Correlation between dopaminergic neurons, acetylcholinesterase and nicotinic acetylcholine receptors containing the alpha 3- or alpha 5-subunit in the rat substantia nigra. J. Chem. Neuroanat. 30 (2005) 34-44
13. Ferrari R., Le Novera N., Picciotto M.R., Changeux J.P., and Zoli M. Acute and long-term changes in the mesolimbic dopamine pathway after systemic or local single nicotine injections. Eur. J. Neurosci. 15 (2002) 1810-1818
14. Fredrickson P., Boules M., Yerbury S., and Richelson E. Blockade of nicotine-induced locomotor sensitization by a novel neurotensin analog in rats. Eur. J. Pharmacol. 458 (2003) 111-118
15. Geisler S., and Zahm D.S. Neurotensin afferents of the ventral tegmental area in the rat: [1] re-examination of their origins and [2] responses to acute psychostimulant and antipsychotic drug administration. Eur. J. Neurosci. 24 (2006) 116-134
16. George T.P., Verrico C.D., Picciotto M.R., and Roth R.H. Nicotinic modulation of mesoprefrontal dopamine neurons: pharmacology and neuroanatomic characterization. J. Pharmacol. Exp. Ther. 295 (2000) 58-66
17. Glimcher P., Giovino A., and Hoebel B. Neurotensin self injection in the ventral tegmental area. Brain Res. 403 (1987) 147-150
18. Gygi S., Gibb J.W., and Hanson G.R. Differential effects of antipsychotic and psychotomimetic drugs on neurotensin systems of discrete extrapyramidal and limbic regions. J. Pharmacol. Exp. Ther. 270 (1994) 192-197
19. Hanson G.R., Smiley P., Johnson M., Letter A., Bush L., and Gibb J.W. Response of neurotensin systems of the basal ganglia to cocaine treatment. Eur. J. Pharmacol. 160 (1989) 23-30
20. Hanson G.R., Singh N., Merchant K., Johnson M., Bush L., and Gibb J.W. Responses of limbic and extrapyramidal neurotensin systems to stimulants of abuse. Involvement of dopaminergic mechanism. Ann. N.Y. Acad. Sci. 668 (1992) 165-172
21. Hanson G.R., Bush L.G., Taylor V.L., Gibb J.W., Davis K., and Schmidt C.J. Comparison of neurotensin responses to MDL 100,907, a selective 5-HT2A antagonist, with clozapine and haloperidol. Brain Res. Bull. 42 (1997) 211-219
22. Hanson G.R., Bush L., Keefe K.A., and Alburges M.E. Distinct responses of basal ganglia substance P systems to low and high doses of methamphetamine. J. Neurochem. 82 (2002) 1171-1178
23. Ikemoto S., Win M., and Liu Z. Primary reinforcing effects of nicotine are triggered from multiple regions both inside and outside the ventral tegmental area. J. Neurosci. 26 (2006) 723-730
24. Jiang Z., Pessia M., and North R. Neurotensin excitation of rat ventral tegmental neurons. J. Physiol. 474 (1994) 119-129
25. Kalivas P. Sensitization to repeated enkephalin administration into the ventral tegmental area of the rat. II. Involvement of the mesolimbic dopamine system. J. Pharmacol. Exp. Ther. 235 (1985) 544-550
26. Kalivas P., and Taylor S. Behavioral and neurochemical effect of daily injection with neurotensin into the ventral tegmental area. Brain Res. 358 (1985) 70-76
27. Kane J.K., Parker S.L., Matta S.G., Fu Y., Sharp B.M., and Li M.D. Nicotine up-regulates expression of orexin and its receptors in rat brain. Endocrinology 141 (2000) 3623-3629
28. Kane J.K., Parker S.L., and Li M.D. Hypothalamic orexin-A binding are downregulated by chronic nicotine treatment in the rat. Neurosci. Lett. 298 (2001) 1-4
29. Kane J.K., Hwang Y., Konu O., Loughlin S.E., Leslie F.M., and Li M.D. Regulation of homer and group I metabotropic glutamate receptors by nicotine. Eur. J. Neurosci. 21 (2005) 1145-1154
30. Kelley A., Cador M., Stinus L., and Le Moal M. Neurotensin, substance P, neurokinin-alpha, and enkephalin: injection into ventral tegmental area in the rat produces differential effects on operant responding. Psychopharmacology (Berl.) 97 (1989) 243-252
31. Kempsill F.E.J., and Pratt J.A. Mecamylamine but not the alpha 7 receptor antagonist alpha-bungarotoxin blocks sensitization to the locomotor stimulant effects of nicotine. Br. J. Pharmacol. 131 (2000) 997-1003
