The potent M1 receptor allosteric agonist GSK1034702 improves episodic memory in humans in the nicotine abstinence model of cognitive dysfunction

International Journal of Neuropsychopharmacology

Volumn 16, Issue 4, 2013, Pages 721-731

  Nathan, Pradeep J ^a,b   Watson, Jeannette ^c   Lund, Jesper ^c   Davies, Ceri H ^d   Peters, Gary ^a   Dodds, Chris M ^a   Swirski, Bridget ^a   Lawrence, Philip ^a   Bentley, Graham D ^a   O'Neill, Barry V ^a   Robertson, Jon ^c   Watson, Stephen ^c   Jones, Gareth A ^c   Maruff, Paul ^e   Croft, Rodney J ^f   Laruelle, Marc ^c   Bullmore, Edward T ^a,b  

^a ADDENBROOKE S HOSPITAL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

^d GSK Research and Development   (Singapore)

^e Cogstate Ltd ^*  (Australia)

^f UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

Alzheimer's disease; cognition; episodic memory; hippocampus; M1 agonist; M1 receptor

Indexed keywords

GSK1034702; MUSCARINIC M1 RECEPTOR; MUSCARINIC M1 RECEPTOR AGONIST; NICOTINE; PLACEBO; UNCLASSIFIED DRUG; BENZIMIDAZOLE DERIVATIVE; GSK 1034702;

ABDOMINAL PAIN; ADULT; ARTICLE; BODY TEMPERATURE; CLINICAL ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; CROSSOVER PROCEDURE; DIARRHEA; DOUBLE BLIND PROCEDURE; DRUG BLOOD LEVEL; DRUG INDUCED HEADACHE; DRUG POTENCY; DRUG SAFETY; DRUG TOLERABILITY; EPISODIC MEMORY; FATIGUE; FLATULENCE; FLUSHING; HIPPOCAMPUS; HUMAN; HYPERHIDROSIS; HYPERSALIVATION; LACRIMATION DISORDER; MALE; MOOD; NAUSEA; NEUROLOGIC EXAMINATION; NEUROTRANSMISSION; PHARMACOKINETICS; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SIDE EFFECT; SMOKING; SMOKING CESSATION; TIME TO MAXIMUM PLASMA CONCENTRATION; WITHDRAWAL SYNDROME; AGONISTS; ALLOSTERISM; BEHAVIOR, ADDICTIVE; COGNITION DISORDERS; DRUG EFFECTS; MIDDLE AGED; PHYSIOLOGY; PSYCHOLOGY; YOUNG ADULT; ADDICTION; CONTROLLED CLINICAL TRIAL; DRUG EFFECT; DRUG POTENTIATION; PSYCHOLOGICAL ASPECT;

ADULT; ALLOSTERIC REGULATION; BEHAVIOR, ADDICTIVE; BENZIMIDAZOLES; COGNITION DISORDERS; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; HUMANS; MALE; MEMORY, EPISODIC; MIDDLE AGED; NICOTINE; RECEPTOR, MUSCARINIC M1; SMOKING; SMOKING CESSATION; YOUNG ADULT;

EID: 84875697137     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145712000752     Document Type: Article

References (52)

