Critical role of nitric oxide on nicotine-induced hyperactivation of dopaminergic nigrostriatal system: Electrophysiological and neurochemical evidence in rats

CNS Neuroscience and Therapeutics

Volumn 16, Issue 3, 2010, Pages 127-136

  Di Matteo, Vincenzo ^a   Pierucci, Massimo ^a   Benigno, Arcangelo ^b   Esposito, Ennio ^a   Crescimanno, Giuseppe ^b   Di Giovanni, Giuseppe ^b,c  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b UNIVERSITY OF PALERMO   (Italy)

^c UNIVERSITY OF MALTA   (Malta)

Author keywords

Corpus striatum; Dopamine; Extracellular recording; Microdialysis; Microiontophoresis; Nicotine; Nitric oxide; Substantia nigra pars compacta

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; 7 NITROINDAZOLE; DOPAMINE; MOLSIDOMINE; N(G) NITROARGININE METHYL ESTER; NICOTINE; NITRIC OXIDE; 7-NITROINDAZOLE; ARGININE; ENZYME INHIBITOR; INDAZOLE DERIVATIVE; NICOTINIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC SYSTEM; ELECTROPHYSIOLOGY; MALE; MICRODIALYSIS; MICROIONTOPHORESIS; MOTOR CONTROL; NERVE CELL STIMULATION; NEUROCHEMISTRY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; ACTION POTENTIAL; ANALYSIS OF VARIANCE; ANIMAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; DRUG INTERACTION; METABOLISM; NERVE CELL; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT; TIME;

3,4-DIHYDROXYPHENYLACETIC ACID; ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ARGININE; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME INHIBITORS; INDAZOLES; MALE; MICRODIALYSIS; NEURONS; NG-NITROARGININE METHYL ESTER; NICOTINE; NICOTINIC AGONISTS; NITRIC OXIDE; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA; TIME FACTORS;

EID: 77952184660     PISSN: 17555930     EISSN: 17555949     Source Type: Journal    
DOI: 10.1111/j.1755-5949.2010.00136.x     Document Type: Article

References (56)