32. Klink R., de Kerchove d'Exaerde A., Zoli M., and Changeux J. Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J. Neurosci. 21 (2001) 1452-1463
33. Laviolette S., and van der Kooy D. Blockade of mesolimbic dopamine transmission dramatically increases sensitivity to the rewarding effects of nicotine in the ventral tegmental area. Mol. Psychiatry 8 (2003) 50-59
34. Legault M., Congar P., Michel F., and Trudeau L. Presynaptic action of neurotensin on cultural ventral tegmental area dopaminergic neurons. Neuroscience 111 (2002) 179-189
35. Letter A.A., Merchant K.M., Gibb J.W., and Hanson G.R. Effect of methamphetamine on neurotensin concentrations in rat brain regions. J. Pharmacol. Exp. Ther. 24 (1987) 443-447
36. Li M.D., and Kane J.K. Effect of nicotine on the expression of leptin and forebrain leptin receptors in the rat. Brain Res. 991 (2003) 222-231
37. Li M.D., Kane J.K., Parker S.L., McAllen K., Matta S.G., and Sharp B.M. Nicotine administration enhances NPY expression in the rat hypothalamus. Brain Res. 867 (2000) 157-164
38. Lopak V., and Erb S. Activation of central neurotensin receptors reinstates cocaine seeking in rat: modulation by a D1/D5, but not D2/D3, receptor antagonist. Psychopharmacology (Berl) 182 (2005) 297-304
39. Maidment N.T., Siddall B.J., Rudolph V.R., Erdelyi E., and Evans C.J. Dual determination of extracellular cholecystokinin and neurotensin fragments in rat forebrain: microdialysis combined with a sequential multiple antigen radioimmunoassay. Neuroscience 45 (1991) 81-93
40. Maskos U., Molles B., Pons S., Besson M., Guiard B., Guilloux J., Evrard A., Cazala P., Cormier A., Mameli-Engvall M., Dufour N., Cloez-Tayarani I., Bemelmans A., Mallet J., Gardier A., David V., Faure P., Granon S., and Changeux J. Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 435 (2005) 103-107
41. Matta S.G., Balfour D.J., Benowitz N.L., Boyd R.T., Buccafusco J.J., Caggiula A.R., Craig C.R., Collins A.C., Damaj M.I., Donny E.C., Gardiner P.S., Grady S.R., Heberlein U., Leonard S.S., Levin E.D., Lukas R.J., Markou A., Marks M.J., McCallum S.E., Prameswaran N., Perkins K.A., Picciotto M.R., Ouik M., Rose J.E., Rothenfluh A., Schafer W.R., Stolerman I.P., Tyndale R.F., Wehner J.M., and Zirger J.M. Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 190 (2007) 269-319
42. Merchant K.M., Letter A., Gibb J.W., and Hanson G.R. Changes in the limbic neurotensin system induced by doaminergic drugs. Eur. J. Pharmacol. 153 (1988) 1-9
43. Merchant K.M., Gibb J.W., and Hanson G.R. Role of dopamine D-1 and D-2 receptors in the regulation of neurotensin systems of the neostriatum and nucleus accumbens. Eur. J. Pharmacol. 160 (1989) 409-412
44. Merchant K.M., Bush L., Gibb J.W., and Hanson G.R. Neurotensin-dopamine interactions in the substantia nigra. J. Pharmacol. Exp. Ther. 255 (1990) 775-780
45. Naftchi N.E., Maker H., Lapin E., Sleis J., Lajtha A., and Leeman S. Acute reduction of brain substance P induced by nicotine. Neurochem. Res. 13 (1988) 305-309
46. Nisell M., Nomikos G.G., and Svensson T.H. Systemic nicotine-induced dopamine release in the rat nucleus accumbens is regulated by nicotinic receptors in the ventral tegmental area. Synapse 16 (1994) 36-44
47. Nisell M., Nomikos G.G., Hertel P., Panagis G., and Svensson T.H. Condition-independent sensitization of locomotor stimulation and mesocortical dopamine release following chronic nicotine treatment in rat. Synapse 22 (1996) 369-381
48. Nomikos G.G., Hildebrand B.E., Panagis G., and Svensson T.H. Nicotine withdrawal in the rat: role of alpha 7 nicotinic receptors in the ventral tegmental area. NeuroReport 10 (1999) 697-702
49. O'Dell T.J., and Christensen B.N. Mecamylamine is a selective non-competitive antagonist of N-methyl-d-aspartate- and aspartate-induced currents in horizontal cells dissociated from catfish retina. Neurosci. Lett. 94 (1988) 93-98
