Donepezil, an acetylcholinesterase inhibitor, attenuates nicotine self-administration and reinstatement of nicotine seeking in rats

Addiction Biology

Volumn 19, Issue 4, 2014, Pages 539-551

  Kimmey, Blake A ^a   Rupprecht, Laura E ^a   Hayes, Matthew R ^a   Schmidt, Heath D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Acetylcholine; nicotine addiction; relapse; self administration; smoking cessation

Indexed keywords

DONEPEZIL; NICOTINE; SUCROSE; CHOLINESTERASE INHIBITOR; INDAN DERIVATIVE; PIPERIDINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG SEEKING BEHAVIOR; DRUG SELF ADMINISTRATION; FEEDING BEHAVIOR; FOOD INTAKE; MALAISE; MALE; NAUSEA; NICOTINE SEEKING BEHAVIOR; NONHUMAN; PICA; PRIORITY JOURNAL; RAT; RELAPSE; SUCROSE SEEKING BEHAVIOR; WITHDRAWAL SYNDROME; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; ASSOCIATION; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; INSTRUMENTAL CONDITIONING; REINFORCEMENT; TOBACCO USE DISORDER;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CHOLINESTERASE INHIBITORS; CONDITIONING, OPERANT; CUES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; INDANS; MALE; NICOTINE; PIPERIDINES; RATS; REINFORCEMENT (PSYCHOLOGY); REINFORCEMENT SCHEDULE; SELF ADMINISTRATION; SUCROSE; TOBACCO USE DISORDER;

EID: 84904244319     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/adb.12014     Document Type: Article

References (84)

1. Andrews PL, Horn CC, (2006) Signals for nausea and emesis: implications for models of upper gastrointestinal diseases. Auton Neurosci 125: 100-115.
2. Arnold HM, Nelson CL, Sarter M, Bruno JP, (2003) Sensitization of cortical acetylcholine release by repeated administration of nicotine in rats. Psychopharmacology 165: 346-358. (Pubitemid 36223076)
3. Ashare RL, Ray R, Lerman C, Strasser AA, (2012) Cognitive effects of the acetylcholinesterase inhibitor, donepezil, in healthy, non-treatment seeking smokers: a pilot feasibility study. Drug Alcohol Depend 126: 263-267.
4. Atzori G, Lemmonds CA, Kotler ML, Durcan MJ, Boyle J, (2008) Efficacy of a nicotine (4 mg)-containing lozenge on the cognitive impairment of nicotine withdrawal. J Clin Psychopharmacol 28: 667-674.
5. Aubin HJ, Farley A, Lycett D, Lahmek P, Aveyard P, (2012) Weight gain in smokers after quitting cigarettes: meta-analysis. BMJ 345: e4439.
6. Audrain-McGovern J, Benowitz NL, (2011) Cigarette smoking, nicotine, and body weight. Clin Pharmacol Ther 90: 164-168.
7. Baker RR, Massey ED, Smith G, (2004) An overview of the effects of tobacco ingredients on smoke chemistry and toxicity. Food Chem Toxicol 42 (Suppl): S53-S83. (Pubitemid 38456980)
8. Benowitz NL, (2010) Nicotine addiction. N Engl J Med 362: 2295-2303.
9. Bespalov AY, Dravolina OA, Sukhanov I, Zakharova E, Blokhina E, Zvartau E, Danysz W, van, Heeke G, Markou A, (2005) Metabotropic glutamate receptor (mGluR5) antagonist MPEP attenuated cue- and schedule-induced reinstatement of nicotine self-administration behavior in rats. Neuropharmacology 49 (Suppl 1): 167-178. (Pubitemid 41115903)
10. Brady KT, Gray KM, Tolliver BK, (2011) Cognitive enhancers in the treatment of substance use disorders: clinical evidence. Pharmacol Biochem Behav 99: 285-294.
11. CDC (2012) Preventing Tobacco Use Among Youth and Young Adults: A Report of the Surgeon General. Atlanta, GA: U.S. Department of Health and Human Services, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health.