1. Reavill C, Stolerman IP. Locomotor activity in rats after administration of nicotinic agonists intracerebrally. Br J Pharmacol 1990 99 : 273 278.
2. Corrigall WA, Coen KM. Selective dopamine antagonists reduce nicotine self-administration. Psychopharmacology 1991 104 : 171 176.
3. Rose JE, Corrigall WA. Nicotine self-administration in animals and humans: Similarities and differences. Psychopharmacology 1997 130 : 28 40.
4. Laviolette SR, 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 2003 8 : 50 59.
5. Clarke PBS, Fu DS, Jakubovic A, Fibiger HC. Evidence that Mesolimbic dopaminergic activation underlies the locomotor stimulant action of nicotine in rats. J Pharmacol Exp Ther 1988 246 : 701 708.
6. Louis M, Clarke PB. Effect of ventral tegmental 6-hydroxydopamine lesions on the locomotor stimulant action of nicotine in rats. Neuropharmacology 1998 37 : 1503 1513.
7. Dani JA, De Biasi M. Cellular mechanisms of nicotine addiction. Pharmacol Biochem Behav 2001 70 : 439 446.
8. Di Chiara G, Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 1988 85 : 5274 5278.
9. Schilström B, Svensson HM, Svensson TH, Nomikos GG. 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 1998 85 : 1005 1009. (Pubitemid 28293408)
10. Imperato A, Mulas A, Di Chiara G. Nicotine preferentially stimulates dopamine release in the limbic system of freely moving rats. Eur J Pharmacol 1986 132 : 337 338.
11. Marshall DL, Redfern PH, Wonnacott S. Presynaptic nicotinic modulation of dopamine release in the three ascending pathways studied by in vivo microdialysis: Comparison of naive and chronic nicotine-treated rats. J Neurochem 1997 68 : 1511 1519.
12. Di Matteo V, Pierucci M, Esposito E. Selective stimulation of serotonin2c receptors blocks the enhancement of striatal and accumbal dopamine release induced by nicotine administration. J Neurochem 2004 89 : 418 429. (Pubitemid 38495990)
13. Clarke PBS, Hommer DW, Pert A, Skirboll LR. Electrophysiological actions of nicotine on substantia nigra single units. Br J Pharmacol 1985 85 : 827 835.
14. Calabresi P, Lacey MG, North RA. Nicotinic excitation of rat ventral tegmental neurones in vitro studied by intracellular recording. Br J Pharmacol 1989 98 : 135 140.
15. Sorenson EM, Shiroyama T, Kitai ST. Postsynaptic nicotinic receptors on dopaminergic neurons in the substantia nigra pars compacta of the rat. Neuroscience 1998 87 : 659 673.
16. Schilström B, Rawal N, Mameli-Engvall M, Nomikos GG, Svensson TH. Dual effects of nicotine on dopamine neurons mediated by different receptor subtypes. Int J Neuropsychopharmacol 2003 6 : 1 11.
17. Schilström B, Mameli-Engvall M, Rawal N, Grillner P, Jardemark K, Svensson TH. Nitric oxide is involved in nicotine-induced burst firing of rat ventral tegmental area dopamine neurons. Neuroscience 2004 125 : 957 964.
18. Pierucci M, Di Matteo V, Esposito E. Stimulation of serotonin2C receptors blocks the hyperactivation of midbrain dopamine neurons induced by nicotine administration. J Pharmacol Exp Ther 2004 309 : 109 118. (Pubitemid 38393121)
19. Mifsud J-C, Hernandez L, Hoebel BG. Nicotine infused into the nucleus accumbens increases synaptic dopamine as measured by in vivo microdialysis. Brain Res 1989 478 : 365 367.
20. Ferrari R, Le Nove're N, Picciotto MR, Changeux JP, Zoli M. Acute and long-term changes in the mesolimbic dopamine pathway after systemic or local single nicotine injections. Eur J Neurosci 2002 15 : 1810 1818.
21. Di Matteo V, Pierucci M, Benigno A, Crescimanno G, Esposito E, Di Giovanni G. Involvement of nitric oxide in 6-OHDA-induced neurodegeneration: A neurochemical study. Ann N Y Acad Sci 2009 1155, 309 315.
22. Di Matteo V, Pierucci M, Benigno A, Orbán G, Crescimanno G, Esposito E, Di Giovanni G. Electrophysiological and neurochemical characterization of 7-Nitroindazole and molsidomine acute and subchronic administration effects in the dopaminergic nigrostriatal system in rats. J Neural Transm Suppl 2009 73, 173 182.
23. McLeod TM, López-Figueroa AL, López-Figueroa MO. Nitric oxide, stress, and depression. Psychopharmacol Bull 2001 35 : 24 41.
24. Yao JK, Leonard S, Reddy RD. Increased nitric oxide radicals in post-mortem brain from patients with schizophrenia. Schizophr Bull 2004 30 : 923 934.
25. Tayfun Uzbay I, Oglesby MW. Nitric oxide and substance dependence. Neurosci Biobehav Rev 2001 25 : 43 52.
26. West AR, Galloway MP, Grace AA. Regulation of striatal dopamine neurotransmission by nitric oxide: Effector pathways and signalling mechanisms. Synapse 2002 44 : 227 245.
27. Vleeming W, Rambali B, Opperhuizen A. The role of nitric oxide in cigarette smoking and nicotine addiction. Nicotine Tob Res 2002 4 : 341 348.
28. Di Giovanni G, Shi WX. Effects of scopolamine on dopamine neurons in the substantia nigra: Role of the pedunculopontine tegmental nucleus. Synapse 2009 63 : 673 680.
29. Paxinos G, Watson C. The Rat brain in stereotaxic coordinates.
30. Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: Burst firing. J Neurosci 1984 4 : 2877 2890.
