Nicotinic and muscarinic agonists and acetylcholinesterase inhibitors stimulate a common pathway to enhance GluN2B-NMDAR responses

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 34, 2014, Pages 12538-12543

  Ishibashi, Masaru ^a,c   Yamazaki, Yoshihiko ^a,b   Miledi, Ricardo ^a   Sumikawa, Katumi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b YAMAGATA UNIVERSITY   (Japan)

^c NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

Donepezil; Hippocampus; m1 muscarinic receptor

Indexed keywords

2 ETHYL 8 METHYL 2,8 DIAZASPIRO[4.5]DECANE 1,3 DIONE; ACETYLCHOLINE; CHOLINERGIC RECEPTOR; DONEPEZIL; FOCAL ADHESION KINASE 2; GLUTAMATE RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; MUSCARINIC M1 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NICOTINE; PIRENZEPINE; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; 2-ETHYL-8-METHYL-2,8-DIAZASPIRO(4,5)DECANE-1,3-DIONE; AMPA RECEPTOR; CHOLINESTERASE INHIBITOR; INDAN DERIVATIVE; MUSCARINIC AGENT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINIC AGENT; NR2B NMDA RECEPTOR; PIPERIDINE DERIVATIVE; SUCCINIMIDE DERIVATIVE;

ACETYLCHOLINE RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EXPOSURE; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPAL CA1 REGION; IN VITRO STUDY; IN VIVO STUDY; LEARNING; LONG TERM POTENTIATION; MEMORY; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; AGONISTS; ANIMAL; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CHOLINESTERASE INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; INDANS; LONG-TERM POTENTIATION; MUSCARINIC AGONISTS; NICOTINE; NICOTINIC AGONISTS; PIPERIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, MUSCARINIC M1; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; SUCCINIMIDES;

EID: 84906678384     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1408805111     Document Type: Article

References (47)

