Involvement of GABAB receptors in biochemical alterations induced by anxiety-related responses to nicotine in mice: Genetic and pharmacological approaches

Neuropharmacology

Volumn 81, Issue , 2014, Pages 31-41

  Varani, Andrés P ^a   Pedrón, Valeria T ^a   Bettler, Bernhard ^b   Balerio, Graciela N ^a,c  

^a Instituto de Investigaciones Farmacologicas   (Argentina)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

2 OH saclofen; Anxiety; c Fos; Catecholamine; GABAB receptor; Nicotine

Indexed keywords

2-HYDROXYSACLOFEN; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; BACLOFEN; NICOTINE; NICOTINIC AGENT; PROTEIN C FOS;

ANALOGS AND DERIVATIVES; ANALYSIS OF VARIANCE; ANIMAL; ANXIETY; CHEMICALLY INDUCED; DISEASE MODEL; DORSAL RAPHE NUCLEUS; DOSE RESPONSE; DRUG EFFECTS; DRUG THERAPY; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; MOUSE; SEPTUM NUCLEUS; TOXICITY;

ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; BACLOFEN; DISEASE MODELS, ANIMAL; DORSAL RAPHE NUCLEUS; DOSE-RESPONSE RELATIONSHIP, DRUG; GABA-B RECEPTOR ANTAGONISTS; GENE EXPRESSION REGULATION; MALE; MICE; MICE, KNOCKOUT; NEUROTRANSMITTER AGENTS; NICOTINE; NICOTINIC AGONISTS; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTORS, GABA-B; SEPTAL NUCLEI;

EID: 84894183507     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.01.030     Document Type: Article

References (72)