1. Anagnostaras SG, Murphy GG, Hamilton SE, Mitchell SL, et al. (2003). Selective cognitive dysfunction in acetylcholine M1 muscarinic receptor mutant mice. Nature Neuroscience 6, 51-58.
2. Atri A, Sherman S, Norman KA, Kirchhoff BA, et al. (2004). Blockade of central cholinergic receptors impairs new learning and increases proactive interference in a word paired-associate memory task. Behavioural Neuroscience 118, 223-236.
3. Blokland A (1996). Acetylcholine: a neurotransmitter for learning and memory? Brain Research Reviews 21, 285-300.
4. Blokland A, Honig W, Raaijmakers WGM (1992). Effects of intra-hippocampal scopolamine injections in a repeated spatial acquisition task in the rat. Psychopharmacology 109, 373-376.
5. Bond A, Lader M (1974). The use of analogue scales in rating subjective feelings. British Journal of Medical Psychology 80, 1-46.
6. Bradley SR, Lameh J, Ohrmund L, Son T, et al. (2010). AC-260584, an orally bioavailable M(1) muscarinic receptor allosteric agonist, improves cognitive performance in an animal model. Neuropharmacology 58, 365-373.
7. Brandeis R, Sapir M, Hafif N, Abraham S, et al. (1995). AF150(S): a new functionally selective M1 agonist improves cognitive performance in rats. Pharmacology Biochemistry Behaviour 51, 667-674.
8. Buchanan KA, Petrovic MM, Chamberlain SE, Marrion NV, et al. (2010). Facilitation of long-term potentiation by muscarinic M(1) receptors is mediated by inhibition of SK channels. Neuron 68, 948-963.
9. Budzik B, Garzya V, Shi D, Walker G, et al. (2010). Novel N-substituted benzimidazolones as potent, selective, CNS-penetrant, and orally active M1 mAChR agonists. ACS Medicinal Chemistry Letters 1, 244-248.
10. Buzsaki G (1989). Two-stage model of memory trace formation: a role for 'noisy' brain states. Neuroscience 31, 551-570.
11. Cole AE, Nicoll RA (1984). Characterization of a slow cholinergic postsynaptic potential recorded in vitro from rat hippocampal pyramidal cells. Journal of Physiology 352, 173-188.
12. Crook JM, Tomaskovic-Crook E, Copolov DL, Dean B (2000). Decreased muscarinic receptor binding in subjects with schizophrenia: a study of the human hippocampal formation. Biological Psychiatry 48, 381-388.
13. Crook JM, Tomaskovic-Crook E, Copolov DL, Dean B (2001). Low muscarinic receptor binding in prefrontal cortex from subjects with schizophrenia: a study of Brodmann's areas 8, 9, 10, and 46 and the effects of neuroleptic drug treatment. American Journal of Psychiatry 158, 918-925.
14. Dean B, McLeod M, Keriakous D, McKenzie J, et al. (2002). Decreased muscarinic1 receptors in the dorsolateral prefrontal cortex of subjects with schizophrenia. Molecular Psychiatry 7, 1083-1091.
15. Deng C, Huang XF (2005). Decreased density of muscarinic receptors in the superior temporal gyrusin schizophrenia. Journal of Neuroscience Research 81, 883-890.
16. Ellis JR, Ellis KA, Bartholomeusz CF, Harrison BJ, et al. (2006). Muscarinic and nicotinic receptors synergistically modulate working memory and attention in humans. International Journal of Neuropsychopharmacology 9, 175-189.
17. Fadda F, Cocco S, Stancampiano R (2000). Hippocampal acetylcholine release correlates with spatial learning performance in freely moving rats. Neuroreport 11, 2265-2269.
18. Fernández de Sevilla D, Núnez A, Borde M, Malinow R, et al. (2008). Cholinergic-mediated IP3-receptor activation induces long-lasting synaptic enhancement in CA1 pyramidal neurons. Journal of Neuroscience 28, 1469-1478.
19. Ferrari-DiLeo G, Mash DC, Flynn DD (1995). Attenuation of muscarinic receptor-G-protein interaction in Alzheimer disease. Molecular and Chemical Neuropathology 24, 69-91.
20. Fisher A, Brandeis R, Bar-Ner RH, Kliger-Spatz M, et al. (2002). AF150(S) and AF267B: M1 muscarinic agonists as innovative therapies for Alzheimer's disease. Journal of Molecular Neuroscience 19, 145-153.
21. Fredrickson A, Snyder PJ, Cromer J, Thomas E, et al. (2008). The use of effect sizes to characterize the nature of cognitive change in psychopharmacological studies: an example with scopolamine. Human Psychopharmacology 23, 425-436.
22. Ghoneim MM, Mewaldt SP (1975). Effects of diazepam and scopolamine on storage, retrieval and organizational processes in memory. Psychopharmacologia 44, 257-262.
23. Ghoneim MM, Mewaldt SP (1977). Studies on human memory: the interactions of diazepam, scopolamine, and physostigmine. Psychopharmacology 52, 1-6.
24. Greenwood PM, Lin MK, Sundararajan R, Fryxell KJ, et al. (2009). Synergistic effects of genetic variation in nicotinic and muscarinic receptors on visual attention but not working memory. Proceedings of the National Academy of Sciences USA 106, 3633-3638.
25. Hasselmo ME (1999). Neuromodulation: acetylcholine and memory consolidation. Trends in Cognitive Sciences 3, 351-359.
