Acute behavioural responses to nicotine and nicotine withdrawal syndrome are modified in GABAB1 knockout mice

Neuropharmacology

Volumn 63, Issue 5, 2012, Pages 863-872

  Varani, Andrés P ^a   Moutinho, Lirane MacHado ^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

Anxiety like behaviour; c Fos; GABAB receptor; Nicotine; Nociception; Withdrawal

Indexed keywords

4 AMINOBUTYRIC ACID B1 RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; NICOTINE; PROTEIN FOS; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ANXIETY; ARTICLE; BASOLATERAL AMYGDALA; BEHAVIOR; CONTROLLED STUDY; DENTATE GYRUS; LOCOMOTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; STRIA TERMINALIS; TOBACCO DEPENDENCE; TRANQUILIZING ACTIVITY; WILD TYPE; WITHDRAWAL SYNDROME;

AMYGDALA; ANALGESICS, NON-NARCOTIC; ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; BEHAVIOR, ANIMAL; DENTATE GYRUS; DOSE-RESPONSE RELATIONSHIP, DRUG; GANGLIONIC BLOCKERS; GANGLIONIC STIMULANTS; INJECTIONS, SUBCUTANEOUS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MOTOR ACTIVITY; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; PAIN THRESHOLD; RECEPTORS, GABA-B; SEPTAL NUCLEI; TOBACCO USE DISORDER;

EID: 84864421325     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.06.006     Document Type: Article

References (69)