12. Cerbai F, Giovannini MG, Melani C, Enz A, Pepeu G, (2007) N1phenethyl-norcymserine, a selective butyrylcholinesterase inhibitor, increases acetylcholine release in rat cerebral cortex: a comparison with donepezil and rivastigmine. Eur J Pharmacol 572: 142-150. (Pubitemid 47429651)
13. Changeux JP, (2010) Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat Rev Neurosci 11: 389-401.
14. Corrigall WA, Coen KM, (1989) Nicotine maintains robust self-administration in rats on a limited-access schedule. Psychopharmacology (Berl) 99: 473-478. (Pubitemid 19273101)
15. Davis JA, James JR, Siegel SJ, Gould TJ, (2005) Withdrawal from chronic nicotine administration impairs contextual fear conditioning in C57BL/6 mice. J Neurosci 25: 8708-8713. (Pubitemid 41362049)
16. De Biasi M, Dani JA, (2011) Reward, addiction, withdrawal to nicotine. Annu Rev Neurosci 34: 105-130.
17. De Jonghe BC, Lawler MP, Horn CC, Tordoff MG, (2009) Pica as an adaptive response: kaolin consumption helps rats recover from chemotherapy-induced illness. Physiol Behav 97: 87-90.
18. De la Garza R, 2nd, Yoon JH, (2011) Evaluation of the effects of rivastigmine on cigarette smoking by methamphetamine-dependent volunteers. Prog Neuropsychopharmacol Biol Psychiatry 35: 1827-1830.
19. Diehl A, Nakovics H, Croissant B, Smolka MN, Batra A, Mann K, (2006) Galantamine reduces smoking in alcohol-dependent patients: a randomized, placebo-controlled trial. Int J Clin Pharmacol Ther 44: 614-622. (Pubitemid 44896139)
20. Diehl A, Nakovics H, Mutschler J, Hermann D, Kiefer F, (2009) Rivastigmine reduces tobacco craving in alcohol-dependent smokers. Pharmacopsychiatry 42: 89-94.
21. Donny EC, Caggiula AR, Weaver MT, Levin ME, Sved AF, (2011) The reinforcement-enhancing effects of nicotine: implications for the relationship between smoking, eating and weight. Physiol Behav 104: 143-148.
22. Dunn NR, Pearce GL, Shakir SA, (2000) Adverse effects associated with the use of donepezil in general practice in England. J Psychopharmacol 14: 406-408. (Pubitemid 32059787)
23. Evans WE, Yee GC, Crom WR, Pratt CB, Green AA, (1981) Clinical pharmacology of bleomycin and cisplatin. Head Neck Surg 4: 98-110. (Pubitemid 12247745)
24. Farlow MR, Salloway S, Tariot PN, Yardley J, Moline ML, Wang Q, Brand-Schieber E, Zou H, Hsu T, Satlin A, (2010) Effectiveness and tolerability of high-dose (23 mg/d) versus standard-dose (10 mg/d) donepezil in moderate to severe Alzheimer's disease: a 24-week, randomized, double-blind study. Clin Ther 32: 1234-1251.
25. Feltenstein MW, Ghee SM, See RE, (2012) Nicotine self-administration and reinstatement of nicotine-seeking in male and female rats. Drug Alcohol Depend 121: 240-246.
26. Fowler CD, Kenny PJ, (2011) Intravenous nicotine self-administration and cue-induced reinstatement in mice: effects of nicotine dose, rate of drug infusion and prior instrumental training. Neuropharmacology 61: 687-698.
27. Fowler CD, Lu Q, Johnson PM, Marks MJ, Kenny PJ, (2011) Habenular alpha5 nicotinic receptor subunit signalling controls nicotine intake. Nature 471: 597-601.
28. Geerts H, Guillaumat PO, Grantham C, Bode W, Anciaux K, Sachak S, (2005) Brain levels and acetylcholinesterase inhibition with galantamine and donepezil in rats, mice, and rabbits. Brain Res 1033: 186-193. (Pubitemid 40193413)
29. George O, Lloyd A, Carroll FI, Damaj MI, Koob GF, (2011) Varenicline blocks nicotine intake in rats with extended access to nicotine self-administration. Psychopharmacology (Berl) 213: 715-722.
30. Giacobini E, Zhu XD, Williams E, Sherman KA, (1996) The effect of the selective reversible acetylcholinesterase inhibitor E2020 on extracellular acetylcholine and biogenic amine levels in rat cortex. Neuropharmacology 35: 205-211. (Pubitemid 26082121)
31. Giarola A, Auber A, Chiamulera C, (2011) Acetylcholinesterase inhibitors partially generalize to nicotine discriminative stimulus effect in rats. Behav Pharmacol 22: 1-6.
32. Giorgetti M, Gibbons JA, Bernales S, Alfaro IE, Drieu La Rochelle C, Cremers T, Altar CA, Wronski R, Hutter-Paier B, Protter AA, (2010) Cognition-enhancing properties of Dimebon in a rat novel object recognition task are unlikely to be associated with acetylcholinesterase inhibition or N-methyl-D-aspartate receptor antagonism. J Pharmacol Exp Ther 333: 748-757.
