Endogenous cannabinoid and opioid systems and their role in nicotine addiction

Current Drug Targets

Volumn 11, Issue 4, 2010, Pages 440-449

  Maldonado, Rafael ^a   Berrendero, Fernando ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

Addiction; Cannabinoid; Nicotine; Opioid; Relapse; Reward; Self administration; Withdrawal syndrome

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE METHANESULFONATE; CANNABINOID; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; DRONABINOL; METHYLLYCACONITINE; MORPHINE; NALOXONE; NALTREXONE; NICOTINE; NORBINALTORPHIMINE; OPIATE; RIMONABANT;

ANTINOCICEPTION; ANXIETY DISORDER; CLINICAL TRIAL; DEPRESSION; DRUG EFFECT; DRUG INHIBITION; DRUG MECHANISM; HUMAN; NAUSEA; NEUROTRANSMISSION; NONHUMAN; REVIEW; TOBACCO DEPENDENCE;

ANIMALS; BEHAVIOR, ADDICTIVE; BRAIN; DOPAMINE; ENDOCANNABINOIDS; HUMANS; OPIOID PEPTIDES; RECURRENCE; REINFORCEMENT (PSYCHOLOGY); REWARD; SIGNAL TRANSDUCTION; SMOKING CESSATION; SUBSTANCE WITHDRAWAL SYNDROME; TOBACCO USE DISORDER;

EID: 77950788196     PISSN: 13894501     EISSN: None     Source Type: Journal    
DOI: 10.2174/138945010790980358     Document Type: Review

References (118)

1. McLellan AT, Lewis DC, O'Brien CP, Kleber HD. Drug dependence, a chronic medical illness: implications for treatment, insurance, and outcomes evaluation. JAMA 2000; 284: 1689-1695
2. Hatsukami DK, Stead LF, Gupta PC. Tobacco addiction. Lancet 2008; 371: 2027-2038
3. Malin DH. Nicotine dependence: studies with a laboratory model. Pharmacol Biochem Behav 2001; 70: 551-559 (Pubitemid 34131648)
4. Millar NS, Gotti C. Diversity of vertebrate nicotinic acetylcholine receptors. Neuropharmacology 2009; 56: 237-246
5. Steinlein OK, Bertrand D. Neuronal nicotinic acetylcholine receptors: from the genetic analysis to neurological diseases. Biochem Pharmacol 2008; 76: 1175-1183
6. Maskos U. Emerging concepts: novel integration of in vivo approaches to localize the function of nicotinic receptors. J Neurochem 2007; 100: 596-602. (Pubitemid 46095612)
7. Picciotto MR, Zoli M, Rimondini R, Léna C, Marubio LM, Pich EM, et al. Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 1998; 391: 173-177
8. McGehee DS, Role LW. Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu Rev Physiol 1995; 57: 521-546
9. Markou A. Review. Neurobiology of nicotine dependence. Philos Trans R Soc Lond B Biol Sci 2008; 363: 3159-3168
10. 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 1988; 85: 5274-5278
11. Nisell M, Nomikos GG, Svensson TH. Systemic nicotine-induced dopamine release in the rat nucleus accumbens is regulated by nicotinic receptors in the ventral tegmental area. Synapse 1994; 16: 36-44. (Pubitemid 24013237)
12. Mansvelder HD, McGehee DS. Cellular and synaptic mechanisms of nicotine addiction. J Neurobiol 2003; 53: 606-617
13. Laviolette SR, van der Kooy, D. The neurobiology of nicotine addiction: bridging the gap from molecules to behaviour. Nat Rev Neurosci 2004; 5: 55-65.
14. Schilström B, Svensson HM, Svensson TH, Nomikos GG. Nicotine and food induced dopamine release in the nucleus accumbens of the rat: putative role of alpha7 nicotinic receptors in the ventral tegmental area. Neuroscience 1998; 85: 1005-1009 (Pubitemid 28293408)
15. Nomikos GG, Schilström B, Hildebrand BE, Panagis G, Grenhoff J, Svensson, TH. Role of alpha7 nicotinic receptors in nicotine dependence and implications for psychiatric illness. Behav Brain Res 2000; 113: 97-103.