1. Rezvani AH, Levin ED (2001) Cognitive effects of nicotine. Biol Psychiatry 49(3):258-267. (Pubitemid 32178435)
2. Fisher A (2008) Cholinergic treatments with emphasis on m1 muscarinic agonists as potential disease-modifying agents for Alzheimer's disease. Neurotherapeutics 5(3):433-442.
3. Winblad B, et al.; Donepezil Nordic Study Group (2001) A 1-year, randomized, placebo-controlled study of donepezil in patients with mild to moderate AD. Neurology 57(3):489-495. (Pubitemid 32757598)
4. Mintzer JE, Kershaw P (2003) The efficacy of galantamine in the treatment of Alzheimer's disease: Comparison of patients previously treated with acetylcholinesterase inhibitors to patients with no prior exposure. Int J Geriatr Psychiatry 18(4):292-297. (Pubitemid 36503039)
5. McGurk SR, Levin ED, Butcher LL (1991) Impairment of radial-arm maze performance in rats following lesions involving the cholinergic medial pathway: Reversal by arecoline and differential effects of muscarinic and nicotinic antagonists. Neuroscience 44(1):137-147.
6. Decker MW, Majchrzak MJ, Anderson DJ (1992) Effects of nicotine on spatial memory deficits in rats with septal lesions. Brain Res 572(1-2):281-285.
7. Iversen SD (1997) Behavioural evaluation of cholinergic drugs. Life Sci 60(13-14):1145-1152.
8. Kenney JW, Gould TJ (2008) Modulation of hippocampus-dependent learning and synaptic plasticity by nicotine. Mol Neurobiol 38(1):101-121.
9. Bliss TV, Collingridge GL (1993) A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361(6407):31-39. (Pubitemid 23020772)
10. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: An evaluation of the hypothesis. Annu Rev Neurosci 23:649-711. (Pubitemid 30350057)
11. Malenka RC, Bear MF (2004) LTP and LTD: An embarrassment of riches. Neuron 44(1):5-21. (Pubitemid 39348827)
12. Fujii S, Ji Z, Morita N, Sumikawa K (1999) Acute and chronic nicotine exposure differentially facilitate the induction of LTP. Brain Res 846(1):137-143. (Pubitemid 29486450)
13. Ji D, Lape R, Dani JA (2001) Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31(1):131-141. (Pubitemid 32757094)
14. Ovsepian SV, Anwyl R, Rowan MJ (2004) Endogenous acetylcholine lowers the threshold for long-term potentiation induction in the CA1 area through muscarinic receptor activation: In vivo study. Eur J Neurosci 20(5):1267-1275. (Pubitemid 39233579)
15. 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. J Neurosci 25(48):11194-11200. (Pubitemid 43089564)
16. Yamazaki Y, Jia Y, Hamaue N, Sumikawa K (2005) Nicotine-induced switch in the nicotinic cholinergic mechanisms of facilitation of long-term potentiation induction. Eur J Neurosci 22(4):845-860. (Pubitemid 41243326)
17. Yamazaki Y, Jia Y, Niu R, Sumikawa K (2006) Nicotine exposure in vivo induces long-lasting enhancement of NMDA receptor-mediated currents in the hippocampus. Eur J Neurosci 23(7):1819-1828.
18. Yamazaki Y, Fujii S, Jia Y, Sumikawa K (2006) Nicotine withdrawal suppresses nicotinic modulation of long-term potentiation induction in the hippocampal CA1 region. Eur J Neurosci 24(10):2903-2916. (Pubitemid 44813841)
19. Yamazaki Y, Jia Y, Wong JK, Sumikawa K (2006) Chronic nicotine-induced switch in Src-family kinase signaling for long-term potentiation induction in hippocampal CA1 pyramidal cells. Eur J Neurosci 24(11):3271-3284. (Pubitemid 44952659)
20. Nakauchi S, Brennan RJ, Boulter J, Sumikawa K (2007) Nicotine gates long-term potentiation in the hippocampal CA1 region via the activation of alpha2*nicotinic ACh receptors. Eur J Neurosci 25(9):2666-2681. (Pubitemid 46888829)
21. Yamazaki Y, Hamaue N, Sumikawa K (2002) Nicotine compensates for the loss of cholinergic function to enhance long-term potentiation induction. Brain Res 946(1):148-152. (Pubitemid 34804714)
22. Salter MW, Kalia LV (2004) Src kinases: A hub for NMDA receptor regulation. Nat Rev Neurosci 5(4):317-328. (Pubitemid 38478658)
23. Reid RT, Lloyd GK, Rao TS (1999) Pharmacological characterization of nicotine-induced acetylcholine release in the rat hippocampus in vivo: Evidence for a permissive dopamine synapse. Br J Pharmacol 127(6):1486-1494. (Pubitemid 29358951)
24. Marino MJ, Rouse ST, Levey AI, Potter LT, Conn PJ (1998) Activation of the genetically defined m1 muscarinic receptor potentiates N-methyl-D-aspartate (NMDA) receptor currents in hippocampal pyramidal cells. Proc Natl Acad Sci USA 95(19):11465-11470. (Pubitemid 28450152)
