ABT-089, but not ABT-107, ameliorates nicotine withdrawal-induced cognitive deficits in C57BL6/J mice

Behavioural Pharmacology

Volumn 26, Issue 3, 2015, Pages 241-248

  Yildirim, Emre ^a   Connor, David A ^a   Gould, Thomas J ^a  

^a TEMPLE UNIVERSITY   (United States)

Author keywords

acetylcholine; addiction; cognition; hippocampus; learning; withdrawal

Indexed keywords

5-(6-(1-AZABICYCLO(2,2,2)OCT-3-YLOXY)PYRIDAZIN-3-YL)-1H-INDOLE; INDOLE DERIVATIVE; NICOTINE; NICOTINIC AGENT; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA4BETA2; NICOTINIC RECEPTOR BETA2; POZANICLINE; PYRIDINE DERIVATIVE; PYRROLIDINE DERIVATIVE; QUINUCLIDINE DERIVATIVE;

ANIMAL; ASSOCIATION; C57BL MOUSE; COGNITION; COMPARATIVE STUDY; COMPLICATION; CONDITIONING; DOSE RESPONSE; DRUG EFFECTS; FEAR; HIPPOCAMPUS; LEARNING; MALE; METABOLISM; MOUSE; PARTIAL AGONISM; TOBACCO USE DISORDER; WITHDRAWAL SYNDROME;

ANIMALS; COGNITION; CONDITIONING (PSYCHOLOGY); CUES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG PARTIAL AGONISM; FEAR; HIPPOCAMPUS; INDOLES; LEARNING; MALE; MICE; MICE, INBRED C57BL; NICOTINE; NICOTINIC AGONISTS; PYRIDINES; PYRROLIDINES; QUINUCLIDINES; RECEPTORS, NICOTINIC; SUBSTANCE WITHDRAWAL SYNDROME; TOBACCO USE DISORDER;

EID: 84939957553     PISSN: 09558810     EISSN: 14735849     Source Type: Journal    
DOI: 10.1097/FBP.0000000000000111     Document Type: Article

References (67)