16. Paterson NE, Semenova S, Gasparini F, Markou A. The mGluR5 antagonist MPEP decreased nicotine self-administration in rats and mice Psychopharmacology (Berl) 2003; 167: 257-264
17. Kenny PJ, Chartoff E, Roberto M, Carlezon WA Jr, Markou A. NMDA receptors regulate nicotine-enhanced brain reward function and intravenous nicotine self-administration: role of the ventral tegmental area and central nucleus of the amygdala. Neuropsychopharmacology 2009; 34: 266-281
18. Lança AJ, Adamson KL, Coen KM, Chow BL, Corrigall WA. The pedunculopontine tegmental nucleus and the role of cholinergic neurons in nicotine self-administration in the rat: a correlative neuroanatomical and behavioral study. Neuroscience 2000; 96: 735-742
19. Picciotto MR, Corrigall WA. Neuronal systems underlying behaviors related to nicotine addiction: neural circuits and molecular genetics. J Neurosci 2002; 22: 3338-3341
20. Mansvelder HD, Keath JR, McGehee DS. Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 2002; 33: 905-919
21. Quick MW, Lester RA. Desensitisation of neuronal nicotinic receptors. J Neurobiol 2002; 53: 457-478
22. Robinson SE, Vann RE, Britton AF, O'Connell MM, James JR, Rosecrans JA. Cellular nicotinic receptor desensitisation correlates with nicotine-induced acute behavioral tolerance in rats. Psychopharmacology (Berl) 2007; 192: 71-78
23. Shiffman S, West R, Gilbert D. Recommendation for the assessment of tobacco craving and withdrawal in smoking cessation trials. Nicotine Tob Res 2004; 6: 599-614.
24. Malin DH, Lake JR, Newlin-Maultsby P, Roberts LK, Lanier JG, Carter VA, et al. Rodent model of nicotine abstinence syndrome. Pharmacol Biochem Behav 1992; 43: 779-784
25. Jackson KJ, Martin BR, Changeux JP, Damaj MI. Differential role of nicotinic acetylcholine receptor subunits in physical and affective nicotine withdrawal signs. J Pharmacol Exp Ther 2008; 325: 302-312
26. Johnson PM, Hollander JA, Kenny PJ. Decreased brain reward function during nicotine withdrawal in C57BL6 mice: evidence from intracranial self-stimulation (ICSS) studies. Pharmacol Biochem Behav 2008; 90: 409-415
27. Markou A, Kosten TR, Koob GF. Neurobiological similarities in depression and drug dependence: a self-medication hypothesis. Neuropsychopharmacology 1998; 18: 135-174
28. Bruijnzeel AW, Zislis G, Wilson C, Gold MS. Antagonism of CRF receptors prevents the deficit in brain reward function associated with precipitated nicotine withdrawal in rats. Neuropsychopharmacology 2007; 32: 955-963
29. Panagis G, Hildebrand BE, Svensson TH, Nomikos GG. Selective c-fos induction and decreased dopamine release in the central nucleus of amygdala in rats displaying a mecamylamine-precipitated nicotine withdrawal syndrome. Synapse 2000; 35: 15-25.