33. Goh CW, Aw CC, Lee JH, Chen CP, Browne ER, (2011) Pharmacokinetic and pharmacodynamic properties of cholinesterase inhibitors donepezil, tacrine, and galantamine in aged and young Lister hooded rats. Drug Metab Dispos 39: 402-411.
34. Grasing K, He S, Yang Y, (2008) Dose-related effects of the acetylcholinesterase inhibitor tacrine on cocaine and food self-administration in rats. Psychopharmacology 196: 133-142.
35. Harvey AL, (1995) The pharmacology of galanthamine and its analogues. Pharmacol Ther 68: 113-128.
36. Hernandez CM, Terry AV, Jr, (2005) Repeated nicotine exposure in rats: effects on memory function, cholinergic markers and nerve growth factor. Neuroscience 130: 997-1012. (Pubitemid 40094631)
37. Hikida T, Kitabatake Y, Pastan I, Nakanishi S, (2003) Acetylcholine enhancement in the nucleus accumbens prevents addictive behaviors of cocaine and morphine. Proc Natl Acad Sci U S A 100: 6169-6173. (Pubitemid 36576949)
38. Hiranita T, Nawata Y, Sakimura K, Anggadiredja K, Yamamoto T, (2006) Suppression of methamphetamine-seeking behavior by nicotinic agonists. Proc Natl Acad Sci U S A 103: 8523-8527. (Pubitemid 43838488)
39. Hopkins TJ, Rupprecht LE, Hayes MR, Blendy JA, Schmidt HD, (2012) Galantamine, an acetylcholinesterase inhibitor and positive allosteric modulator of nicotinic acetylcholine receptors, attenuates nicotine taking and seeking in rats. Neuropsychopharmacology 37: 2310-2321.
40. Hughes JR, Hatsukami D, (1986) Signs and symptoms of tobacco withdrawal. Arch Gen Psychiatry 43: 289-294. (Pubitemid 16052281)
41. Hughes JR, Keely J, Naud S, (2004) Shape of the relapse curve and long-term abstinence among untreated smokers. Addiction 99: 29-38. (Pubitemid 38142221)
42. Jackisch R, Forster S, Kammerer M, Rothmaier AK, Ehret A, Zentner J, Feuerstein TJ, (2009) Inhibitory potency of choline esterase inhibitors on acetylcholine release and choline esterase activity in fresh specimens of human and rat neocortex. J Alzheimers Dis 16: 635-647.
43. Jann MW, Shirley KL, Small GW, (2002) Clinical pharmacokinetics and pharmacodynamics of cholinesterase inhibitors. Clin Pharmacokinet 41: 719-739. (Pubitemid 34948194)
44. Kaasinen V, Nagren K, Jarvenpaa T, Roivainen A, Yu M, Oikonen V, Kurki T, Rinne JO, (2002) Regional effects of donepezil and rivastigmine on cortical acetylcholinesterase activity in Alzheimer's disease. J Clin Psychopharmacol 22: 615-620. (Pubitemid 35416788)
45. Kanoski SE, Rupprecht LE, Fortin SM, De Jonghe BC, Hayes MR, (2012) The role of nausea in food intake and body weight suppression by peripheral GLP-1 receptor agonists, exendin-4 and liraglutide. Neuropharmacology 62: 1916-1927.
46. Kelly DL, McMahon RP, Weiner E, Boggs DL, Dickinson D, Conley RR, Buchanan RW, (2008) Lack of beneficial galantamine effect for smoking behavior: a double-blind randomized trial in people with schizophrenia. Schizophr Res 103: 161-168.
47. Kendall I, Slotten HA, Codony X, Burgueno J, Pauwels PJ, Vela JM, Fone KC, (2011) E-6801, a 5-HT6 receptor agonist, improves recognition memory by combined modulation of cholinergic and glutamatergic neurotransmission in the rat. Psychopharmacology 213: 413-430.