1. Agaku IT, King BA, Dube SR (2014). Current cigarette smoking among adults-United States, 2005-2012. Morb Mortal Wkly Rep 63:29-34.
2. Andre JM, Gulick D, Portugal GS, Gould TJ (2008). Nicotine withdrawal disrupts both foreground and background contextual fear conditioning but not prepulse inhibition of the acoustic startle response in C57BL/6 mice. Behav Brain Res 190:174-181.
3. Ashare RL, Falcone M, Lerman C (2014). Cognitive function during nicotine withdrawal: Implications for nicotine dependence treatment. Neuropharmacology 76 Pt B:581-591.
4. Bitner RS, Bunnelle WH, Decker MW, Drescher KU, Kohlhaas KL, Markosyan S, et al. (2010). In vivo pharmacological characterization of a novel selective alpha7 neuronal nicotinic acetylcholine receptor agonist ABT-107: preclinical considerations in Alzheimer's disease. J Pharmacol Exp Ther 334:875-886.
5. Blake J, Smith A (1997). Effects of smoking and smoking deprivation on the articulatory loop of working memory. Hum Psychopharmacol Clin 12:259-264.
6. Blanchard RJ, Blanchard DC (1969). Passive and active reactions to fear-eliciting stimuli. J Comp Physiol Psychol 68:129-135.
7. Changeux JP (2012). The nicotinic acetylcholine receptor: the founding father of the pentameric ligand-gated ion channel superfamily. J Biol Chem 287:40207-40215.
8. Damaj MI, Kao W, Martin BR (2003). Characterization of spontaneous and precipitated nicotine withdrawal in the mouse. J Pharmacol Exp Ther 307:526-534.
9. Dani JA, Heinemann S (1996). Molecular and cellular aspects of nicotine abuse. Neuron 16:905-908.
10. Davis JA, Gould TJ (2007). β2 subunit-containing nicotinic receptors mediate the enhancing effect of nicotine on trace cued fear conditioning in C57BL/6 mice. Psychopharmacology (Berl) 190:343-352.
11. Davis JA, Gould TJ (2009). Hippocampal nAChRs mediate nicotine withdrawalrelated learning deficits. Eur Neuropsychopharmacol 19:551-561.
12. 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.
13. Davis JA, Porter J, Gould TJ (2006). Nicotine enhances both foreground and background contextual fear conditioning. Neurosci Lett 394:202-205.
14. Davis JA, Kenney JW, Gould TJ (2007). Hippocampal alpha4beta2 nicotinic acetylcholine receptor involvement in the enhancing effect of acute nicotine on contextual fear conditioning. J Neurosci 27:10870-10877.
15. Decker MW, Bannon AW, Curzon P, Gunther KL, Brioni JD, Holladay MW, et al. (1997). ABT-089 [2-methyl-3-(2-(S)-pyrrolidinylmethoxy)pyridine dihydrochloride]: II. A novel cholinergic channel modulator with effects on cognitive performance in rats and monkeys. J Pharmacol Exp Ther 283:247-258.
16. Devinsky O, Morrell MJ, Vogt BA (1993). Contributions of anterior cingulate cortex to behavior. Brain 118:279-306.
17. Doura MB, Gold AB, Keller AB, Perry DC (2008). Adult and periadolescent rats differ in expression of nicotinic cholinergic receptor subtypes and in the response of these subtypes to chronic nicotine exposure. Brain Res 1215:40-52.
18. Garvey AJ, Bliss RE, Hitchcock JL, Heinold JW, Rosner B (1992). Predictors of smoking relapse among self-quitters: a report from the Normative Aging Study. Addict Behav 17:367-377.
19. Gould TJ (2006). Nicotine and hippocampus-dependent learning: implications for addiction. Mol Neurobiol 34:93-107.
20. Gould TJ, Wehner JM (1999). Nicotine enhancement of contextual fear conditioning. Behav Brain Res 102:31-39.
21. Gould TJ, Higgins JS (2003). Nicotine enhances contextual fear conditioning in C57BL/6J mice at 1 and 7 days post-training. Neurobiol Learn Mem 80:147-157.
22. Gould TJ, Leach PT (2014). Cellular, molecular, and genetic substrates underlying the impact of nicotine on learning. Neurobiol Learn Mem 107:108-132.
23. Gould TJ, Portugal GS, Andre JM, Tadman MP, Marks MJ, Kenney JW, et al. (2012). The duration of nicotine withdrawal-associated deficits in contextual fear conditioning parallels changes in hippocampal high affinity nicotinic acetylcholine receptor upregulation. Neuropharmacology 62:2118-2125.
24. Gould TJ, Wilkinson DS, Yildirim E, Blendy JA, Adoff MD (2014). Dissociation of tolerance and nicotine withdrawal-associated deficits in contextual fear. Brain Res 1559:1-10.