30. Hildebrand BE, Panagis G, Svensson TH, Nomikos GG. Behavioral and biochemical manifestations of mecamylamine-precipitated nicotine withdrawal in the rat: role of nicotinic receptors in the ventral tegmental area. Neuropsychopharmacology 1999; 21: 560-574
31. Liechti ME, Markou A. Role of the glutamatergic system in nicotine dependence: implications for the discovery and development of new pharmacological smoking cessation therapies. CNS Drugs 2008; 22: 705-724
32. Dravolina OA, Zakharova ES, Shekunova EV, Zvartau EE, Danysz W, Bespalov AY. mGlu1 receptor blockade attenuates cue- and nicotine-induced reinstatement of extinguished nicotine self-administration behavior in rats. Neuropharmacology 2007; 52: 263-269
33. Bilkei-Gorzo A, Rácz I, Michel K, Darvas M, Maldonado R, Zimmer A. A common genetic predisposition to stress sensitivity and stress-induced nicotine craving. Biol Psychiatry 2008; 63: 164-171
34. Martín-García E, Barbano MF, Galeote L, Maldonado R. New operant model of nicotine-seeking behaviour in mice. Int J Neuropsychopharmacol 2009; 12: 343-356
35. Caggiula AR, Donny EC, White AR, Chaudhri N, Booth S, Gharib MA, et al. Cue dependency of nicotine self-administration and smoking. Pharmacol Biochem Behav 2001; 70: 515-530
36. Paterson NE, Froestl W, Markou A. Repeated administration of the GABAB receptor agonist CGP44532 decreased nicotine self-administration, and acute administration decreased cue-induced reinstatement of nicotine-seeking in rats. Neuropsychopharmacology 2005; 30: 119-128
37. Bespalov AY, Dravolina OA, Sukhanov I., Zakharova E, Blokhina E, Zvartau E, et al. Metabotropic glutamate receptor (mGluR5) antagonist MPEP attenuated cue- and schedule-induced reinstatement of nicotine self-administration behavior in rats. Neuropharmacology 2005; 49 Suppl 1: 167-178
38. Liechti ME, Lhuillier L, Kaupmann K, Markou A. Metabotropic glutamate 2/3 receptors in the ventral tegmental area and the nucleus accumbens shell are involved in behaviors relating to nicotine dependence. J Neurosci 2007; 27: 9077-9085
39. Pacher P, Bátkai S, Kunos G. The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol Rev 2006; 58: 389-462.
40. Fride E, Mechoulam R. In: Maldonado R Ed, Molecular biology of drug addiction. Humana Press. Totowa, New Jersey 2003; 173-198
41. Van Sickle MD, Duncan M, Kingsley PJ, Mouihate A, Urbani P, Mackie K, et al. Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 2005; 310: 329-332
42. Begg M, Pacher P, Bátkai S, Osei-Hyiaman D, Offertáler L, Mo FM, et al. Evidence for novel cannabinoid receptors. Pharmacol Ther 2005; 106: 133-145
43. Ryberg E, Larsson N, Sjögren S, Hjorth S, Hermansson NO, Leonova J, et al. The orphan receptor GPR55 is a novel cannabinoid receptor Br J Pharmacol 2007; 152: 1092-1101
44. Pertwee RG. Ligands that target cannabinoid receptors in the brain: from THC to anandamide and beyond. Addict Biol 2008; 13: 147-159
45. Wilson RI, Nicoll RA. Endocannabinoid signaling in the brain. Science 2002; 296: 678-682
46. Maldonado R, Valverde O, Berrendero F. Involvement of the endocannabinoid system in drug addiction. Trends Neurosci 2006; 29: 225-232
47. Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F, et al. Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 1999; 283: 401-404
48. Pryor GT, Larsen FF, Husain S, Braude, MC. Interactions of delta9-tetrahydrocannabinol with d-amphetamine, cocaine, and nicotine in rats. Pharmacol Biochem Behav 1978; 8: 295-318.
49. Valjent E, Mitchell JM, Besson MJ, Caboche J, Maldonado R. Behavioural and biochemical evidence for interactions between Delta 9-tetrahydrocannabinol and nicotine. Br J Pharmacol 2002; 135: 564-578
50. Balerio GN, Aso E, Maldonado R. Role of the cannabinoid system in the effects induced by nicotine on anxiety-like behaviour in mice. Psychopharmacology (Berl) 2006; 184: 504-513
51. Marco EM, Llorente R, Moreno E, Biscaia JM, Guaza C, Viveros MP. Adolescent exposure to nicotine modifies acute functional responses to cannabinoid agonists in rats. Behav Brain Res 2006; 172: 46-53.