26. Hasselmo ME, Sarter M (2011). Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 36, 52-73.
27. Hughes JR, Hatsukami D (2005). Background on the Minnesota Withdrawal Scale Revised (MNWS-R). (http://www.uvm.edu/yhbpl/?Page=minnesota/default.html) Accessed October 2010.
28. 11C]GSK1034702 for clinical use on an Eckert and Ziegler Modular Lab system. Applied Radiation and Isotopes 69, 1390-1394.
29. Levey AI, Kitt CA, Simonds WF, Price DL, Brann MR (1991). Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. Journal of Neuroscience 11, 3218-3226.
30. Madison DV, Nicoll RA (1984). Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. Journal of Physiology 354, 319-331.
31. Malenka RC, Bear MF (2004). LTP and LTD: an embarrassment of riches. Neuron 44, 5-21.
32. Marino MJ, Rouse ST, Levey AI, Potter LT, et al. (1998). Activation of the genetically defined m1 muscarinic receptor potentiates N-methyl-D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proceedings of the National Academy of Sciences USA 95, 11465-11470.
33. Miyakawa T, Yamada M, Duttaroy A, Wess J (2001). Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor. Journal of Neuroscience 21, 5239-5250.
34. 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.
35. Nicoll RA (1985). The septo-hippocampal projection: a model cholinergic pathway. Trends in Neuroscience 8, 533-553.
36. Overk CR, Felder CC, Tu Y, Schober DA, et al. (2010). Cortical M1 receptor concentration increases without a concomitant change in function in Alzheimer's disease. Journal of Chemical Neuroanatomy 40, 63-70.
37. Pakrasi S, Colloby SJ, Firbank MJ, Perry EK, et al. (2007). Muscarinic acetylcholine receptor status in Alzheimer's disease assessed using (R, R) 123I-QNB SPECT. Journal of Neurology 254, 907-913.
38. Petersen RC (1977). Scopolamine induced learning failures in man. Psychopharmacology 52, 283-289.
39. Potter PE, Rauschkolb PK, Pandya Y, Sue LI, et al. (2011). Pre-and post-synaptic cortical cholinergic deficits are proportional to amyloid plaque presence and density at preclinical stages of Alzheimer's disease. Acta Neuropathologica 122, 49-60.
40. Rodríguez-Puertas R, Pascual J, Vilaró T, Pazos A (1997). Autoradiographic distribution of M1, M2, M3, and M4 muscarinic receptor subtypes in Alzheimer's disease. Synapse 26, 341-350.
41. Rogers JL, Kesner RP (2003). Cholinergic modulation of the hippocampus during encoding and retrieval. Neurobiology of Learning and Memory 80, 332-342.
42. Ruske AC, White KG (1999). Facilitation of memory performance by a novel muscarinic agonist in young and old rats. Pharmacology Biochemistry Behaviour 63, 663-667.
43. Salah-Uddin H, Thomas DR, Davies CH, Hagan JJ, et al. (2008). Pharmacological assessment of M1 muscarinic acetylcholine receptor-Gq/11 protein coupling in membranes prepared from post mortem human brain tissue. Journal of Pharmacology and Experimental Therapeutics 325, 869-874.
44. Shinoe T, Matsui M, Taketo MM, Manabe T (2005). Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus. Journal of Neuroscience 25, 11194-11200.
45. Spalding TA, Trotter C, Skjaerbaek N, Messier TL, et al. (2002). Discovery of an ectopic activation site on the M(1) muscarinic receptor. Molecular Pharmacology 61, 1297-1302.
46. Thiels E, Klann E (2001). Extracellular signal-regulated kinase, synaptic plasticity, and memory. Review in Neuroscience 12, 327-345.
47. Thompson TA, Wilson PH, Snyder PJ, Pietrzak RH, et al. (2011). Sensitivity and test-retest reliability of the international shopping list test in assessing verbal learning and memory in mild Alzheimer's disease. Archives Clinical Neuropsychology 26, 412-424.
48. Tsang SW, Lai MK, Kirvell S, Francis PT, et al. (2006). Impaired coupling of muscarinic M1 receptors to G-proteins in the neocortex is associated with severity of dementia in Alzheimer's disease. Neurobiology Aging 27, 1216-1223.
49. Tsang SW, Pomakian J, Marshall GA, Vinters HV, et al. (2007). Disrupted muscarinic M1 receptor signaling correlates with loss of protein kinase C activity and glutamatergic deficit in Alzheimer's disease. Neurobiology of Aging 28, 1381-1387.
50. Vanover KE, Veinbergs I, Davis RE (2008). Antipsychotic-like behavioral effects and cognitive enhancement by a potent and selective muscarinic M-sub-1 receptor agonist, AC-260584. Behavioural Neuroscience 122, 570-575
51. Vincent GP, Sepinwall J (1992). AF102B, a novel M1 agonist, enhanced spatial learning in C57BL/10 mice with a long duration of action. Brain Research 597, 264-268.
52. Watt ML, Schober DA, Hitchcock S, Lui B, et al. (2011). Pharmacological characterization of LY593093, an M1 muscarinic acetylcholine receptor-selective partial orthosteric agonist. Journal of Pharmacology and Experimental Therapeutics, 338, 622-632.