48. Kenny PJ, Markou A, (2001) Neurobiology of the nicotine withdrawal syndrome. Pharmacol Biochem Behav 70: 531-549. (Pubitemid 34131647)
49. Kosasa T, Kuriya Y, Matsui K, Yamanishi Y, (1999) Effect of donepezil hydrochloride (E2020) on basal concentration of extracellular acetylcholine in the hippocampus of rats. Eur J Pharmacol 380: 101-107. (Pubitemid 29469519)
50. Liang YQ, Tang XC, (2004) Comparative effects of huperzine A, donepezil and rivastigmine on cortical acetylcholine level and acetylcholinesterase activity in rats. Neurosci Lett 361: 56-59. (Pubitemid 38609215)
51. Liu YL, Malik N, Sanger GJ, Friedman MI, Andrews PL, (2005) Pica-a model of nausea? Species differences in response to cisplatin. Physiol Behav 85: 271-277. (Pubitemid 40840743)
52. Maelicke A, Albuquerque EX, (2000) Allosteric modulation of nicotinic acetylcholine receptors as a treatment strategy for Alzheimer's disease. Eur J Pharmacol 393: 165-170. (Pubitemid 30193413)
53. Mathieu-Kia AM, Kellogg SH, Butelman ER, Kreek MJ, (2002) Nicotine addiction: insights from recent animal studies. Psychopharmacology 162: 102-118. (Pubitemid 34743950)
54. Matta SG, Balfour DJ, Benowitz NL, Boyd RT, Buccafusco JJ, Caggiula AR, Craig CR, Collins AC, Damaj MI, Donny EC, Gardiner PS, Grady SR, Heberlein U, Leonard SS, Levin ED, Lukas RJ, Markou A, Marks MJ, McCallum SE, Parameswaran N, Perkins KA, Picciotto MR, Quik M, Rose JE, Rothenfluh A, Schafer WR, Stolerman IP, Tyndale RF, Wehner JM, Zirger JM, (2007) Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 190: 269-319. (Pubitemid 46156883)
55. Mitchell D, Wells C, Hoch N, Lind K, Woods SC, Mitchell LK, (1976) Poison induced pica in rats. Physiol Behav 17: 691-697. (Pubitemid 8004084)
56. Myers CS, Taylor RC, Moolchan ET, Heishman SJ, (2008) Dose-related enhancement of mood and cognition in smokers administered nicotine nasal spray. Neuropsychopharmacology 33: 588-598.
57. O'Connor EC, Parker D, Rollema H, Mead AN, (2010) The alpha4beta2 nicotinic acetylcholine-receptor partial agonist varenicline inhibits both nicotine self-administration following repeated dosing and reinstatement of nicotine seeking in rats. Psychopharmacology 208: 365-376.
58. Ota T, Shinotoh H, Fukushi K, Kikuchi T, Sato K, Tanaka N, Shimada H, Hirano S, Miyoshi M, Arai H, Suhara T, Irie T, (2010) Estimation of plasma IC50 of donepezil for cerebral acetylcholinesterase inhibition in patients with Alzheimer disease using positron emission tomography. Clin Neuropharmacol 33: 74-78.
59. Patterson F, Jepson C, Loughead J, Perkins K, Strasser AA, Siegel S, Frey J, Gur R, Lerman C, (2010) Working memory deficits predict short-term smoking resumption following brief abstinence. Drug Alcohol Depend 106: 61-64.
60. Pepeu G, Giovannini MG, (2009) Cholinesterase inhibitors and beyond. Curr Alzheimer Res 6: 86-96.
61. Perkins KA, Stitzer M, Lerman C, (2006) Medication screening for smoking cessation: a proposal for new methodologies. Psychopharmacology 184: 628-636. (Pubitemid 43255879)
62. Powell J, Dawkins L, West R, Pickering A, (2010) Relapse to smoking during unaided cessation: clinical, cognitive and motivational predictors. Psychopharmacology 212: 537-549.
63. Pratt RD, Perdomo CA, Surick IW, Ieni JR, (2002) Donepezil: tolerability and safety in Alzheimer's disease. Int J Clin Pract 56: 710-717. (Pubitemid 35414512)
64. Raybuck JD, Portugal GS, Lerman C, Gould TJ, (2008) Varenicline ameliorates nicotine withdrawal-induced learning deficits in C57BL/6 mice. Behav Neurosci 122: 1166-1171.
65. Reid RT, Sabbagh MN, (2008) Effects of cholinesterase inhibitors on rat nicotinic receptor levels in vivo and in vitro. J Neural Transm 115: 1437-1444.
66. Rogers SL, Friedhoff LT, (1998) Pharmacokinetic and pharmacodynamic profile of donepezil HCl following single oral doses. Br J Clin Pharmacol 46 (Suppl 1): 1-6. (Pubitemid 29197007)
67. Rollema H, Chambers LK, Coe JW, Glowa J, Hurst RS, Lebel LA, Lu Y, Mansbach RS, Mather RJ, Rovetti CC, Sands SB, Schaeffer E, Schulz DW, Tingley FD, 3rd, Williams KE, (2007) Pharmacological profile of the alpha4beta2 nicotinic acetylcholine receptor partial agonist varenicline, an effective smoking cessation aid. Neuropharmacology 52: 985-994. (Pubitemid 46227486)
68. Sacco KA, Creeden C, Reutenauer EL, George TP, (2008) Effects of galantamine on cognitive deficits in smokers and non-smokers with schizophrenia. Schizophr Res 103: 326-327.