52. Merritt LL, Martin BR, Walters C, Lichtman AH, Damaj MI. The endogenous cannabinoid system modulates nicotine reward and dependence. J Pharmacol Exp Ther 2008; 326: 483-492
53. Scherma M, Panlilio LV, Fadda P, Fattore L, Gamaleddin I, Le Foll B, et al. Inhibition of anandamide hydrolysis by cyclohexyl carbamic acid 3′-carbamoyl-3-yl ester (URB597) reverses abuse-related behavioral and neurochemical effects of nicotine in rats. J Pharmacol Exp Ther 2008; 327: 482-490
54. Spivak CE, Lupica CR, Oz M. The endocannabinoid anandamide inhibits the function of alpha4beta2 nicotinic acetylcholine receptors. Mol Pharmacol 2007; 72: 1024-1032 (Pubitemid 47481425)
55. Butt C, Alptekin A, Shippenberg T, Oz M. Endogenous cannabinoid anandamide inhibits nicotinic acetylcholine receptor function in mouse thalamic synaptosomes. J Neurochem 2008; 105: 1235-1243
56. Castañé A, Valjent E, Ledent C, Parmentier M, Maldonado R, Valverde O. Lack of CB1 cannabinoid receptors modifies nicotine behavioural responses, but not nicotine abstinence. Neuropharmacology 2002; 43: 857-867
57. Cossu G, Ledent C, Fattore L, Imperato A, Böhme GA, Parmentier M, et al. Cannabinoid CB1 receptor knockout mice fail to self-administer morphine but not other drugs of abuse. Behav Brain Res 2001; 118: 61-65
58. Cohen C, Perrault G, Voltz C, Steinberg R, Soubrié P. SR141716, a central cannabinoid (CB(1)) receptor antagonist, blocks the motivational and dopamine-releasing effects of nicotine in rats. Behav Pharmacol 2002; 13: 451-463
59. Le Foll B, Goldberg SR. Rimonabant, a CB1 antagonist, blocks nicotine-conditioned place preferences. Neuroreport 2004; 15: 2139-2143
60. Forget B, Hamon M, Thiébot MH. Cannabinoid CB1 receptors are involved in motivational effects of nicotine in rats. Psychopharmacology (Berl) 2005; 181: 722-734
61. Forget B, Barthélémy S, Saurini F, Hamon M, Thiébot MH. Differential involvement of the endocannabinoid system in short- and long-term expression of incentive learning supported by nicotine in rats. Psychopharmacology (Berl) 2006; 189: 59-69.
62. Solinas M, Scherma M, Fattore L, Stroik J, Wertheim C, Tanda G, et al. Nicotinic alpha 7 receptors as a new target for treatment of cannabis abuse. J Neurosci 2007; 27: 5615-5620
63. Cheer JF, Wassum KM, Sombers LA, Heien ML, Ariansen JL, Aragona BJ, et al. Phasic dopamine release evoked by abused substances requires cannabinoid receptor activation. J Neurosci 2007; 27: 791-795
64. Cahill K, Ussher M. Cannabinoid type 1 receptor antagonists (rimonabant) for smoking cessation. Cochrane Database Syst Rev 2007; 4:CD005353.