1. E. Aso, R. Maldonado, and G. Balerio Baclofen modifies nicotine behavioural responses, but not motivational manifestations of nicotine withdrawal in mice Biocell Abstract 66 2007 98
2. G.N. Balerio, E. Aso, F. Berrendero, P. Murtra, and R. Maldonado Delta9-tetrahydrocannabinol decreases somatic and motivational manifestations of nicotine withdrawal in mice Eur. J. Neurosci. 20 2004 2737 2748 (Pubitemid 39573789)
3. 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)
4. 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)
5. A.W. Bannon, M.W. Decker, M.W. Holladay, P. Curzon, D. Donnelly-Roberts, P.S. Puttfarcken, R.S. Bitner, A. Diaz, A.H. Dickenson, R.D. Porsolt, M. Williams, and S.P. Arneric Broad-spectrum, non-opioid analgesic activity by selective modulation of neuronal nicotinic acetylcholine receptors Science 279 1998 77 81 (Pubitemid 28079158)
6. E.A. Barnard, P. Skolnick, R.W. Olsen, H. Mohler, W. Sieghart, G. Biggio, C. Braestrup, A.N. Bateson, and S.Z. Langer International Union of Pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function Pharmacol. Rev. 50 1998 291 313 (Pubitemid 28304030)
7. J.D. Berke, and S.E. Hyman Addiction, dopamine, and the molecular mechanisms of memory Neuron 25 2000 515 532
8. F. Berrendero, V. Mendizábal, P. Robledo, L. Galeote, A. Bilkei-Gorzo, A. Zimmer, and R. Maldonado Nicotine-induced antinociception, rewarding effects, and physical dependence are decreased in mice lacking the preproenkephalin gene J. Neurosci. 25 2005 1103 1112 (Pubitemid 40268951)
9. A. Berry, F. Capone, M. Giorgio, P.G. Pelicci, E.R. de Kloet, E. Alleva, L. Minghetti, and F. Cirulli Deletion of the life span determinant p66Shc prevents age-dependent increases in emotionality and pain sensitivity in mice Exp. Gerontol. 42 2007 37 45 (Pubitemid 44937826)
10. 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)
11. J.W. Blaszczyk, I.B. Lapo, T. Werka, and B. Sadowski Differential startle magnitude in mice selected for high and low swim analgesia is not related to difference in nociception Acta Neurobiol. Exp. (Wars) 70 2010 398 405
12. N.G. Bowery, B. Bettler, W. Froestl, J.P. Gallagher, F. Marshall, M. Raiteri, T.I. Bonner, and S.J. Enna International Union of Pharmacology. XXXIII. Mammalian gamma-aminobutyric acid(B) receptors: structure and function Pharmacol. Rev. 54 2002 247 264 (Pubitemid 34575715)
13. A.R. Caggiula, L.H. Epstein, K.A. Perkins, and S. Saylor Different methods of assessing nicotine-induced antinociception may engage different neuronal mechanisms Psychopharmacology 122 1995 301 306
14. A. Castañé, E. Valjent, C. Ledent, M. Parmentier, R. Maldonado, and O. Valverde Lack of CB1 cannabinoid receptors modifies nicotine behavioural responses, but not nicotine abstinence Neuropharmacology 43 2002 857 867 (Pubitemid 35221396)
15. A. Castañé, L. Wells, G. Soria, S. Hourani, C. Ledent, I. Kitchen, J. Opacka-Juffry, R. Maldonado, and O. Valverde Behavioural and biochemical responses to morphine associated with its motivational properties are altered in adenosine A(2A) receptor knockout mice Br. J. Pharmacol. 155 2008 757 766
16. E.J. Chesler, S.G. Wilson, W.R. Lariviere, S.L. Rodriguez-Zas, and J.S. Mogil Identification and ranking of genetic and laboratory environment factors influencing a behavioral trait, thermal nociception, via computational analysis of a large data archive Neurosci. Biobehav. Rev. 26 2002 907 923 (Pubitemid 36344032)
17. P.B. Clarke, and R. Kumar The effects of nicotine on locomotor activity in non-tolerant and tolerant rats Br. J. Pharmacol. 78 1983 329 337 (Pubitemid 13192204)
18. M. Cordero-Erausquin, and J.P. Changeux Tonic nicotinic modulation of serotoninergic transmission in the spinal cord Proc. Natl. Acad. Sci. U. S. A. 98 2001 2803 2807 (Pubitemid 32209564)
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 Schmiedebergs Arch. Pharmacol. 362 2000 41 45 (Pubitemid 30431634)
22. S.E. File, N. Andrews, P.Y. Wu, A. Zharkovsky, and H. Zangrossi Jr. Modification of chlordiazepoxide's behavioural and neurochemical effects by handling and plus-maze experience Eur. J. Pharmacol. 218 1992 9 14
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 anxiety Soc. Neurosci. Abstract 24 1999 1981
24. B receptor ligands in animal tests of depression and anxiety Pharmacol. Rep. 59 2007 645 655 (Pubitemid 351586555)
25. Y.K. Fung, M.J. Schimid, T.M. Anderson, and Y. Lau Effects of nicotine withdrawal on central dopaminergic systems Pharmacol. Biochem. Behav. 53 1996 635 640 (Pubitemid 26086452)
