Learning performances and vulnerability to amyloid toxicity in the butyrylcholinesterase knockout mouse

Behavioural Brain Research

Volumn 296, Issue , 2016, Pages 351-360

  Maurice, Tangui ^a,b,c,d   Strehaiano, Manon ^a,b,c   Siméon, Nathalie ^d   Bertrand, Christelle ^a,e   Chatonnet, Arnaud ^a,e  

^a UNIV MONTPELLIER   (France)

^b University of Montpellier   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d AMYLGEN   (France)

^e University of Montpellier   (France)

Author keywords

Alzheimer's disease; Amyloid toxicity; Butyrylcholinesterase; Knockout mice; Learning and memory

Indexed keywords

ACETYLCHOLINE; AMYLOID BETA PROTEIN[25-35]; CHOLINESTERASE; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (25-35); PEPTIDE FRAGMENT;

ACETYLCHOLINE BRAIN LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE PREDISPOSITION; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; HIPPOCAMPUS; KNOCKOUT MOUSE; LEARNING DISORDER; LIPID PEROXIDATION; MALE; MEMORY DISORDER; MOUSE; NON-SPATIAL MEMORY TEST; NONHUMAN; OPEN FIELD TEST; OXIDATIVE STRESS; PASSIVE AVOIDANCE; PRIORITY JOURNAL; SEX DIFFERENCE; SPATIAL MEMORY TEST; WATER MAZE TEST; WILD TYPE MOUSE; 129 MOUSE; ANIMAL; ANIMAL BEHAVIOR; CHEMICALLY INDUCED; COGNITIVE DEFECT; GENETICS; PATHOPHYSIOLOGY; PHYSIOLOGY; SPATIAL LEARNING;

AMYLOID BETA-PEPTIDES; ANIMALS; BEHAVIOR, ANIMAL; BUTYRYLCHOLINESTERASE; COGNITION DISORDERS; FEMALE; MALE; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; SEX FACTORS; SPATIAL LEARNING;

EID: 84960896632     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.08.026     Document Type: Article

References (54)