65. Balerio GN, Aso E, Berrendero F, Murtra P, Maldonado R. Delta9-tetrahydrocannabinol decreases somatic and motivational manifestations of nicotine withdrawal in mice. Eur J Neurosci 2004; 20: 2737-2748
66. Kodes E, Cohen C, Louis C, Griebel G. Cortico-limbic circuitry for conditioned nicotine-seeking behavior in rats involves endocannabinoid signaling. Psychopharmacology (Berl) 2007; 194: 161-171
67. Diergaarde L, de Vries W, Raasø H, Schoffelmeer AN, de Vries TJ. Contextual renewal of nicotine seeking in rats and its suppression by the cannabinoid-1 receptor antagonist Rimonabant (SR141716A). Neuropharmacology 2008 ; 55: 712-716
68. Cohen C, Perrault G, Griebel G, Soubrié P. Nicotine-associated cues maintain nicotine-seeking behavior in rats several weeks after nicotine withdrawal: reversal by the cannabinoid (CB1) receptor antagonist, rimonabant (SR141716). Neuropsychopharmacology 2005; 30: 145-155
69. De Vries TJ, de Vries W, Janssen MC, Schoffelmeer AN. Suppression of conditioned nicotine and sucrose seeking by the cannabinoid-1 receptor antagonist SR141716A. Behav Brain Res 2005; 161: 164-168
70. Shoaib M. The cannabinoid antagonist AM251 attenuates nicotine self-administration and nicotine-seeking behaviour in rats. Neuropharmacology 2008; 54: 438-444
71. Xue Y, Domino EF. Tobacco/nicotine and endogenous brain opioids. Prog Neuropsychopharmacol Biol Psychiatry 2008; 32: 1131-1138
72. Kieffer BL, Gavériaux-Ruff C. Exploring the opioid system by gene knockout. Prog Neurobiol 2002; 66: 285-306.
73. Meunier JC, Mollereau C, Toll L, Suaudeau C, Moisand C, Alvinerie P, et al. Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature 1995; 377: 532-535
74. Reinscheid RK, Nothacker HP, Bourson A, Ardati A, Henningsen RA, Bunzow JR, et al. Orphanin FQ: a neuropeptide that activates an opioidlike G protein-coupled receptor. Science 1995; 270: 792-794
75. Kieffer BL, Evans CJ. Opioid receptors: from binding sites to visible molecules in vivo. Neuropharmacology 2009; 56 Suppl 1:205-212
76. Mollereau C, Parmentier M, Mailleux P, Butour JL, Moisand C, Chalon P, et al. ORL1, a novel member of the opioid receptor family. Cloning, functional expression and localization. FEBS Lett 1994; 341: 33-38
77. Roth-Deri I, Green-Sadan T, Yadid G. Beta-endorphin and drug-induced reward and reinforcement. Prog Neurobiol 2008; 86: 1-21.
78. Dhatt RK, Gudehithlu KP, Wemlinger TA, Tejwani GA, Neff NH. Hadjiconstantinou M. Preproenkephalin mRNA and methionine-enkephalin content are increased in mouse striatum after treatment with nicotine. J Neurochem 1995; 64: 1878-1883
79. Houdi AA, Dasgupta R, Kindy MS. Effect of nicotine use and withdrawal on brain preproenkephalin A mRNA. Brain Res 1998; 799: 257-263
80. Isola R, Zhang H, Duchemin AM, Tejwani GA, Neff NH, Hadjiconstantinou M. Met-enkephalin and preproenkephalin mRNA changes in the striatum of the nicotine abstinence mouse. Neurosci Lett 2002; 325: 67-71.