25. Gulick D, Gould TJ (2009). The hippocampus and cingulate cortex differentially mediate the effects of nicotine on learning versus on ethanol-induced learning deficits through different effects at nicotinic receptors. Neuropsychopharmacology 34:2167-2179.
26. Higgins GA, Breysse N (2008). Rodent model of attention: the 5-choice serial reaction time task. Curr Protoc Pharmacol 5:5-49.
27. Hughes JR (1992). Tobacco withdrawal in self-quitters. J Consult Clin Psychol 60:689-697.
28. Hughes JR (2007). Effects of abstinence from tobacco: valid symptoms and time course. Nicotine Tob Res 9:315-327.
29. Hughes JR, Gust SW, Skoog K, Keenan RM, Fenwick JW (1991). Symptoms of tobacco withdrawal. A replication and extension. Arch Gen Psychiatry 48:52-59.
30. Jackson KJ, Martin BR, Changeux JP, Damaj MI (2008). Differential role of nicotinic acetylcholine receptor subunits in physical and affective nicotine withdrawal signs. J Pharmacol Exp Ther 325:302-312.
31. Jacobsen LK, Krystal JH, Mencl WE, Westerveld M, Frost SJ, Pugh KR (2005). Effects of smoking and smoking abstinence on cognition in adolescent tobacco smokers. Biol Psychiatry 57:56-66.
32. Kenney JW, Gould TJ (2008). Modulation of hippocampus-dependent learning and synaptic plasticity by nicotine. Mol Neurobiol 38:101-121.
33. Kenney JW, Adoff MD, Wilkinson DS, Gould TJ (2011). The effects of acute, chronic, and withdrawal from chronic nicotine on novel and spatial object recognition in male C57BL/6J mice. Psychopharmacology (Berl) 217:353-365.
34. Leiser SC, Bowlby MR, Comery TA, Dunlop J (2009). A cog in cognition: how the alpha 7 nicotinic acetylcholine receptor is geared towards improving cognitive deficits. Pharmacol Ther 122:302-311.
35. Lendvai B, Kassai F, Szajli A, Nemethy Z (2013). a7 nicotinic acetylcholine receptors and their role in cognition. Brain Res Bull 93:86-96.
36. Lerman C, LeSage MG, Perkins KA, O'Malley SS, Siegel SJ, Benowitz NL, Corrigall WA (2007). Translational research in medication development for nicotine dependence. Nat Rev Drug Discov 6:746-762.
37. Levin ED (2012). a7-Nicotinic receptors and cognition. Curr Drug Targets 13:602-606.
38. Levin ED, Petro A, Rezvani AH, Pollard N, Christopher NC, Strauss M, et al. (2009). Nicotinic alpha7-or beta2-containing receptor knockout: effects on radial-arm maze learning and long-term nicotine consumption in mice. Behav Brain Res 196:207-213.
39. Lin NH, Gunn DE, Ryther KB, Garvey DS, Donnelly-Roberts DL, Decker MW, et al. (1997). Structure-activity studies on 2-methyl-3-(2(S)-pyrrolidinylmethoxy) pyridine (ABT-089): an orally bioavailable 3-pyridyl ether nicotinic acetylcholine receptor ligand with cognition-enhancing properties. J Med Chem 40:385-390.
40. Malysz J, Anderson DJ, Grønlien JH, Ji J, Bunnelle WH, Håkerud M, et al. (2010). In vitro pharmacological characterization of a novel selective alpha7 neuronal nicotinic acetylcholine receptor agonist ABT-107. J Pharmacol Exp Ther 334:863-874.
41. Marks MJ, Wageman CR, Grady SR, Gopalakrishnan M, Briggs CA (2009). Selectivity of ABT-089 for alpha4beta2∗ and alpha6beta2∗ nicotinic acetylcholine receptors in brain. Biochem Pharmacol 78:795-802.
42. Mendrek A, Monterosso J, Simon SL, Jarvik M, Brody A, Olmstead R, et al. (2006). Working memory in cigarette smokers: comparison to non-smokers and effects of abstinence. Addict Behav 31:833-844.
43. Papke RL, Trocmé-Thibierge C, Guendisch D, Al Rubaiy SAA, Bloom SA (2011). Electrophysiological perspectives on the therapeutic use of nicotinic acetylcholine receptor partial agonists. J Pharmacol Exp Ther 337:367-379.
44. Parrott AC, Craig D (1992). Cigarette smoking and nicotine gum (0, 2 and 4 mg): effects upon four visual attention tasks. Neuropsychobiology 25:34-43.
45. Patterson F, Jepson C, Loughead J, Perkins K, Strasser AA, Siegel S, et al. (2010). Working memory deficits predict short-term smoking resumption following brief abstinence. Drug Alcohol Depend 106:61-64.
46. Perez XA, Bordia T, McIntosh JM, Grady SR, Quik M (2008). Long-term nicotine treatment differentially regulates striatal a6a4β2∗ and a6(nona4)β2∗ nAChR expression and function. Mol Pharmacol 74:844-853.