1. J. Antonopoulos, M. Latsari, I. Dori, M. Chiotelli, J.G. Parnavelas, and A. Dinopoulos Noradrenergic innervation of the developing and mature septal area of the rat J. Comp. Neurol. 476 2004 80 90 (Pubitemid 38880234)
2. G.N. Balerio, E. Aso, and R. Maldonado Involvement of the opioid system in the effects induced by nicotine on anxiety-like behaviour in mice Psychopharmacology (Berl) 181 2005 260 269 (Pubitemid 41492196)
3. G.N. Balerio, E. Aso, and R. Maldonado Role of the cannabinoid system in the effects induced by nicotine on anxiety-like behaviour in mice Psychopharmacology (Berl) 184 2006 504 513 (Pubitemid 43255867)
4. S.J. Bang, and K.G. Commons Age-dependent effects of initial exposure to nicotine on serotonin neurons Neuroscience 179 2011 1 8
5. N.L. Benowitz Neurobiology of nicotine Addiction: implications for smoking cessation treatment Am. J. Med. 121 2008 S3 S10
6. J.D. Berke, and S.E. Hyman Addiction, dopamine, and the molecular mechanisms of memory Neuron 25 2000 515 532
7. H. Bester, C. De Felipe, and S.P. Hunt The NK1 receptor is essential for the full expression of noxious inhibitory controls in the mouse J. Neurosci. 21 2001 1039 1046 (Pubitemid 32163144)
8. G. Biala, and M. Kruk Effects of co-administration of bupropion and nicotine or D-amphetamine on the elevated plus maze test in mice J. Pharm. Pharmacol. 61 2009 493 502
9. G. Biala, M. Kruk, and B. Budzynska Effects of the cannabinoid receptor ligands on anxiety-related effects of d-amphetamine and nicotine in the mouse elevated plus maze test J. Physiol. Pharmacol. 60 2009 113 122
10. A.A. Braun, M.R. Skelton, C.V. Vorhees, and M.T. Williams Comparison of the elevated plus and elevated zero mazes in treated and untreated male Sprague-Dawley rats: effects of anxiolytic and anxiogenic agents Pharmacol. Biochem. Behav. 97 2011 406 415
11. M.T. Castañeda, E.R. Sanabria, S. Hernandez, A. Ayala, T.A. Reyna, J.Y. Wu, and L.V. Colom Glutamic acid decarboxylase isoforms are differentially distributed in the septal region of the rat Neurosci. Res. 52 2005 107 119 (Pubitemid 40461877)
12. B. Chang, C.A. Daniele, K. Gallagher, M. Madonia, R.D. Mitchum, L. Barrett, P. Vezina, and D.S. McGehee Nicotinic excitation of serotonergic projections from dorsal raphe to the nucleus accumbens J. Neurophysiol. 106 2011 801 808
13. S. Cheeta, E.E. Irvine, P.J. Kenny, and S.E. File The dorsal raphé nucleus is a crucial structure mediating nicotine's anxiolytic effects and the development of tolerance and withdrawal responses Psychopharmacology (Berl) 155 2001 78 85 (Pubitemid 32295772)
14. 1A receptors in mediating the anxiogenic effects of nicotine following lateral septal administration Eur. J. Neurosci. 12 2000 3797 3802
15. S. Cheeta, P.J. Kenny, and S.E. File Hippocampal and septal injections of nicotine and 8-OH-DPAT distinguish among different animal tests of anxiety Prog. Neuropsychopharmacol. Biol. Psychiatry 24 2000 1053 1067 (Pubitemid 32268863)
16. S. Cheeta, S. Tucci, and S.E. File Antagonism of the anxiolytic effect of nicotine in the dorsal raphe nucleus by dihydro-b-erythroidine Pharmacol. Biochem. Behav. 70 2001 491 496 (Pubitemid 34131643)
17. A. Dalvi, and R.J. Rodgers GABAergic influences on plus-maze behaviour in mice Psychopharmacology (Berl) 128 1996 380 397 (Pubitemid 26417680)
18. M.I. Damaj, R.A. Glennon, and B.R. Martin Involvement of the serotonergic system in the hypoactive and antinociceptive effects of nicotine in mice Brain Res. Bull. 33 1994 199 203 (Pubitemid 124009936)
19. M.A. Delfino, A.V. Stefano, J.E. Ferrario, I.R. Taravini, M.G. Murer, and O.S. Gershanik Behavioral sensitization to different dopamine agonists in a parkinsonian rodent model of drug-induced dyskinesias Behav. Brain Res. 152 2004 297 306 (Pubitemid 38757900)
20. M. Dragunow, and R. Faull The use of c-fos as a metabolic marker in neuronal pathway tracing J. Neurosci. Methods 29 1989 261 265 (Pubitemid 19222725)
21. G. Engberg, S. Erhardt, T. Sharp, and M. Hajós Nicotine inhibits firing activity of dorsal raphe 5-HT neurones in vivo Naunyn Schmiedeb. Arch. Pharmacol. 362 2000 41 45 (Pubitemid 30431634)
22. S.E. File, S. Cheeta, and P.J. Kenny Neurobiological mechanisms by which nicotine mediates different types of anxiety Eur. J. Pharmacol. 393 2000 231 236 (Pubitemid 30193421)
23. S.E. File, S. Cheeta, P.J. Kenny, and A.M. Ouagazzal Roles of the dorsal raphe nucleus, lateral septum and dorsal hippocampus in nicotine's effects on axiety Soc. Neurosci. 1999 Abstract. 24:1981. (Personal communication)