26. L. Galeote, R. Maldonado, and F. Berrendero Involvement of kappa/dynorphin system in the development of tolerance to nicotine-induced antinociception J. Neurochem. 105 2008 1358 1368 (Pubitemid 351590804)
27. V. Gangadharan, N. Agarwal, S. Brugger, I. Tegeder, B. Bettler, R. Kuner, and M. Kurejova Conditional gene deletion reveals functional redundancy of GABAB receptors in peripheral nociceptors in vivo Mol. Pain 5 2009 68
28. M. Gassmann, H. Shaban, R. Vigot, G. Sansig, C. Haller, S. Barbieri, Y. Humeau, V. Schuler, M. Müller, B. Kinzel, K. Klebs, M. Schmutz, W. Froestl, J. Heid, P.H. Kelly, C. Gentry, A.L. Jaton, H. Van der Putten, C. Mombereau, L. Lecourtier, J. Mosbacher, J.F. Cryan, J.M. Fritschy, A. Lüthi, K. Kaupmann, and B. Bettler Redistribution of GABAB(1) protein and atypical GABAB responses in GABAB(2)-deficient mice J. Neurosci. 24 2004 6086 6097 (Pubitemid 38891099)
29. Guide for the Care and Use of Laboratory Animals National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals eighth ed. 1985 National Academies Press (US) Washington (DC)
30. B.E. Hildebrand, G. Panagis, T.H. Svensson, and G.G. Nomikos Behavioral and biochemical manifestations of mecamylamine-precipitated nicotine withdrawal in the rat: role of nicotinic receptors in the ventral tegmental area Neuropsychopharmacology 21 1999 560 574 (Pubitemid 29414801)
31. N. Imamachi, G.H. Park, H. Lee, D.J. Anderson, M.I. Simon, A.I. Basbaum, and S.K. Han TRPV1-expressing primary afferents generate behavioral responses to pruritogens via multiple mechanisms Proc. Natl. Acad. Sci. U. S. A. 106 2009 11330 11335
32. E.T. Iwamoto Characterization of the antinociception induced by nicotine in the pedunculopontine tegmental nucleus and the nucleus raphe magnus J. Pharmacol. Exp. Ther. 257 1991 120 133
33. J.H. Jeong, K.B. Choi, B.C. Yi, C.H. Chun, K.Y. Sung, J.Y. Sung, Y.M. Gimm, I.H. Huh, and U.D. Sohn Effects of extremely low frequency magnetic fields on pain thresholds in mice: roles of melatonin and opioids J. Auton. Pharmacol. 20 2000 259 264 (Pubitemid 34209008)
34. A.M. Konecka, and I. Sroczynska Circadian rhythm of pain in male mice Gen. Pharmacol. 31 1998 809 810 (Pubitemid 28520062)
35. B. Le Foll, C.E. Wertheim, and S.R. Goldberg Effects of baclofen on conditioned rewarding and discriminative stimulus effects of nicotine in rats Neurosci. Lett. 443 2008 236 240
36. C. Mannucci, A. Pieratti, F. Firenzuoli, A.P. Caputi, and G. Calapai Serotonin mediates beneficial effects of Hypericum perforatum on nicotine withdrawal signs Phytomedicine 14 2007 645 651 (Pubitemid 47432840)
37. A. Markou Neurobiology of nicotine dependence Philos. Trans. R. Soc. Lond. B Biol. Sci. 363 2008 3159 3168
38. F.H. Marshall, K.A. Jones, K. Kaupmann, and B. Bettler GABAB receptors - the first 7TM heterodimers Trends Pharmacol. Sci. 20 1999 396 399 (Pubitemid 29450359)
39. K. Marttila, H. Raattamaa, and L. Ahtee Effects of chronic nicotine administration and its withdrawal on striatal FosB/DeltaFosB and c-Fos expression in rats and mice Neuropharmacology 51 2006 44 51
40. L.M. Marubio, M. del Mar Arroyo-Jimenez, M. Cordero-Erausquin, C. Léna, N. Le Novère, A. de Kerchove d'Exaerde, M. Huchet, M.I. Damaj, and J.P. Changeux Reduced antinociception in mice lacking neuronal nicotinic receptor subunits Nature 398 1999 805 810
41. D.S. McGehee, M.J. Heath, S. Gelber, P. Devay, and L.W. Role Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors Science 269 1995 1692 1696
42. C. Mombereau, K. Kaupmann, W. Froestl, G. Sansig, H. Van der Putten, and J.F. Cryan Genetic and pharmacological evidence of a role for GABA(B) receptors in the modulation of anxiety- and antidepressant-like behavior Neuropsychopharmacology 29 2004 1050 1062 (Pubitemid 38670043)
43. C. Mombereau, L. Lhuillier, K. Kaupmann, and J.F. Cryan GABAB 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)
44. C.J. Murray, and A.D. Lopez Alternative projections of mortality and disability by cause 1990-2020: Global Burden of Disease Study Lancet 349 1997 1498 1504 (Pubitemid 27216360)
45. E.J. Nestler Genes and addiction Nat. Genet. 26 2000 277 281
46. 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)
47. G. Panagis, A. Kastellakis, C. Spyraki, and G. Nomikos Effects of methyllycaconitine (MLA), an alpha 7 nicotinic receptor antagonist, on nicotine- and cocaine-induced potentiation of brain stimulation reward Psychopharmacology (Berl.) 149 2000 388 396 (Pubitemid 30331429)