31. West AR, Grace AA. Striatal nitric oxide signalling regulates the neuronal activity of midbrain dopamine neurons in vivo. J Neurophysiol 2000 83 : 1796 1808.
32. Cox BA, Johnson SW. Nitric oxide facilitates N-methyl-D-aspartate-induced burst firing in dopamine neurons from rat midbrain slices. Neurosci Lett 1998 255 : 131 134.
33. Nowak P, Brus R, Oświecimska J, Sokoła A, Kostrzewa RM. 7-Nitroindazole enhances amphetamine-evoked dopamine release in rat striatum. An in vivo microdialysis and voltammetric study. J Physiol Pharmacol 2002 53 : 251 263.
34. Campos F, Alfonso M, Vidal L, Faro LR, Durán R. Mediation of glutamatergic receptors and nitric oxide on striatal dopamine release evoked by anatoxin-a. An in vivo microdialysis study. Eur J Pharmacol 2006 548 : 90 98.
35. Southan GJ, Szabo C. Selective pharmacological inhibition of distinct nitric oxide synthase isoforms. Biochem Pharmacol 1996 51 : 383 394.
36. Meyer RC, Spangler EL, Patel N, London ED, Ingram DK. Impaired learning in rats in a 14-unit T-maze by 7-nitroindazole, a neuronal nitric oxide synthase inhibitor, is attenuated by the nitric oxide donor, molsidomine. Eur J Pharmacol 1998 341 : 17 22.
37. Castagnoli K, Palmer S, Anderson A, Bueters T, Castagnoli N Jr. The neuronal nitric oxide synthase inhibitor 7-nitroindazole also inhibits the monoamine oxidase-B-catalyzed oxidation of 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine. Chem Res Toxicol 1997 10 : 364 368.
38. Boireau A, Dubedat P, Bordier F, Imperato A, Moussaoui S. The protective effect of riluzole in the MPTP model of Parkinson's disease in mice is not due to a decrease in MPP(+) accumulation. Neuropharmacology 2000 39 : 1016 1020.
39. Thomas B, Saravanan KS, Mohanakumar KP. In vitro and in vivo evidences that antioxidant action contributes to the neuroprotective effects of the neuronal nitric oxide synthase and monoamine oxidase-B inhibitor, 7-nitroindazole. Neurochem Int 2008 52 : 990 1001.
40. Klink R, de Kerkhove d'Exaerde A, Zoli M, Changeux J-P. Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 2001 21 : 1452 1463.
41. Mansvelder HD, McGehee DS. Cellular and synaptic mechanisms of nicotine addiction. J Neurobiol 2002 53 : 606 617.
42. Mansvelder HD, Keath JR, McGehee DS. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 2002 33 : 905 919.
43. Klejbor I, Domaradzka-Pytel B, Ludkiewicz B, Wójcik S, Moryś J. The relationships between neurons containing dopamine and nitric oxide synthase in the ventral tegmental area. Folia Histochem Cytobio 2004 42 : 83 87.
44. Del Bel E, Bermúdez-Echeverry M, Salum C, Raisman-Vozari R. Nitric oxide system and basal ganglia physiopathology. In : Di Giovanni G, editor. The basal ganglia pathophysiology: Recent advances.
45. Exley R, Cragg SJ. Presynaptic nicotinic receptors: A dynamic and diverse cholinergic filter of striatal dopamine neurotransmission. Br J Pharmacol 2008 153 (Suppl 1 S283 S297.
46. Sammut S, Bray KE, West AR. Dopamine D2 receptor-dependent modulation of striatal NO synthase activity. Psychopharmacology 2007 191 : 793 803.
47. Sammut S, Dec A, Mitchell D, Linardakis J, Ortiguela M, West AR. Phasic dopaminergic transmission increases NO efflux in the rat dorsal striatum via a neuronal NOS and a dopamine D(1/5) receptor-dependent mechanism. Neuropsychopharmacology 2006 31 : 493 505.
48. Martin JL, Itzhak Y. 7-Nitroindazole blocks nicotine-induced conditioned place preference but not LiCl-induced conditioned place aversion. Neuroreport 2000 11 : 947 949.
49. Malin DH, Lake JR, Shenoi M, Upchurch TP, Johnson SC, Schweinle WE, Cadle CD. The nitric oxide synthesis inhibitor nitro-L-arginine (L-NNA) attenuates nicotine abstinence syndrome in the rat. Psychopharmacology (Berl) 1998 140 : 371 377.
50. Adams ML, Cicero T. Nitric oxide mediates mecamylamine- and naloxone-precipitated nicotine withdrawal. Eur J Pharmacol 1998 345 : R1 R2.
51. Jain R, Mukherjee K, Mohan D. Effects of nitric oxide synthase inhibitors in attenuating nicotine withdrawal in rats. Pharmacol Biochem Behav 2008 88 : 473 480.
52. Shim I, Kim HT, Kim YH, et al. Role of nitric oxide synthase inhibitors and NMDA receptor antagonist in nicotine-induced behavioral sensitization in the rat. Eur J Pharmocol 2002 443 : 119 124.
53. Ulusu U, Uzbay IT, Kayir H, Alici T, Karakas S. Evidence for the role of nitric oxide in nicotine-induced locomotor sensitization in mice. Psychopharmacology (Berl) 2005 178 : 500 504.
54. Hong SK, Jung IS, Bang SA, Kim SE. Effect of nitric oxide synthase inhibitor and NMDA receptor antagonist on the development of nicotine sensitization of nucleus accumbens dopamine release: An in vivo microdialysis study. Neurosci Lett 2006 409 : 220 223.
55. Wilkes S. The use of bupropion SR in cigarette smoking cessation. Int J Chron Obstruct Pulmon Dis 2008 3 : 45 53.
56. Dhir A, Kulkarni SK. Involvement of nitric oxide (NO) signaling pathway in the antidepressant action of bupropion, a dopamine reuptake inhibitor. Eur J Pharmacol 2007 568 : 177 185.