24. J. Foulds, J.A. Stapleton, N. Bell, J. Swettenham, M.J. Jarvis, and M.A. Russell Mood and physiological effects of subcutaneous nicotine in smokers and never-smokers Drug Alcohol Depend. 44 1997 105 115 (Pubitemid 27129503)
25. 1A-mediated responses: effect of treatments that modify serotonergic neurotransmission Ann. N. Y. Acad. Sci. 600 1990 460 475
26. J. Garduño, L. Galindo-Charles, J. Jiménez-Rodríguez, E. Galarraga, D. Tapia, S. Mihailescu, and S. Hernandez-Lopez Presynaptic α4β2 nicotinic acetylcholine receptors increase glutamate release and serotonin neuron excitability in the dorsal raphe nucleus J. Neurosci. 32 2012 15148 15157
27. E.R. Garrido Sanabria, M.T. Castañeda, C. Banuelos, M.G. Perez-Cordova, S. Hernandez, and L.V. Colom Septal GABAergic neurons are selectively vulnerable to pilocarpine-induced status epilepticus and chronic spontaneous seizures Neuroscience 142 2006 871 883 (Pubitemid 44485907)
28. © 2007 by
29. R. Guzmán-Marín, M.N. Alam, S. Mihailescu, R. Szymusiak, D. McGinty, and R. Drucker-Colín Subcutaneous administration of nicotine changes dorsal raphe serotonergic neurons discharge rate during REM sleep Brain Res. 888 2001 321 325 (Pubitemid 32058800)
30. L.G. Harsing Jr. The pharmacology of the neurochemical transmission in the midbrain raphe nuclei of the rat Curr. Neuropharmacol. 4 2006 313 339 (Pubitemid 44524467)
31. R.E. Heikkila, A. Hess, and R.C. Duvoisin Dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine in mice Science 224 1984 1451 1453 (Pubitemid 14123348)
32. S. Hernandez-Lopez, J. Garduño, and S. Mihailescu Nicotinic modulation of serotonergic activity in the dorsal raphe nucleus Rev. Neurosci. 24 2013 455 469
33. R. Hurst, H. Rollema, and D. Bertrand Nicotinic acetylcholine receptors: from basic science to therapeutics Pharmacol. Ther. 137 2013 22 54
34. F.F. Ikard, D.E. Green, and D. Horn A scale differentiates between types of smoking as related to the management of affect Int. J. Addict. 4 1969 649 659
35. B receptor positive modulator CGP7930 in rodents Neuropharmacology 54 2008 854 862
36. J.D. Kassel, and M. Unrod Smoking, anxiety, and attention: support for the role of nicotine in attentionally mediated anxiolysis J. Abnorm. Psychol. 109 2000 161 166 (Pubitemid 30155419)
37. Y.Q. Li, T. Kaneko, and N. Mizuno Collateral projections of nucleus raphe dorsalis neurones to the caudate-putamen and region around the nucleus raphe magnus and nucleus reticularis gigantocellularis pars alpha in the rat Neurosci. Lett. 299 2001 33 36 (Pubitemid 32146338)
38. A.M. Mathieu-Kia, C. Pages, and M.J. Besson Inducibility of c-Fos protein in visuo-motor system and limbic structures after acute and repeated administration of nicotine in the rat Synapse 29 1998 343 354 (Pubitemid 28328678)
39. S. Mihailescu, R. Guzmán-Marín, M. del C. Domínguez, and R. Drucker-Colín Mechanisms of nicotine actions on dorsal raphe serotoninergic neurons Eur. J. Pharmacol. 452 2002 77 82 (Pubitemid 35248126)
40. S. Mihailescu, R. Guzmán-Marín, and R. Drucker-Colín Nicotine stimulation of dorsal raphe neurons: effects on laterodorsal and pedunculopontine neurons Eur. Neuropsychopharmacol. 11 2001 359 366 (Pubitemid 32946886)
41. (B) receptors in the modulation of anxiety- and antidepressant-like behaviour Neuropsychopharmacology 29 2004 1050 1062 (Pubitemid 38670043)
42. B receptor-positive modulation-induced blockade of the rewarding properties of nicotine is associated with a reduction in nucleus accumbens DeltaFosB accumulation J. Pharmacol. Exp. Ther. 321 2007 172 177 (Pubitemid 46456987)
43. E.J. Nestler Molecular basis of long-term plasticity underlying addiction Nat. Rev. Neurosci. 2 2001 119 128 (Pubitemid 33673366)
44. P. Netter, J. Hennig, S. Huwe, and R. Olbrich Personality related effects of nicotine, mode of application, and expectancies on performance, emotional states, and desire for smoking Psychopharmacology 135 1998 52 62 (Pubitemid 28055450)
45. P.A. Newhouse, T. Sunderland, P.K. Narang, A.M. Mellow, J.B. Fertig, B.A. Lawlor, and D.L. Murphy Neuroendocrine, physiologic, and behavioral responses following intravenous nicotine in nonsmoking healthy volunteers and in patients with Alzheimer's disease Psychoneuro-Endocrinology 15 1990 471 484
46. K. Okada, K. Nakamura, and Y. Kobayashi A neural correlate of predicted and actual reward-value information in monkey pedunculopontine tegmental and dorsal raphe nucleus during saccade tasks Neural Plast. 2011 2011 1 21
47. A.M. Ouagazzal, P.J. Kenny, and S.E. File Stimulation of nicotinic receptors in the lateral septal nucleus increases anxiety Eur. J. Neurosci. 11 1999 3957 3962 (Pubitemid 29537575)
