Behavioral phenotyping of heterozygous acetylcholinesterase knockout (AChE+/-) mice showed no memory enhancement but hyposensitivity to amnesic drugs

Behavioural Brain Research

Volumn 206, Issue 2, 2010, Pages 263-273

  Espallergues, Julie ^a,b,c   Galvan, Laurie ^a,b,c   Sabatier, Florence ^c,d   Rana Poussine, Vanessa ^c,d   Maurice, Tangui ^a,b,c   Chatonnet, Arnaud ^c,d  

^a University of Montpellier   (France)

^b PSL RESEARCH UNIVERSITY   (France)

^c UNIV MONTPELLIER   (France)

^d University of Montpellier   (France)

Author keywords

Acetylcholinesterase; Amyloid toxicity; Knockout model; Learning and memory; Scopolamine

Indexed keywords

ACETYLCHOLINESTERASE; AMYLOID BETA PROTEIN[25-35]; CHOLINESTERASE; SCOPOLAMINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN CORTEX; BRAIN LEVEL; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; ENZYME ACTIVITY; EXPLORATORY BEHAVIOR; FEMALE; HETEROZYGOSITY; HIPPOCAMPUS; KNOCKOUT MOUSE; LEARNING; LEARNING DISORDER; LIPID PEROXIDATION; LOCOMOTION; MALE; MAZE TEST; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OPEN FIELD TEST; PHENOTYPE; PRIORITY JOURNAL; SPATIAL DISCRIMINATION; TOXICITY TESTING; WORKING MEMORY;

ACETYLCHOLINESTERASE; AMYLOID BETA-PROTEIN; ANALYSIS OF VARIANCE; ANIMALS; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; FEMALE; HETEROZYGOTE; HIPPOCAMPUS; LIPID PEROXIDATION; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; MUSCARINIC ANTAGONISTS; PEPTIDE FRAGMENTS; PHENOTYPE; SCOPOLAMINE; SEX FACTORS;

EID: 70350336541     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.09.024     Document Type: Article

References (59)

