Heteromeric nicotinic receptors are involved in the sensitization and addictive properties of MDMA in mice

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 44, Issue , 2013, Pages 201-209

  Ciudad Roberts, Andrés ^a   Camarasa, Jorge ^a   Pubill, David ^a   Escubedo, Elena ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Addiction; MDMA; Nicotinic receptors; Sensitization

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; BUNGAROTOXIN RECEPTOR; DIHYDRO BETA ERYTHROIDINE; NICOTINE; NICOTINIC RECEPTOR; VARENICLINE;

ADDICTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; CORPUS STRIATUM; HIPPOCAMPUS; HYPERACTIVITY; MALE; MOUSE; NONHUMAN; PLACE PREFERENCE; RECEPTOR DENSITY;

ANALYSIS OF VARIANCE; ANIMALS; BENZAZEPINES; BRAIN; CHOLINERGIC AGENTS; CONDITIONING, OPERANT; DIHYDRO-BETA-ERYTHROIDINE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; HALLUCINOGENS; HYPERKINESIS; MALE; MICE; MOTOR ACTIVITY; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; PROTEIN BINDING; QUINOXALINES; RECEPTORS, NICOTINIC; SUBSTANCE-RELATED DISORDERS; TRITIUM;

EID: 84875589728     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2013.02.013     Document Type: Article

References (60)