1. Silver A. Cholinesterases of the central nervous system with special reference to the cerebellum. Int. Rev. Neurobiol. 1967, 10:57-109.
2. Silver A. The Biology of Cholinesterases 1974, Elsevier, Amsterdam.
3. Lockridge O. Review of human butyrylcholinesterase structure, function, genetic variants, history of use in the clinic, and potential therapeutic uses. Pharmacol. Ther. 2015, 148:34-46.
4. Yamada H., Otsuka M., Fujimoto K., Kawashima K., Yoshida M. Determination of acetylcholine concentration in cerebrospinal fluid of patients with neurologic diseases. Acta Neurol. Scand. 1996, 93:76-78.
5. Li B., Stribley J.A., Ticu A., Xie W., Schopfer L.M., Hammond P., Brimijoin S., Hinrichs S.H., Lockridge O. Abundant tissue butyrylcholinesterase and its possible function in the acetylcholinesterase knockout mouse. J. Neurochem. 2000, 75:1320-1331.
6. Mesulam M.M., Guillozet A., Shaw P., Levey A., Duysen E.G., Lockridge O. Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine. Neuroscience 2002, 110:627-639.
7. Giacobini E. Selective inhibitors of butyrylcholinesterase: a valid alternative for therapy of Alzheimer's disease?. Drug Aging 2001, 18:891-898.
8. Green R.C., Mesulam M.M. Acetylcholinesterase fiber staining in the human hippocampus and parahippocampal gyrus. J. Comp. Neurol 1988, 273:488-499.
9. Mesulam M.M., Geula C. Acetylcholinesterase-rich neurons of the human cerebral cortex: cytoarchitectonic and ontogenetic patterns of distribution. J. Comp. Neurol. 1991, 306:193-220.
10. Darvesh S., Grantham D.L., Hopkins D.A. Distribution of butyrylcholinesterase in the human amygdala and hippocampal formation. J. Comp. Neurol. 1998, 393:374-390.
11. Nordberg A., Ballard C., Bullock R., Darreh-Shori T., Somogyi M. A review of butyrylcholinesterase as a therapeutic target in the treatment of Alzheimer's disease. Prim. Care Companion CNS Disord. 2013, 15. pii: PCC.12r01412.
12. Davies P., Maloney A.J. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 1976, 2:1403.
13. Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., Delon M.R. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 1982, 215:1237-1239.
14. Ciro A., Park J., Burkhard G., Yan N., Geula C. Biochemical differentiation of cholinesterases from normal and Alzheimer's disease cortex. Curr. Alzheimer Res. 2012, 9:138-143.
15. Bales K.R., Tzavara E.T., Wu S., Wade M.R., Bymaster F.P., Paul S.M., Nomikos G.G. Cholinergic dysfunction in a mouse model of Alzheimer disease is reversed by an anti-A beta antibody. J. Clin. Invest. 2006, 116:825-832.
16. Zhang W., Bai M., Xi Y., Hao J., Liu L., Mao N., Su C., Miao J., Li Z. Early memory deficits precede plaque deposition in APPswe/PS1dE9 mice: involvement of oxidative stress and cholinergic dysfunction. Free. Radic. Biol. Med. 2012, 52:1443-1452.
17. Atack J.R., Perry E.K., Bonham J.R., Perry R.H. Molecular forms of acetylcholinesterase and butyrylcholinesterase in human plasma and cerebrospinal fluid. J. Neurochem. 1987, 48:1845-1850.
18. Darvesh S., Reid G.A., Martin E. Biochemical and histochemical comparison of cholinesterases in normal and Alzheimer brain tissues. Curr. Alzheimer Res. 2010, 7:386-400.
19. Perry E.K., Perry R.H., Blessed G., Tomlinson B.E. Changes in brain cholinesterases in senile dementia of Alzheimer type. Neuropathol. Appl. Neurobiol. 1978, 4:273-277.
20. Mesulam M.M., Geula C. Butyrylcholinesterase reactivity differentiates the amyloid plaques of aging from those of dementia. Ann. Neurol. 1994, 36:722-727.
21. Guillozet A.L., Smiley J.F., Mash D.C., Mesulam M.M. Butyrylcholinesterase in the life cycle of amyloid plaques. Ann. Neurol. 1997, 42:909-918.
22. Reid G.A., Darvesh S. Butyrylcholinesterase-knockout reduces brain deposition of fibrillar β-amyloid in an Alzheimer mouse model. Neuroscience 2015, 298:424-435.
23. Darreh-Shori T., Brimijoin S., Kadir A., Almkvist O., Nordberg A. Differential CSF butyrylcholinesterase levels in Alzheimer's disease patients with the ApoE epsilon4 allele, in relation to cognitive function and cerebral glucose metabolism. Neurobiol. Dis. 2006, 24:326-333.
24. Holmes C., Ballard C., Lehmann D., David Smith A., Beaumont H., Day I.N., et al. Rate of progression of cognitive decline in Alzheimer's disease: effect of butyrylcholinesterase K gene variation. J. Neurol. Neurosurg. Psychiatry 2005, 76:640-643.
25. Bono G.F., Simão-Silva D.P., Batistela M.S., Josviak N.D., Dias P.F., Nascimento G.A., et al. Butyrylcholinesterase: K variant, plasma activity, molecular forms and rivastigmine treatment in Alzheimer's disease in a Southern Brazilian population. Neurochem. Int. 2015, 81:57-62.