48. S.R. Pagliusi, M. Tessari, S. DeVevey, C. Chiamulera, and E.M. Pich The reinforcing properties of nicotine are associated with a specific patterning of c-fos expression in the rat brain Eur. J. Neurosci. 8 1996 2247 2256 (Pubitemid 26387886)
49. A.C. Parrott, and N.J. Garnham Comparative mood states and cognitive skills of cigarette smokers, deprived smokers and nonsmokers Hum. Psychopharmacol. Clin. Exp. 13 1998 367 376 (Pubitemid 28358164)
50. B receptor ligands in rodent tests of anxiety-like behavior Pharmacol. Rep. 59 2007 757 762 (Pubitemid 351586569)
51. G. Paxinos, and K. Franklin The Mouse Brain in Stereotaxic Coordinates second ed. 2004 Academic Press London
52. M.R. Picciotto, D.H. Brunzell, and B.J. Caldarone Effect of nicotine and nicotinic receptors on anxiety and depression Neuroreport 13 2002 1097 1106 (Pubitemid 34722033)
53. M. Piri, M. Nasehi, Z. Shahab, and M.R. Zarrindast The effects of nicotine on nitric oxide induced anxiogenic-like behaviors in the dorsal hippocampus Neurosci. Lett. 528 2012 93 98
54. A. Plaza-Zabala, E. Martín-García, L. de Lecea, R. Maldonado, and F. Berrendero Hypocretins regulate the anxiogenic-like effects of nicotine and induce reinstatement of nicotine-seeking behavior J. Neurosci. 30 2010 2300 2310
55. O.F. Pomerleau Nicotine as a psychoactive drug: anxiety and pain reduction Psychopharmacol. Bull. 22 1986 865 869 (Pubitemid 17183396)
56. P. Riekkinen Jr., J. Sirviö, and M. Riekkinen Serotonin depletion decreases the therapeutic effect of nicotine, but not THA in medial septal-lesioned rats Brain Res. 662 1994 95 102 (Pubitemid 24326867)
57. O. Salminen, S. Lahtinen, and L. Ahtee Expression of Fos protein in various rat brain areas following acute nicotine and diazepam Pharmacol. Biochem. Behav. 54 1996 241 248 (Pubitemid 26143105)
58. (B(1)) Neuron 31 2001 47 58 (Pubitemid 32757088)
59. SENASA, Resolución 617/2002. Requisitos, Condiciones y procedimientos para la habilitación técnica de laboratorios que posean bioterios de producción, mantenimiento y local de experimentación.
60. P. Seth, S. Cheeta, S. Tucci, and S.E. File Nicotinic-serotonergic interactions in brain and behaviour Pharmacol. Biochem. Behav. 71 2002 795 805 (Pubitemid 34219229)
61. E. Shearman, S. Fallon, H. Sershen, and A. Lajtha Nicotine-induced monoamine neurotransmitter changes in the brain of young rats Brain Res. Bull. 76 2008 626 639
62. T.P. Sheehan, R.A. Chambers, and D.S. Russell Regulation of affect by the lateral septum: implications for neuropsychiatry Brain Res. Brain Res. Rev. 46 2004 71 117 (Pubitemid 39036164)
63. M.J. Shram, D. Funk, Z. Li, and A.D. Lê Acute nicotine enhances c-fos mRNA expression differentially in reward-related substrates of adolescent and adult rat brain Neurosci. Lett. 418 2007 286 291 (Pubitemid 46670565)
64. K. Soderstrom, W. Qin, H. Williams, D.A. Taylor, and B.A. McMillen Nicotine increases FosB expression within a subset of reward- and memory-related brain regions during both peri- and post-adolescence Psychopharmacology (Berl) 191 2007 891 897 (Pubitemid 46399153)
65. 1A receptor-mediated inhibition of dorsal raphe serotonin neurons produced by nicotine exposure and withdrawal Eur. J. Neurosci. 33 2011 1866 1875
66. H.W. Steinbusch, D. Van der Kooy, A.A. Verhofstad, and A. Pellegrino Serotonergic and non-serotonergic projections from the nucleus raphe dorsalis to the caudate-putamen complex in the rat, studied by a combined immunofluorescence and fluorescent retrograde axonal labeling technique Neurosci. Lett. 19 1980 137 142 (Pubitemid 11239137)
67. 3 receptor antagonist ondansetron Life Sci. 61 1997 249 254
68. B receptors involvement in the effects induced by nicotine on anxiety-related behaviour in mice Behav. Pharmacol. 65 2012 507 513
69. A.P. Varani, L. Machado Moutinho, B. Bettler, and G.N. Balerio Acute behavioural responses to nicotine and nicotine withdrawal syndrome are modified in GABA(B1) knockout mice Neuropharmacology 63 2012 863 872
70. M.R. Zarrindast, A. Aghamohammadi-Sereshki, A. Rezayof, and P. Rostami Nicotine-induced anxiogenic-like behaviours of rats in the elevated plus-maze: possible role of NMDA receptors of the central amygdala J. Psychopharmacol. 26 2012 555 563
71. M.R. Zarrindast, R. Tajik, M. Ebrahimi-Ghiri, M. Nasehi, and A. Rezayof Role of the medial septum cholinoceptors in anxiogenic-like effects of nicotine Physiol. Behav. 119 2013 103 109
72. C. Zhao, B. Eisinger, and S.C. Gammie Characterization of GABAergic neurons in the mouse lateral septum: double fluorescence in situ hybridization and immunohistochemical study using tyramide signal amplification PLoS One 8 8 2013 e73750