1. Avale M.E., Faure P., Pons S., Robledo P., Deltheil T., David D.J., et al. Interplay of beta2* nicotinic receptors and dopamine pathways in the control of spontaneous locomotion. Proc Natl Acad Sci U S A 2008, 105:15991-15996.
2. Avila A.M., Dávila-García M.I., Ascarrunz V.S., Xiao Y., Kellar K.J. Differential regulation of nicotinic acetylcholine receptors in PC12 cells by nicotine and nerve growth factor. Mol Pharmacol 2003, 64:974-986.
3. Balfour D.J., Wright A.E., Benwell M.E., Birrell C.E. The putative role of extra-synaptic mesolimbic dopamine in the neurobiology of nicotine dependence. Behav Brain Res 2000, 113:73-83.
4. Ball K.T., Wellman C.L., Fortenberry E., Rebec G.V. Sensitizing regimens of (±)3,4-methylenedioxymethamphetamine (Ecstasy) elicit enduring and differential structural alterations in the brain motive circuit of the rat. Neuroscience 2009, 160:264-274.
5. Bankson M.G., Cunningham K.A. 3,4-Methylenedioxymethamphetamine (MDMA) as a unique model of serotonin receptor function and serotonin-dopamine interactions. J Pharmacol Exp Ther 2001, 297:846-852.
6. Biala G., Staniak N., Budzynska B. Effects of varenicline and mecamylamine on the acquisition, expression and reinstatement of nicotine-conditioned place preference by drug priming in rats. Naunyn Schmiedebergs Arch Pharmacol 2010, 381:361-370.
7. Bilsky E.J., Montegut M.J., Nichols M.L., Reid L.D. CGS 10746B, a novel dopamine release inhibitor, blocks the establishment of cocaine and MDMA conditioned place preferences. Pharmacol Biochem Behav 1998, 59:215-220.
8. Birrell C.E., Balfour D.J. The influence of nicotine pretreatment on mesoaccumbens dopamine overflow and locomotor responses to d-amphetamine. Psychopharmacology (Berl) 1998, 140:142-149.
9. Cadoni C., Solinas M., Di Chiara G. Psychostimulant sensitization: differential changes in accumbal shell and core dopamine. Eur J Pharmacol 2000, 388:69-76.
10. Camarasa J., García-Ratés S., Pubill D., Escubedo E. Study of the involvement of nicotinic receptor subtypes in the locomotor activity and analgesia induced by methamphetamine in mice. Behav Pharmacol 2009, 20:623-630.
11. Camarasa J., Ros C., Pubill D., Escubedo E. Tumour necrosis factor alpha suppression by MDMA is mediated by peripheral heteromeric nicotinic receptors. Immunopharmacol Immunotoxicol 2010, 32:265-271.
12. Champtiaux N., Gotti C., Cordero-Erausquin M., David D.J., Przybylski C., Léna C., et al. Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J Neurosci 2003, 23:7820-7829.
13. Chipana C., Camarasa J., Pubill D., Escubedo E. Memantine prevents MDMA-induced neurotoxicity. Neurotoxicology 2008, 29:179-183.
14. Chipana C., García-Ratés S., Camarasa J., Pubill D., Escubedo E. Different oxidative profile and nicotinic receptor interaction of amphetamine and 3,4-methylenedioxy-methamphetamine. Neurochem Int 2008, 52:401-410.
15. Chipana C., Torres I., Camarasa J., Pubill D., Escubedo E. Memantine protects against amphetamine derivatives-induced neurotoxic damage in rodents. Neuropharmacology 2008, 54:1254-1263.
16. Damaj M.I., Kao W., Martin B.R. Characterization of spontaneous and precipitated nicotine withdrawal in the mouse. J Pharmacol Exp Ther 2003, 307:526-534.
17. 3H]methyllycaconitine: a new radioligand for labelling alpha 7-type neuronal nicotinic acetylcholine receptors. Neuropharmacology 1999, 38:679-690.
18. Day J., Damsma G., Fibiger H.C. Cholinergic activity in the rat hippocampus, cortex and striatum correlates with locomotor activity: an in vivo microdialysis study. Pharmacol Biochem Behav 1991, 38:723-729.
19. 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 U S A 1998, 85:5274-5278.
20. Dougherty J.J., Wu J., Mehta T.K., Brown B., Nichols R.A. Chronic nicotine alters nicotinic receptor-induced presynaptic Ca2+ responses in isolated nerve terminals. Neurochem Res 2008, 33:1106-1112.
21. Escubedo E., Camarasa J., Chipana C., García-Ratés S., Pubill D. Involvement of nicotinic receptors in methamphetamine and MDMA induced neurotoxicity. Pharmacological implications. Int Rev Neurobiol 2009, 88:121-166.
22. Gaimarri A., Moretti M., Riganti L., Zanardi A., Clementi F., Gotti C. Regulation of neuronal nicotinic receptor traffic and expression. Brain Res Rev 2007, 55:134-143.
23. García-Ratés S., Camarasa J., Escubedo E., Pubill D. Methamphetamine and 3,4-methylenedioxymethamphetamine interact with central nicotinic receptors and induce their up-regulation. Toxicol Appl Pharmacol 2007, 223:195-205.
24. Goto Y., Grace A.A. Limbic and cortical information processing in the nucleus accumbens. Trends Neurosci 2008, 31:552-558.
25. Gould T.J., Portugal G.S., André J.M., Tadman M.P., Marks M.J., Kenney J.W., et al. The duration of nicotine withdrawal-associated deficits in contextual fear conditioning parallels changes in hippocampal high affinity nicotinic acetylcholine receptor upregulation. Neuropharmacology 2012, 62:2118-2125.
26. Govind A.P., Vezina P., Green W.N. Nicotine-induced upregulation of nicotinic receptors: underlying mechanisms and relevance to nicotine addiction. Biochem Pharmacol 2009, 78:756-765.
27. Isola R., Vogelsberg V., Wemlinger T.A., Neff N.H., Hadjiconstantinou M. Nicotine abstinence in the mouse. Brain Res 1999, 850:189-196.
28. Johnson M.P., Hoffman A.J., Nichols D.E. Effects of the enantiomers of MDA, MDMA and related analogues on [3H]serotonin and [3H]dopamine release from superfused rat brain slices. Eur J Pharmacol 1986, 132:269-276.
29. Jutkiewicz E.M., Nicolazzo D.M., Kim M.N., Gnegy M.E. Nicotine and amphetamine acutely cross-potentiate their behavioral and neurochemical responses in female Holtzman rats. Psychopharmacology (Berl) 2008, 200:93-103.
30. Kalivas P.W., Duffy P., White S.R. MDMA elicits behavioral and neurochemical sensitization in rats. Neuropsychopharmacology 1998, 18:469-479.