26. Greig N.H., Utsuki T., Ingram D.K., Wang Y., Pepeu G., Scali C., et al. Selective butyrylcholinesterase inhibition elevates brain acetylcholine, augments learning and lowers Alzheimer beta-amyloid peptide in rodent. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:17213-17218.
27. Maurice T., Lockhart B.P., Privat A. Amnesia induced in mice by centrally administered β-amyloid peptides involves cholinergic dysfunction. Brain Res. 1996, 706:181-193.
28. 1 receptor. Br. J. Pharmacol. 2006, 149:998-1012.
29. 1) ligand ANAVEX2-73, a novel aminotetrahydrofuran derivative. J. Psychopharmacol. 2011, 25:1101-1117.
30. 25-35-induced toxicity in mice. Neuropsychopharmacology 2009, 34:1552-1566.
31. Zussy C., Brureau A., Delair B., Marchal S., Keller E., Ixart G., et al. Time-course and regional analyses of the physiopathological changes induced after cerebral injection of an amyloid-β fragment in rats. Am. J. Pathol. 2011, 179:315-334.
32. 1 receptor agonist, in a nontransgenic mouse model of Alzheimer's disease. Neuropsychopharmacology 2013, 38:1706-1723.
33. 25-35 peptide-injected mice, a nontransgenic Alzheimer's disease model. Front. Cell. Neurosci. 2015, 8:463.
34. Li B., Duysen E.G., Lockridge O. The butyrylcholinesterase knockout mouse is obese on a high-fat diet. Chem. Biol. Interact. 2008, 175:88-91.
35. Chen V.P., Gao Y., Geng L., Parks R.J., Pang Y.P., Brimijoin S. Plasma butyrylcholinesterase regulates ghrelin to control aggression. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:2251-2256.
36. Sarter M., Bodewitz G., Stephens D.N. Attenuation of scopolamine-induced impairment of spontaneous alteration behaviour by antagonist but not inverse agonist and agonist beta-carbolines. Psychopharmacology (Berl.) 1988, 94:491-495.
37. 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 2008, 33:1584-1602.
38. Crawley J.N., Belknap J.K., Collins A., Crabbe J.C., Frankel W., Henderson N., et al. Behavioural phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl.) 1997, 13:107-124.
39. +/-) mice showed no memory enhancement but hyposensitivity to amnesic drugs. Behav. Brain Res. 2010, 206:263-273.
40. +/-) mice. Chem. Biol. Interact. 2008, 175:131-134.
41. Ikari H., Spangler E.L., Greig N.H., Pei X.F., Brossi A., Speer D., et al. Maze learning in aged rats is enhanced by phenserine, a novel anticholinesterase. Neuroreport 1995, 6:481-484.
42. Ingram D.K., Shimada A., Spangler E.L., Ikari H., Hengemihle J., Kuo H., et al. Cognitive enhancement. New strategies for stimulating cholinergic, glutamatergic, and nitric oxide systems. Ann. N. Y. Acad. Sci. 1996, 786:348-361.
43. Manoharan I., Kuznetsova A., Fisk J.D., Boopathy R., Lockridge O., Darvesh S. Comparison of cognitive functions between people with silent and wild-type butyrylcholinesterase. J. Neural. Transm. 2007, 114:939-945.
44. 25-35-induced amnesia in the rat. Eur. J. Pharmacol. 1997, 319:1-4.
45. Stepanichev M.Y., Zdobnova I.M., Yakovlev A.A., Onufriev M.V., Lazareva N.A., Zarubenko I.I., et al. Effects of tumor necrosis factor-α central administration on hippocampal damage in rat induced by amyloid β-peptide (25-35). J. Neurosci. Res. 2003, 71:110-120.
46. Stepanichev M.Y., Zdobnova I.M., Zarubenko I.I., Lazareva N.A., Gulyaeva N.V. Studies of the effects of central administration of β-amyloid peptide (25-5): pathomorphological changes in the hippocampus and impairment of spatial memory. Neurosci. Behav. Physiol. 2006, 36:101-106.
47. 25-35-induced memory impairments correlate with cell loss in rat hippocampus. Physiol. Behav. 2004, 80:647-655.
48. Chavant F., Deguil J., Pain S., Ingrand I., Milin S., Fauconneau B., et al. Imipramine, in part through tumor necrosis factor inhibition, prevents cognitive decline and β-amyloid accumulation in a mouse model of Alzheimer's disease. J. Pharmacol. Exp. Ther. 2010, 332:505-514.
49. Mamiya T., Asanuma T., Kise M., Ito Y., Mizukuchi A., Aoto H., et al. Effects of pre-germinated brown rice on beta-amyloid protein-induced learning and memory deficits in mice. Biol. Pharm. Bull. 2004, 27:1041-1045.
50. 25-35. Neuroscience 2007, 145:209-224.
51. Alves-Amaral G., Pires-Oliveira M., Andrade-Lopes A.L., Chiavegatti T., Godinho R.O. Gender-related differences in circadian rhythm of rat plasma acetyl- and butyrylcholinesterase: effects of sex hormone withdrawal. Chem. Biol. Interact. 2010, 186:9-15.
52. Vest R.S., Pike C.J. Gender, sex steroid hormones, and Alzheimer's disease. Horm. Behav. 2013, 63:301-307.
53. Barry G., Ross I.L. Neurosteroids and sporadic Alzheimer's diseas. Curr. Alzheimer Res. 2008, 5:367-374.
54. 25-35 mouse model of Alzheimer's disease. Eur. J. Pharmacol. 2013, 698:193-199.