50. Panayi F., Colussi-Mas J., Lambas-Senas L., Renaud B., Scarna H., and Berod A. Endogenous neurotensin in the ventral termental area contributes to amphetamine behavioral sensitization. Neuropsychopharmacology 30 (2005) 871-879
51. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. second ed (1986), Academic Press, San Diego, CA
52. Pontieri F., Rasura M., Scontrini A., and Buttarelli F. Effects of intra-VTA injection of neurotensin on local cerebral glucose utilization in freely moving rats. Peptides 21 (2000) 1751-1753
53. Posnett D.N., McGrath H., and Tam J.P. A novel method for producing antipeptide antibodies. J. Biol. Chem. 261 (1988) 1719-1725
54. Quarta D., Ciruela F., Patkar K., Borycz J., Solinas M., Lluis C., Franco R., Wise R.A., Goldberg S.R., Hope B.T., Woods A.S., and Ferré S. Heteromeric nicotinic acetylcholine-dopamine autoreceptor complexes modulate striatal dopamine release. Neuropsychopharmacology 32 (2007) 35-42
55. Rahman S., Zhang J., and Corrigall W.A. Effects of acute and chronic nicotine on somatodendritic dopamine release of the VTA: in vivo microdialysis study. Neurosci. Lett. 348 (2003) 61-64
56. Reynolds S., Geisler S., Berod A., and Zahm D. Neurotensin antgonist acutely and robustly attenuates locomotion that accompanies stimulation of an neurotensin-containing pathway from rostrobasal forebrain to the ventral tegmental area. Eur. J. Neurosci. 24 (2006) 188-196
57. Ritter J.K., Schmidt C.J., Gibb J.W., and Hanson G.R. Increases of substance P-like immunoreactivity within striatal-nigral structures after subacute methamphetamine treatment. J. Pharmacol. Exp. Ther. 229 (1984) 233-240
58. Rompré P.P., and Bauco P. Neurotensin receptor activation sensitizes to the locomotor stimulant effect of cocaine: a role for NMDA receptors. Brain Res. 1085 (2006) 77-86
59. Rowell P., and Volk K. Nicotinic activation of mesolimbic neurons assessed by rubidium efflux in rat accumbens and ventral tegmentum. NeuroSignals 13 (2004) 114-121
60. Scott D.J., Domino E.F., Heitzeg M.M., Koeppe R.A., Ni L., Guthrie S., and Zubieta J.K. Smoking modulation of mu-opioid and dopamine D2 receptors-mediated neurotransmission in humans. Neuropsychopharmacology 32 (2007) 450-457
61. Sotty F., Brun P., Leonetti M., Steinberg R., Soubrie P., Renaud B., and Suaud-Chagny M. Comparative effects of neurotensin, neurotensin (8-13 and (D-Tyr[11] neurotensin applied into the ventral tegmental area on extracellular dopamine in the rat prefrontal cortex and nucleus accumbens. Neuroscience 98 (2000) 485-492
62. Seeman P., and Grigoriadis D. Dopamine D2 receptor dissociation constant for spiperone: identical values using 3H-labeled agonist or 3H-labeled antagonist. Biochem. Pharmacol. 34 (1985) 4065-4066
63. Singer S., Rossi S., Verzosa S., Hashim A., Lonow R., Cooper T., Sershen H., and Lajtha A. Nicotine-induced changes in neurotransmitter levels in brain areas associated with cognitive function. Neurochem. Res. 29 (2004) 1779-1792
64. Sziraki I., Sershen H., Hashim A., and Lajtha A. Receptors in the ventral tegmental area mediating nicotine-induced dopamine release in the nucleus accumbens. Neurochem. Res. 27 (2002) 253-261
65. Tam J.P. Synthetic peptide vaccine design: Synthesis and properties of a high-density multiple antigenic peptide system. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 5409-5413
66. Wagstaff J., Bush L., Gibb J.W., and Hanson G.R. Endogenous neurotensin antagonizes methamphetamine-enhanced dopaminergic activity. Brain Res. 665 (1994) 237-244
67. Wagstaff J., Gibb J.W., and Hanson G.R. Dopamine D2-receptors regulate neurotensin release from nucleus accumbens and striatum as measured by in vivo microdialysis. Brain Res. 721 (1996) 196-203
68. Wu J., George A.A., Schroeder K.M., Xu L., Marxer-Miller S., Lucero L., and Lukas R.J. Electrophysiological, pharmacological, and molecular evidence for alpha 7-nicotinic acethylcholine receptors in rat midbrain dopamine neurons. J. Pharmacol. Exp. Ther. 311 (2004) 80-91