31. Karler R., Calder L.D., Bedingfield J.B. A novel nicotinic cholinergic role in behavioral sensitization to amphetamine-induced stereotypy in mice. Brain Res 1996, 725:192-198.
32. Kim M.N., Jutkiewicz E.M., Zhang M., Gnegy M.E. The sensitizing effect of acute nicotine on amphetamine-stimulated behavior and dopamine efflux requires activation of b2 subunit-containing nicotinic acetylcholine receptors and glutamate N-methyl-d-aspartate receptors. Neuropharmacology 2011, 60:1126-1134.
33. Kita H., Kitai S.T. Amygdaloid projections to the frontal cortex and the striatum in the rat. J Comp Neurol 1990, 298:40-49.
34. Klingler W., Heffron J.J., Jurkat-Rott K., O'sullivan G., Alt A., Schlesinger F., et al. 3,4-Methylenedioxymethamphetamine (Ecstasy) activates skeletal muscle nicotinic acetylcholine receptors. J Pharmacol Exp Ther 2005, 314:1267-1273.
35. Laviolette S.R. Dopamine modulation of emotional processing in cortical and subcortical neural circuits: evidence for a final common pathway in schizophrenia?. Schizophr Bull 2007, 33:971-981.
36. Malin D.H., Lake J.R., Upchurch T.P., Shenoi M., Rajan N., Schweinle W.E. Nicotine abstinence syndrome precipitated by the competitive nicotinic antagonist dihydro-beta-erythroidine. Pharmacol Biochem Behav 1998, 60:609-613.
37. McGinty V.B., Grace A.A. Selective activation of medial prefrontal-to-accumbens projection neurons by amygdala stimulation and Pavlovian conditioned stimuli. Cereb Cortex 2008, 18:1961-1972.
38. Megirian D., Leary D.E., Slater I.H. The action of some derivatives of beta-erythroidine on peripheral neuro-effector systems. J Pharmacol Exp Ther 1955, 113:212-227.
39. Mihalak K.B., Carroll F.I., Luetje C.W. Varenicline is a partial agonist at alpha4beta2 and a full agonist at alpha7 neuronal nicotinic receptors. Mol Pharmacol 2006, 70:801-805.
40. Miller D.K., Segert I.L. Mecamylamine attenuates ephedrine-induced hyperactivity in rats. Pharmacol Biochem Behav 2005, 81:165-169.
41. Picciotto M.R., Zoli M., Changeux J.P. Use of knock-out mice to determine the molecular basis for the actions of nicotine. Nicotine Tob Res 1999, 1(Suppl. 2):121-125.
42. Pubill D., Garcia-Ratés S., Camarasa J., Escubedo E. Neuronal nicotinic receptors as new targets for amphetamine-induced oxidative damage and neurotoxicity. Pharmaceuticals 2011, 4:822-847.
43. Pubill D., Garcia-Ratés S., Camarasa J., Escubedo E. 3,4-Methylenedioxy-methamphetamine induces in vivo regional up-regulation of central nicotinic receptors in rats and potentiates the regulatory effects of nicotine on these receptors. Neurotoxicology 2013, 35:41-49.
44. Rao T.S., Correa L.D., Adams P., Santori E.M., Sacaan A.I. Pharmacological characterization of dopamine, norepinephrine and serotonin release in the rat prefrontal cortex by neuronal nicotinic acetylcholine receptor agonists. Brain Res 2003, 990:203-208.
45. Robinson T.E., Berridge K.C. Addiction. Annu Rev Psychol 2003, 54:25-53.
46. Robledo P., Balerio G., Berrendero F., Maldonado R. Study of the behavioural responses related to the potential addictive properties of MDMA in mice. Naunyn Schmiedebergs Arch Pharmacol 2004, 369:338-349.
47. Rollema H., Chambers L.K., Coe J.W., Glowa J., Hurst R.S., Lebel L.A., et al. Pharmacological profile of the alpha4beta2 nicotinic acetylcholine receptor partial agonist varenicline, an effective smoking cessation aid. Neuropharmacology 2007, 52:985-994.
48. Salzmann J., Marie-Claire C., Le Guen S., Roques B.P., Noble F. Importance of ERK activation in behavioral and biochemical effects induced by MDMA in mice. Br J Pharmacol 2003, 140:831-838.
49. Schoffelmeer A.N., De Vries T.J., Wardeh G., van de Ven H.W., Vanderschuren L.J. Psychostimulant-induced behavioral sensitization depends on nicotinic receptor activation. J Neurosci 2002, 22:3269-3276.
50. Scholey A.B., Parrott A.C., Buchanan T., Heffernan T.M., Ling J., Rodgers J. Increased intensity of Ecstasy and polydrug usage in the more experienced recreational Ecstasy/MDMA users: a WWW study. Addict Behav 2004, 29:743-752.
51. Vanderschuren L.J., Kalivas P.W. Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacology (Berl) 2000, 151:99-120.
52. 2 receptors in mice. Behav Pharmacol 2011, 22:362-369.
53. Vidal-Infer A., Roger-Sánchez C., Daza-Losada M., Aguilar M.A., Miñarro J., Rodríguez-Arias M. Role of the dopaminergic system in the acquisition, expression and reinstatement of MDMA-induced conditioned place preference in adolescent mice. PLoS One 2012, 7:e43107.
54. Walters C.L., Brown S., Changeux J.P., Martin B., Damaj M.I. The beta2 but not alpha7 subunit of the nicotinic acetylcholine receptor is required for nicotine-conditioned place preference in mice. Psychopharmacology (Berl) 2006, 184:339-344.
55. Williams M.J., Adinoff B. The role of acetylcholine in cocaine addiction. Neuropsychopharmacology 2008, 33:1779-1797.
56. Wise R.A., Bozarth M.A. A psychomotor stimulant theory of addiction. Psychol Rev 1987, 94:469-492.
57. Wooters T.E., Bardo M.T. Nicotinic receptors differentially modulate the induction and expression of behavioral sensitization to methylphenidate in rats. Psychopharmacology (Berl) 2009, 204:551-562.
58. Zachariou V., Caldarone B.J., Weathers-Lowin A., George T.P., Elsworth J.D., Roth R.H., et al. Nicotine receptor inactivation decreases sensitivity to cocaine. Neuropsychopharmacology 2001, 24:576-589.
59. Zaniewska M., McCreary A.C., McCreary A.C., Stefański R., Przegaliński E., Filip M., et al. Effect of varenicline on the acute and repeated locomotor responses to nicotine in rats. Synapse 2008, 62:935-939.
60. Zhang L., Dong Y., Doyon W.M., Dani J.A. Withdrawal from chronic nicotine exposure alters dopamine signaling dynamics in the nucleus accumbens. Biol Psychiatry 2012, 71:184-191.