1. 25-35. Behav Brain Res 180 (2007) 139-145
2. Alvarez A., Alarcon R., Opazo C., Campos E.O., Munoz F.J., Calderon F.H., et al. Stable complexes involving acetylcholinesterase and amyloid-β peptide change the biochemical properties of the enzyme and increase the neurotoxicity of Alzheimer's fibrils. J Neurosci 18 (1998) 3213-3223
3. Arias E., Gallego-Sandín S., Villarroya M., García A.G., and López M.G. Unequal neuroprotection afforded by the acetylcholinesterase inhibitors galantamine, donepezil, and rivastigmine in SH-SY5Y neuroblastoma cells: role of nicotinic receptors. J Pharmacol Exp Ther 315 (2005) 1346-1353
4. 7 nicotinic receptor in oral keratinocytes. FASEB J 20 (2006) 2093-2101
5. Buckingham S.D., Jones A.K., Brown L.A., and Sattelle D.B. Nicotinic acetylcholine receptor signalling: roles in Alzheimer's disease and amyloid neuroprotection. Pharmacol Rev 61 (2009) 39-61
6. Butterfield D.A., Reed T., Newman S.F., and Sultana R. Roles of amyloid β-peptide-associated oxidative stress and brain protein modifications in the pathogenesis of Alzheimer's disease and mild cognitive impairment. Free Radic Biol Med 43 (2007) 658-677
7. Chacon M.A., Reyes A.E., and Inestrosa N.C. Acetylcholinesterase induces neuronal cell loss, astrocyte hypertrophy and behavioral deficits in mammalian hippocampus. J Neurochem 87 (2003) 195-204
8. Crawley J.N., Belknap J.K., Collins A., Crabbe J.C., Frankel W., Henderson N., et al. Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology 132 (1997) 107-124
9. 7 nicotinic acetylcholine receptors: in vitro and in vivo mechanisms related to Alzheimer's disease. J Neurosci 21 (2001) 4125-4133
10. Ellman G.L., Courtney K.D., Andres V., and Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7 (1961) 88-95
11. Erme M., Geula C., Ransil B.J., and Mesulam M.M. The acute neurotoxicity and effects upon cholinergic axons or intracerebrally injected β-amyloid in the rat brain. Neurobiol Aging 13 (1992) 553-559
12. 1 receptor activates Nrf2 through a signaling cascade that involves protein kinase C and inhibition of GSK-3β: connecting neurotransmission with neuroprotection. J Neurochem 110 (2009) 1107-1119
13. +/-) mice. Chem Biol Interact 175 (2008) 131-134
14. 25-35-induced mouse hippocampal injury and learning and memory impairment. Acta Pharmacol Sin 27 (2006) 651-658
15. Fleischhacker W.W., Buchgeher A., and Schubert H. Memantine in the treatment of senile dementia of the Alzheimer type. Prog Neuropsychopharmacol Biol Psychiatr 10 (1986) 87-93
16. Francis P.T., Nordberg A., and Arnold S.E. A preclinical view of cholinesterase inhibitors in neuroprotection: do they provide more than symptomatic benefits in Alzheimer's disease?. Trends Pharmacol Sci 26 (2005) 104-111
17. Girard E., Barbier J., Chatonnet A., Krejci E., and Molgo J. Synaptic remodeling at the skeletal neuromuscular junction of acetylcholinesterase knockout mice and its physiological relevance. Chem Biol Interact 157 (2005) 87-96
18. Girard E., Bernard V., Minic J., Chatonnet A., Krejci E., and Molgo J. Butyrylcholinesterase and the control of synaptic responses in acetylcholinesterase knockout mice. Life Sci 80 (2007) 2380-2385
19. 4 muscarinic acetylcholine receptor knockout mice. Proc Natl Acad Sci USA 96 (1999) 10483-10488
20. Hermes-Lima M., Willmore W.G., and Storey K.B. Quantification of lipid peroxidation in tissue extracts based on Fe(III)xylenol orange complex formation. Free Radic Biol Med 19 (1995) 271-280
21. Inestrosa N.C., Alvarez A., Perez C., Moreno R., Vicente M., Linker C., et al. Acetylcholinesterase accelerates assembly of amyloid-β-peptides into Alzheimer's fibrils: possible role of the peripheral site of the enzyme. Neuron 16 (1996) 881-891
22. Joseph J.A., and Fisher D.R. Muscarinic receptor subtype determines vulnerability to amyloid toxicity in transfected cos-7 cells. J Alzheimers Dis 5 (2003) 197-208
23. Kettenman H. Neuroscience: the brain's garbage men. Nature 446 (2007) 987-989
24. Kihara T., Sawada H., Nakamizo T., Kanki R., Yamashita H., Maelicke A., et al. Galantamine modulates nicotinic receptor and blocks Aβ-enhanced glutamate toxicity. Biochem Biophys Res Commun 325 (2004) 976-982
25. 7 Nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block a β-amyloid-induced neurotoxicity. J Biol Chem 276 (2001) 13541-13546
26. Kihara T., Shimohama S., Sawada H., Kimura J., Kume T., Kochiyama H., et al. Nicotinic receptor stimulation protects neurons against β-amyloid toxicity. Ann Neurol 42 (1997) 159-163
27. Kornhuber J., and Weller M. Psychotogenicity and N-methyl-d-aspartate receptor antagonism: implications for neuroprotective pharmacotherapy. Biol Psychiatr 41 (1997) 135-144
28. 25-35-induced neurodegeneration. Eur J Neurosci 23 (2006) 1417-1426
29. Levey A.I., Edmunds S.M., Koliatsos V., Wiley R.G., and Heilman C.J. Expression of M1-M4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J Neurosci 15 (1995) 4077-4092
30. Levey A.I., Kitt C.A., Simonds W.F., Price D.L., and Brann M.R. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci 11 (1991) 3218-3226