47. Portugal GS, Gould TJ (2007). Bupropion dose-dependently reverses nicotine withdrawal deficits in contextual fear conditioning. Pharmacol Biochem Behav 88:179-187.
48. Portugal GS, Gould TJ (2008). Genetic variability in nicotinic acetylcholine receptors and nicotine addiction: Converging evidence from human and animal research. Behav Brain Res 193:1-16.
49. Portugal GS, Gould TJ (2009). Nicotine withdrawal disrupts new contextual learning. Pharmacol Biochem Behav 92:117-123.
50. Portugal GS, Kenney JW, Gould TJ (2008). Beta2 subunit containing acetylcholine receptors mediate nicotine withdrawal deficits in the acquisition of contextual fear conditioning. Neurobiol Learn Mem 89:106-113.
51. Portugal GS, Wilkinson DS, Kenney JW, Sullivan C, Gould TJ (2012a). Straindependent effects of acute, chronic, and withdrawal from chronic nicotine on fear conditioning. Behav Genet 42:133-150.
52. Portugal GS, Wilkinson DS, Turner JR, Blendy JA, Gould TJ (2012b). Developmental effects of acute, chronic, and withdrawal from chronic nicotine on fear conditioning. Neurobiol Learn Mem 97:482-494.
53. 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.
54. Ren K, Thinschmidt J, Liu J, Ai L, Papke RL, King MA, et al. (2007). alpha7 Nicotinic receptor gene delivery into mouse hippocampal neurons leads to functional receptor expression, improved spatial memory-related performance, and tau hyperphosphorylation. Neuroscience 145:314-322.
55. Rueter LE, Anderson DJ, Briggs CA, Donnelly-Roberts DL, Gintant GA, Gopalakrishnan M, et al. (2004). ABT-089: pharmacological properties of a neuronal nicotinic acetylcholine receptor agonist for the potential treatment of cognitive disorders. CNS Drug Rev 10:167-182.
56. Rukstalis M, Jepson C, Patterson F, Lerman C (2005). Increases in hyperactiveimpulsive symptoms predict relapse among smokers in nicotine replacement therapy. J Subst Abuse Treat 28:297-304.
57. Sarter M, Parikh V, Howe WM (2009). nAChR agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms. Biochem Pharmacol 78:658-667.
58. Semenova S, Stolerman IP, Markou A (2007). Chronic nicotine administration improves attention while nicotine withdrawal induces performance deficits in the 5-choice serial reaction time task in rats. Pharmacol Biochem Behav 87:360-368.
59. Shoaib M, Bizarro L (2005). Deficits in a sustained attention task following nicotine withdrawal in rats. Psychopharmacology (Berl) 178:211-222.
60. Snyder FR, Davis FC, Henningfield JE (1989). The tobacco withdrawal syndrome: performance decrements assessed on a computerized test battery. Drug Alcohol Depend 23:259-266.
61. United States, Public Health Service, Office of the Surgeon General (2010). How tobacco smoke causes disease : the biology and behavioral basis for smoking-attributable disease : a report of the Surgeon General. Rockville, MD; Washington, DC, USA: Department of Health and Human Services, Public Health Service.
62. Wehner JM, Keller JJ, Keller AB, Picciotto MR, Paylor R, Booker TK, et al. (2004). Role of neuronal nicotinic receptors in the effects of nicotine and ethanol on contextual fear conditioning. Neuroscience 129:11-24.
63. 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.
64. Wilkinson DS, Gould TJ (2013).Withdrawal from chronic nicotine and subsequent sensitivity to nicotine challenge on contextual learning. Behav Brain Res 250:58-61.
65. Wilkinson DS, Turner JR, Blendy JA, Gould TJ (2013). Genetic background influences the effects of withdrawal from chronic nicotine on learning and high-affinity nicotinic acetylcholine receptor binding in the dorsal and ventral hippocampus. Psychopharmacology (Berl) 225:201-208.
66. Yohn NL, Turner JR, Blendy JA (2014). Activation of a4β2∗/a6β2∗ nicotinic receptors alleviates anxiety during nicotine withdrawal without upregulating nicotinic receptors. J Pharmacol Exp Ther 349:348-354.
67. Young JW, Meves JM, Tarantino IS, Caldwell S, Geyer MA (2011). Delayed procedural learning in alpha7-nicotinic acetylcholine receptor knockout mice. Genes Brain Behav 10:720-733.