81. Kiguchi N, Maeda T, Tsuruga M, Yamamoto A, Yamamoto C, Ozaki M, et al. Involvement of spinal Met-enkephalin in nicotine-induced antinociception in mice. Brain Res 2008; 1189: 70-77 (Pubitemid 351842550)
82. Isola R, Zhang H, Tejwani GA, Neff NH, Hadjiconstantinou M. Acute nicotine changes dynorphin and prodynorphin mRNA in the striatum. Psychopharmacology (Berl) 2009; 201: 507-516
83. Zarrindast MR, Pazouki M, Nassiri-Rad S. Involvement of cholinergic and opioid receptor mechanisms in nicotine-induced antinociception. Pharmacol Toxicol 1997; 81: 209-213 (Pubitemid 27475646)
84. Zarrindast MR, Nami AB, Farzin D. Nicotine potentiates morphine antinociception: a possible cholinergic mechanism. Eur Neuropsychopharmacol 1996; 6: 127-133 (Pubitemid 26000426)
85. Campbell VC, Taylor RE, Tizabi Y. Antinociceptive effects of alcohol and nicotine: involvement of the opioid system. Brain Res 2006; 1097: 71-77 (Pubitemid 44043109)
86. Campbell VC, Taylor RE, Tizabi Y. Effects of selective opioid receptor antagonists on alcohol-induced and nicotine-induced antinociception. Alcohol Clin Exp Res 2007; 31: 1435-1440 (Pubitemid 47063125)
87. Galeote L, Maldonado R, Berrendero F. Involvement of kappa/dynorphin system in the development of tolerance to nicotine-induced antinociception. J Neurochem 2008; 105: 1358-1368 (Pubitemid 351590804)
88. Berrendero F, Kieffer BL, Maldonado R. Attenuation of nicotine-induced antinociception, rewarding effects, and dependence in muopioid receptor knock-out mice. J Neurosci 2002; 22: 10935-10940 (Pubitemid 36005169)
89. Berrendero F, Mendizábal V, Robledo P, Galeote L, Bilkei-Gorzo A, Zimmer A, et al. Nicotine-induced antinociception, rewarding effects, and physical dependence are decreased in mice lacking the preproenkephalin gene. J Neurosci 2005; 25: 1103-1112 (Pubitemid 40268951)
90. Balerio GN, Aso E, Maldonado R. Involvement of the opioid system in the effects induced by nicotine on anxiety-like behaviour in mice. Psychopharmacology (Berl) 2005; 181: 260-269 (Pubitemid 41492196)
91. Marco EM, Llorente R, Pérez-Alvarez L, Moreno E, Guaza C, Viveros MP. The kappa-opioid receptor is involved in the stimulating effect of nicotine on adrenocortical activity but not in nicotine induced anxiety Behav Brain Res 2005; 163: 212-218
92. Filliol D, Ghozland S, Chluba J, Martin M, Matthes HW, Simonin F, et al. Mice deficient for delta- and mu-opioid receptors exhibit opposing alterations of emotional responses. Nat Genet 2000; 25: 195-200.
93. Berrendero F, Maldonado R. Involvement of the opioid system in the anxiolytic-like effects induced by Delta(9)-tetrahydrocannabinol. Psychopharmacology (Berl) 2002; 163: 111-117
94. Galeote L, Kieffer BL, Maldonado R, Berrendero F. Mu-opioid receptors are involved in the tolerance to nicotine antinociception. J Neurochem 2006; 97: 416-423
95. Biala G, Weglinska B. On the mechanism of cross-tolerance between morphine- and nicotine-induced antinociception: involvement of calcium channels. Prog Neuropsychopharmacol Biol Psychiatry 2006; 30: 15-21. (Pubitemid 43021318)
96. Bohn LM, Gainetdinov RR, Lin FT, Lefkowitz RJ, Caron MG. Mu-opioid receptor desensitisation by beta-arrestin-2 determines morphine tolerance but not dependence. Nature 2000; 408: 720-723
97. David S, Lancaster T, Stead LF, Evins AE. Opioid antagonists for smoking cessation. Cochrane Database Syst Rev 2006; 4:CD003086.
98. Covey LS, Glassman AH, Stetner F. Naltrexone effects on short-term and long-term smoking cessation. J Addict Dis 1999; 18: 31-40. (Pubitemid 29231718)
99. Wong GY, Wolter TD, Croghan GA, Croghan IT, Offord KP, Hurt RD. A randomized trial of naltrexone for smoking cessation. Addiction 1999; 94: 1227-1237 (Pubitemid 29385151)
100. King A, de Wit H, Riley RC, Cao D, Niaura R, Hatsukami D. Efficacy of naltrexone in smoking cessation: a preliminary study and an examination of sex differences. Nicotine Tob Res 2006; 8: 671-682 (Pubitemid 44480416)
101. O'Malley SS, Cooney JL, Krishna-Sarin S, Dubin JA, McKee SA, Cooney NL, et al. A controlled trial of naltrexone augmentation of nicotine replacement therapy for smoking cessation. Arch Intern Med 2006; 166: 667-674
102. Munafò MR, Elliot KM, Murphy MF, Walton RT, Johnstone EC. Association of the mu-opioid receptor gene with smoking cessation. Pharmacogenomics J 2007; 7: 353-361 (Pubitemid 47471313)
103. Walsh Z, Epstein A, Munisamy G, King A. The impact of depressive symptoms on the efficacy of naltrexone in smoking cessation J Addict Dis 2008; 27: 65-72.