69. Samochocki M, Hoffle A, Fehrenbacher A, Jostock R, Ludwig J, Christner C, Radina M, Zerlin M, Ullmer C, Pereira EF, Lubbert H, Albuquerque EX, Maelicke A, (2003) Galantamine is an allosterically potentiating ligand of neuronal nicotinic but not of muscarinic acetylcholine receptors. J Pharmacol Exp Ther 305: 1024-1036. (Pubitemid 36617980)
70. Schmidt HD, Anderson SM, Famous KR, Kumaresan V, Pierce RC, (2005) Anatomy and pharmacology of cocaine priming-induced reinstatement of drug seeking. Eur J Pharmacol 526: 65-76. (Pubitemid 41744106)
71. Schnoll RA, Lerman C, (2006) Current and emerging pharmacotherapies for treating tobacco dependence. Expert Opin Emerg Drugs 11: 429-444. (Pubitemid 44386368)
72. Shaham Y, Adamson LK, Grocki S, Corrigall WA, (1997) Reinstatement and spontaneous recovery of nicotine seeking in rats. Psychopharmacology 130: 396-403. (Pubitemid 27179734)
73. Shalev U, Grimm JW, Shaham Y, (2002) Neurobiology of relapse to heroin and cocaine seeking: a review. Pharmacol Rev 54: 1-42. (Pubitemid 34208828)
74. Slotkin TA, Bodwell BE, Ryde IT, Seidler FJ, (2008) Adolescent nicotine treatment changes the response of acetylcholine systems to subsequent nicotine administration in adulthood. Brain Res Bull 76: 152-165.
75. Smith JW, Mogg A, Tafi E, Peacey E, Pullar IA, Szekeres P, Tricklebank M, (2007) Ligands selective for alpha4beta2 but not alpha3beta4 or alpha7 nicotinic receptors generalise to the nicotine discriminative stimulus in the rat. Psychopharmacology 190: 157-170. (Pubitemid 46011176)
76. Snape MF, Misra A, Murray TK, De Souza RJ, Williams JL, Cross AJ, Green AR, (1999) A comparative study in rats of the in vitro and in vivo pharmacology of the acetylcholinesterase inhibitors tacrine, donepezil and NXX-066. Neuropharmacology 38: 181-193. (Pubitemid 29073537)
77. Sofuoglu M, (2010) Cognitive enhancement as a pharmacotherapy target for stimulant addiction. Addiction 105: 38-48.
78. Substance Abuse and Mental Health Services Administration (2009) Results from the 2008 National Survey on Drug Use and Health. Rockville, MD: National Findings Office of Applied Studies.
79. Taylor DH, Jr, Hasselblad V, Henley SJ, Thun MJ, Sloan FA, (2002) Benefits of smoking cessation for longevity. Am J Public Health 92: 990-996. (Pubitemid 34552904)
80. Terry AV, Jr, Buccafusco JJ, (2003) The cholinergic hypothesis of age and Alzheimer's disease-related cognitive deficits: recent challenges and their implications for novel drug development. J Pharmacol Exp Ther 306: 821-827. (Pubitemid 37025286)
81. Tuesta LM, Fowler CD, Kenny PJ, (2011) Recent advances in understanding nicotinic receptor signaling mechanisms that regulate drug self-administration behavior. Biochem Pharmacol 82: 984-995.
82. Wilkinson DS, Gould TJ, (2011) The effects of galantamine on nicotine withdrawal-induced deficits in contextual fear conditioning in C57BL/6 mice. Behav Brain Res 223: 53-57.
83. Yan Y, Pushparaj A, Gamaleddin I, Steiner RC, Picciotto MR, Roder J, Le Foll B, (2012a) Nicotine-taking and nicotine-seeking in C57Bl/6J mice without prior operant training or food restriction. Behav Brain Res 230: 34-39.
84. Yan Y, Pushparaj A, Le Strat Y, Gamaleddin I, Barnes C, Justinova Z, Goldberg SR, Le Foll B, (2012b) Blockade of dopamine d4 receptors attenuates reinstatement of extinguished nicotine-seeking behavior in rats. Neuropsychopharmacology 37: 685-696.