31. Levey A.I. Muscarinic acetylcholine receptor expression in memory circuits: implications for treatment of Alzheimer disease. Proc Natl Acad Sci USA 93 (1996) 13541-13546
32. Li B., Duysen E.G., Volpicelli-Daley L.A., Levey A.I., and Lockridge O. Regulation of muscarinic acetylcholine receptor function in acetylcholinesterase knockout mice. Pharmacol Biochem Behav 74 (2003) 977-986
33. Liu Q., Zhang J., Zhu H., Qin C., Chen Q., and Zhao B. Dissecting the signaling pathway of nicotine-mediated neuroprotection in a mouse Alzheimer disease model. FASEB J 21 (2007) 61-73
34. Mash D.C., Flynn D.D., and Potter L.T. Loss of M2 muscarine receptors in the cerebral cortex in Alzheimer's disease and experimental cholinergic denervation. Science 228 (1985) 1115-1117
35. 2+ homeostasis in Alzheimer's disease. Trends Neurosci 16 (1993) 409-414
36. Maurice T., Duclot F., Meunier J., Naert G., Givalois L., Meffre J., et al. Altered memory capacities and response to stress in p300/CBP-associated factor (PCAF) histone acetylase knockout mice. Neuropsychopharmacology 33 (2008) 1584-1602
37. Maurice T., Hippert C., Serratrice N., Dubois G., Jacquet C., Antignac C., et al. Cystine accumulation in the CNS results in severe age-related memory deficits. Neurobiol Aging 30 (2009) 987-1000
38. Maurice T., Lockhart B.P., and Privat A. Amnesia induced in mice by centrally administered β-amyloid peptides involves cholinergic dysfunction. Brain Res 706 (1996) 181-193
39. Melo J.B., Agostinho P., and Oliveira C.R. Involvement of oxidative stress in the enhancement of acetylcholinesterase activity induced by amyloid β-peptide. Neurosci Res 45 (2003) 117-127
40. 1 receptor. Br J Pharmacol 149 (2006) 998-1012
41. Miyakawa T., Yamada M., Duttaroy A., and Wess J. Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor. J Neurosci 21 (2001) 5239-5250
42. Ogura H., Kosasa T., Kuriya Y., and Yamanishi Y. Comparison of inhibitory activities of donepezil and other cholinesterase inhibitors on acetylcholinesterase and butyrylcholinesterase in vitro. Methods Find Exp Clin Pharmacol 22 (2000) 609-613
43. Pappolla M.A., Omar R.A., Kim K.S., and Robakis N.K. Immunohistochemical evidence of oxidative [corrected] stress in Alzheimer's disease. Am J Pathol 140 (1992) 621-628
44. Perry E.K., Tomlinson B.E., Blessed G., Bergman K., Gibson P.H., and Perry R.H. Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Br Med J 2 (1978) 1457-1459
45. Polinsky R.J. Clinical pharmacology of rivastigmine: a new-generation acetylcholinesterase inhibitor for the treatment of Alzheimer's disease. Clin Ther 20 (1998) 634-647
46. Reyes A.E., Chacon M.A., Dinamarca M.C., Cerpa W., Morgan C., and Inestrosa N.C. Acetylcholinesterase-Aβ complexes are more toxic than Aβ fibrils in rat hippocampus: Effect on rat β-amyloid aggregation, laminin expression, reactive astrocytosis, and neuronal cell loss. Am J Pathol 164 (2004) 2163-2174
47. Selkoe D.J. Alzheimer's disease: a central role for amyloid. J Neuropathol Exp Neurol 53 (1994) 438-447
48. Selkoe D.J. Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat Cell Biol 6 (2004) 1054-1061
49. Selkoe D.J. The molecular pathology of Alzheimer's disease. Neuron 6 (1991) 487-498
50. Sherman K.A., and Messamore E. Cholinesterase inhibitor therapy for Alzheimer dementia: what do animal models tell us?. Prog Clin Biol Res. 317 (1989) 1209-1222
51. 25-35 in rat PC12 cells. Neuroreport 9 (1998) 1519-1522
52. Tzavara E.T., Bymaster F.P., Felder C.C., Wade M., Gomeza J., Wess J., et al. Dysregulated hippocampal acetylcholine neurotransmission and impaired cognition in M2, M4 and M2/M4 muscarinic receptor knockout mice. Mol Psychiatr 8 (2003) 673-679
53. Um M.Y., Choi W.H., Aan J.Y., Kim S.R., and Ha T.Y. Protective effect of Polygonum multiflorum Thunb on amyloid β-peptide 25-35 induced cognitive deficits in mice. J Ethnopharmacol 104 (2006) 144-148
54. 25-35-induced toxicity in mice. Neuropsychopharmacology 34 (2009) 1552-1566
55. Volpicelli-Daley L.A., Duysen E.G., Lockridge O., and Levey A.I. Altered hippocampal muscarinic receptors in acetylcholinesterase-deficient mice. Ann Neurol 53 (2003) 788-796
56. Volpicelli-Daley L.A., Hrabovska A., Duysen E.G., Ferguson S.M., Blakely R.D., Lockridge O., et al. Altered striatal function and muscarinic cholinergic receptors in acetylcholinesterase knockout mice. Mol Pharmacol 64 (2003) 1309-1316
57. Weinstock M. The pharmacotherapy of Alzheimer's disease based on the cholinergic hypothesis: an update. Neurodegeneration 4 (1995) 349-356
58. Williamson R., Scales T., Clark B.R., Gibb G., Reynolds C.H., Kellie S., et al. Rapid tyrosine phosphorylation of neuronal proteins including tau and focal adhesion kinase in response to amyloid-β peptide exposure: involvement of Src family protein kinases. J Neurosci 22 (2002) 10-20
59. Yamada K., and Nabeshima T. Animal models of Alzheimer's disease and evaluation of anti-dementia drugs. Pharmacol Ther 88 (2000) 93-113