104. Rukstalis M, Jepson C, Strasser A, Lynch KG, Perkins K, Patterson F, et al. Naltrexone reduces the relative reinforcing value of nicotine in a cigarette smoking choice paradigm. Psychopharmacology (Berl) 2005; 180: 41-48 (Pubitemid 40897069)
105. Walters CL, Cleck JN, Kuo YC, Blendy JA. Mu-opioid receptor and CREB activation are required for nicotine reward. Neuron 2005; 46: 933-943
106. Corrigall WA. Coen KM. Opiate antagonists reduce cocaine but not nicotine self-administration. Psychopharmacology (Berl) 1991; 104: 167-170
107. Galeote L, Berrendero F, Andreea Bura S, Zimmer A, Maldonado R. Prodynorphin gene disruption increases the sensitivity to nicotine self-administration in mice. Int J Neuropsychopharmacol 2009; 12:615-625
108. Shippenberg TS, Zapata A, Chefer VI. Dynorphin and the pathophysiology of drug addiction. Pharmacol Ther 2007; 116: 306-321
109. Mendizábal V, Zimmer A, Maldonado R. Involvement of kappa/dynorphin system in WIN 55,212-2 self-administration in mice. Neuropsychopharmacology 2006; 31: 1957-1966 (Pubitemid 44246342)
110. Liu X, Palmatier MI, Caggiula AR, Sved AF, Donny EC, Gharib M, et al. Naltrexone attenuation of conditioned but not primary reinforcement of nicotine in rats. Psychopharmacology (Berl) 2009; 202:589-598
111. Sutherland G, Stapleton JA, Russell MA, Feyerabend C. Naltrexone, smoking behaviour and cigarette withdrawal. Psychopharmacology (Berl) 1995; 120: 418-425
112. Krishnan-Sarin S, Rosen MI, O'Malley SS. Naloxone challenge in smokers. Preliminary evidence of an opioid component in nicotine dependence. Arch Gen Psychiatry 1999; 56: 663-668
113. Biała G, Budzyńska B, Kruk M. Naloxone precipitates nicotine abstinence syndrome and attenuates nicotine-induced antinociception in mice. Pharmacol Rep 2005; 57: 755-760
114. Tomé AR, Izaguirre V, Rosario LM, Ceña V, González-García C. Naloxone inhibits nicotine-induced receptor current and catecholamine secretion in bovine chromaffin cells. Brain Res 2001; 903: 62-65 (Pubitemid 32904607)
115. Malin DH, Lake JR, Carter VA, Cunningham JS, Wilson OB. Naloxone precipitates nicotine abstinence syndrome in the rat. Psychopharmacology (Berl) 1993; 112: 339-342 (Pubitemid 23278298)
116. Hildebrand BE, Nomikos GG, Bondjers C, Nisell M, Svensson TH. Behavioral manifestations of the nicotine abstinence syndrome in the rat: peripheral versus central mechanisms. Psychopharmacology (Berl) 1997; 129: 348-356 (Pubitemid 27092998)
117. Watkins SS, Stinus L, Koob GF, Markou A. Reward and somatic changes during precipitated nicotine withdrawal in rats: centrally and peripherally mediated effects. J Pharmacol Exp Ther 2000; 292: 1053-1064 (Pubitemid 30136601)
118. Isola R, Zhang H, Tejwani GA, Neff NH, Hadjiconstantinou M. Dynorphin and prodynorphin mRNA changes in the striatum during nicotine withdrawal. Synapse 2008; 62: 448-455 (Pubitemid 351614769)