48. H.J. Park, D.S. Cha, and H. Jeon Antinociceptive and hypnotic properties of Celastrus orbiculatus J. Ethnopharmacol. 137 2011 1240 1244
49. K.R. Paudel, S. Bhattacharya, G. Rauniar, and B. Das Comparison of antinociceptive effect of the antiepileptic drug gabapentin to that of various dosage combinations of gabapentin with lamotrigine and topiramate in mice and rats J. Neurosci. Rural Pract. 2 2011 130 136
50. G. Paxinos, and K. Franklin The Mouse Brain in Stereotaxic Coordinates second ed. 2004 Academic Press London
51. S. Pellow, P. Chopin, S.E. File, and M. Briley Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat J. Neurosci. Methods 14 1985 149 167 (Pubitemid 16239568)
52. M.R. Picciotto, and W.A. Corrigall Neuronal systems underlying behaviors related to nicotine addiction: neural circuits and molecular genetics J. Neurosci. 22 2002 3338 3341 (Pubitemid 37465738)
53. M.R. Picciotto, M. Zoli, C. Léna, A. Bessis, Y. Lallemand, N. Le Novère, P. Vincent, E.M. Pich, P. Brûlet, and J.P. Changeux Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain Nature 374 1995 65 67
54. 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)
55. F.E. Pontieri, G. Tanda, F. Orzi, and G. Di Chiara Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs Nature 382 1996 255 257 (Pubitemid 26251360)
56. M. Rubinstein, J.S. Mogil, M. Japón, E.C. Chan, R.G. Allen, and M.J. Low Absence of opioid stress-induced analgesia in mice lacking beta-endorphin by site-directed mutagenesis Proc. Natl. Acad. Sci. U. S. A. 93 1996 3995 4000 (Pubitemid 26144234)
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. O. Salminen, T. Seppä, H. Gäddnäs, and L. Ahtee The effects of acute nicotine on the metabolism of dopamine and the expression of Fos protein in striatal and limbic brain areas of rats during chronic nicotine infusion and its withdrawal J. Neurosci. 19 1999 8145 8151 (Pubitemid 30225810)
59. O. Salminen, T. Seppä, H. Gäddnäs, and L. Ahtee Effect of acute nicotine on Fos protein expression in rat brain during chronic nicotine and its withdrawal Pharmacol. Biochem. Behav. 66 2000 87 93 (Pubitemid 30317521)
60. B.E. Schroeder, J.M. Binzak, and A.E. Kelley A common profile of prefrontal cortical activation following exposure to nicotine- or chocolate-associated contextual cues Neuroscience 105 2001 535 545 (Pubitemid 32769820)
61. V. Schuler, C. Lüscher, C. Blanchet, N. Klix, G. Sansig, K. Klebs, M. Schmutz, J. Heid, C. Gentry, L. Urban, A. Fox, W. Spooren, A.L. Jaton, J. Vigouret, M. Pozza, P.H. Kelly, J. Mosbacher, W. Froestl, E. Käslin, R. Korn, S. Bischoff, K. Kaupmann, H. Van der Putten, and B. Bettler Epilepsy, hyperalgesia, impaired memory, and loss of pre- and postsynaptic GABA(B) responses in mice lacking GABA(B(1)) Neuron 31 2001 47 58 (Pubitemid 32757088)
62. SENASA (Resolución 617/2002): Requisitos, condiciones y procedimientos para la habilitación técnica de laboratorios que posean bioterios de producción, mantenimiento y local de experimentación.
63. F. Simonin, O. Valverde, C. Smadja, S. Slowe, I. Kitchen, A. Dierich, M. Le Meur, B.P. Roques, R. Maldonado, and B.L. Kieffer Disruption of the kappa-opioid receptor gene in mice enhances sensitivity to chemical visceral pain, impairs pharmacological actions of the selective kappa-agonist U-50,488H and attenuates morphine withdrawal EMBO J. 17 1998 886 897 (Pubitemid 28077643)
64. T.A. Slotkin, and F.J. Seidler A unique role for striatal serotonergic systems in the withdrawal from adolescent nicotine administration Neurotoxicol. Teratol. 29 2007 10 16 (Pubitemid 46205155)
65. 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)
66. O. Tajima, N. Egashira, Y. Ohmi, Y. Fukue, K. Mishima, K. Iwasaki, M. Fujiwara, J. Inokuchi, Y. Sugiura, K. Furukawa, and K. Furukawa Reduced motor and sensory functions and emotional response in GM3-only mice: emergence from early stage of life and exacerbation with aging Behav. Brain Res. 198 2009 74 82
67. J.M. Trigo, A. Zimmer, and R. Maldonado Nicotine anxiogenic and rewarding effects are decreased in mice lacking beta-endorphin Neuropharmacology 56 2009 1147 1153
68. A.P. Varani, and G.N. Balerio GABAB 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.M. Moutinho, M. Calvo, and G.N. Balerio Ability of baclofen to prevent somatic manifestations and neurochemical changes during nicotine withdrawal Drug Alcohol Depend. 119 2011 e5 12