25. Gower AJ (1987) Effects of acetylcholine agonists and antagonists on yawning and analgesia in the rat. Eur J Pharmacol 139(1):79-89.
26. Seo H, Ferree AW, Isacson O (2002) Cortico-hippocampal APP and NGF levels are dynamically altered by cholinergic muscarinic antagonist or M1 agonist treatment in normal mice. Eur J Neurosci 15(3):498-506. (Pubitemid 35463668)
27. Rauner C, Köhr G (2011) Triheteromeric NR1/NR2A/NR2B receptors constitute the major N-methyl-D-aspartate receptor population in adult hippocampal synapses. J Biol Chem 286(9):7558-7566.
28. Petralia RS (2012) Distribution of extrasynaptic NMDA receptors on neurons. ScientificWorldJournal 2012:267120.
29. Tang YP, et al. (1999) Genetic enhancement of learning and memory in mice. Nature 401(6748):63-69.
30. Thinschmidt JS, Frazier CJ, King MA, Meyer EM, Papke RL (2005) Medial septal/diagonal band cells express multiple functional nicotinic receptor subtypes that are correlated with firing frequency. Neurosci Lett 389(3):163-168. (Pubitemid 41267219)
31. Liu Q, et al. (2009) A novel nicotinic acetylcholine receptor subtype in basal forebrain cholinergic neurons with high sensitivity to amyloid peptides. J Neurosci 29(4):918-929.
32. Billard W, Binch H, 3rd, Crosby G, McQuade RD (1995) Identification of the primary muscarinic autoreceptor subtype in rat striatum as m2 through a correlation of in vivo microdialysis and in vitro receptor binding data. J Pharmacol Exp Ther 273(1):273-279.
33. Daeffler L, Schmidlin F, Gies JP, Landry Y (1999) Inverse agonist activity of pirenzepine at M2 muscarinic acetylcholine receptors. Br J Pharmacol 126(5):1246-1252. (Pubitemid 29123762)
34. Imperato A, Scrocco MG, Ghirardi O, Ramacci MT, Angelucci L (1991) In vivo probing of the brain cholinergic system in the aged rat. Effects of long-term treatment with acetyl-L-carnitine. Ann N Y Acad Sci 621:90-97.
35. Wall SJ, Wolfe BB, Kromer LF (1994) Cholinergic deafferentation of dorsal hippocampus by fimbria-fornix lesioning differentially regulates subtypes (m1-m5) of muscarinic receptors. J Neurochem 62(4):1345-1351.
36. Pohorecki R, Head R, Domino EF (1988) Effects of selected muscarinic cholinergic antagonists on [3H]acetylcholine release from rat hippocampal slices. J Pharmacol Exp Ther 244(1):213-217. (Pubitemid 18042383)
37. Quirion R, et al. (1995) Facilitation of acetylcholine release and cognitive performance by an M(2)-muscarinic receptor antagonist in aged memory-impaired. J Neurosci 15(2):1455-1462.
38. Porter AC, et al. (2002) M1 muscarinic receptor signaling in mouse hippocampus and cortex. Brain Res 944(1-2):82-89. (Pubitemid 34775011)
39. Levey AI, Edmunds SM, Koliatsos V, Wiley RG, Heilman CJ (1995) Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J Neurosci 15(5 Pt 2):4077-4092.
40. Barnes CA, et al. (2000) Chronic treatment of old rats with donepezil or galantamine: Effects on memory, hippocampal plasticity and nicotinic receptors. Neuroscience 99(1):17-23. (Pubitemid 30495548)
41. Wettstein A, Spiegel R (1984) Clinical trials with the cholinergic drug RS 86 in Alzheimer's disease (AD) and senile dementia of the Alzheimer type (SDAT). Psychopharmacology (Berl) 84(4):572-573. (Pubitemid 15179682)
42. Miura M, Watanabe M, Offermanns S, Simon MI, Kano M (2002) Group I metabotropic glutamate receptor signaling via Galpha q/Galpha 11 secures the induction of long-term potentiation in the hippocampal area CA1. J Neurosci 22(19):8379-8390. (Pubitemid 35387578)
43. Pitcher GM, et al. (2011) Schizophrenia susceptibility pathway neuregulin 1-ErbB4 suppresses Src upregulation of NMDA receptors. Nat Med 17(4):470-478.
44. Potter PE, Gaughan C, Assouline Y (1999) Lesion of septal-hippocampal neurons with 192 IgG-saporin alters function of M1 muscarinic receptors. Neuropharmacology 38(4):579-586. (Pubitemid 29088235)
45. Janičková H, et al. (2013) Uncoupling of M1 muscarinic receptor/G-protein interaction by amyloid β(1-42). Neuropharmacology 67:272-283.
46. Tsang SW, 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. Neurobiol Aging 27(9):1216-1223. (Pubitemid 44088578)
47. Committee on Care and Use of Laboratory Animals (1985) Guide for the Care and Use of Laboratory Animals (Natl Inst Health, Bethesda), DHHS Publ No (NIH) 85-23.