Effects of sub-chronic donepezil on brain Abeta and cognition in a mouse model of Alzheimer's disease

Psychopharmacology

Volumn 230, Issue 2, 2013, Pages 279-289

  Easton, Amy ^a   Sankaranarayanan, Sethu ^a   Tanghe, An ^a   Terwel, Dick ^a   Lin, Alan X ^a   Hoque, Nina ^a   Bourin, Clotilde ^a   Gu, Huidong ^a   Ahlijanian, Michael ^a   Bristow, Linda ^a  

^a BRISTOL MYERS SQUIBB   (United States)

Author keywords

Acetylcholine; Acetylcholinesterase; Alzheimer; Amyloid; Animal model; APP; Cognition; Glia; Tau

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; DONEPEZIL; PRESENILIN 1; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; DRUG BLOOD LEVEL; DRUG BRAIN LEVEL; FEMALE; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; REFERENCE MEMORY; SHORT COURSE THERAPY; SPATIAL LEARNING; SPATIAL MEMORY; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; CHOLINESTERASE INHIBITORS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HUMANS; INDANS; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; PIPERIDINES; PRESENILIN-1; SYNAPSES;

EID: 84891835593     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-013-3152-3     Document Type: Article

References (68)

1. Akasofu S, Kosasa T, Kimura M, Kubota A (2003) Protective effect of donepezil in a primary culture of rat cortical neurons exposed to oxygen-glucose deprivation. Eur J Pharmacol 472(1-2):57-63
2. Ashe KH, Zahs KR (2010) Probing the biology of Alzheimer's disease in mice. Neuron 66(5):631-645
3. Ballard CG, Chalmers KA, Tod C, McKeith IG, O'Brien JT, Wilock G, Love S, Perry EK (2007) Cholinesterase inhibitors reduce cortical Abeta in dementia with Lewy bodies. Neurology 68(20):1726-1179
4. Ballatore C, Lee VM, Trojanowski J (2007) Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat Rev Neurosci 8(9):663-672
5. Beach TG, Kuo YM, Spiegel K, Emmerling MR, Sue LI, Kokjohn K, Roher AE (2000) The cholinergic deficit coincides with Aβ deposition at the earliest histopathologic stages of Alzheimer disease. J Neuropathol Exp Neurol 59(4):308-313
6. Bejar C, Wang RH, Weinstock M (1999) Effect of rivastigmine on scopolamine-induced memory impairment in rats. Eur J Pharmacol 383(3):231-240
7. Bitan G, Fradinger EA, Spring SM, Teplow DB (2005) Neurotoxic protein oligomers - what you see is not always what you get. Amyloid 12(2):88-95
8. Bitner RS, Nikkel AL, Markosyan S, Otte S, Puttfarcken P, Gopalakrishnan M (2009) Selective alpha7 nicotinic acetylcholine receptor activation regulates glycogen synthase kinase3beta and decreases tau phosphorylation in vivo. Brain Res 1265:65-74
9. Bitner RS, Bunnelle WH, Decker MW, Drescher KU, Kohlhaas KL, Markosyan S, Marsh KC, Nikkel AL, Browman K, Radek R, Anderson DJ, Buccafusco J, Gopalakrishnan M (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(3):875-886
10. Black SE, Doody R, Li H, McRae T, Jambor KM, Xu Y, Sun Y, Perdomo CA, Richardson S (2007) Donepezil preserves cognition and global function in patients with severe Alzheimer disease. Neurology 69(5):459-469
11. Braida D, Paladini E, Griffini P, Lamperti M, Maggi A, Sala M (1996) An inverted U-shaped curve for heptylphysostigmine on radial maze performance in rats: comparison with other cholinesterase inhibitors. Eur J Pharmacol 302(1-3):13-20
12. Bruggink KA, Müller M, Kuiperij HB, Verbeek MM (2012) Methods for analysis of amyloid-β aggregates. J Alzheimers Dis 28(4):735-758
13. Buccafusco JJ (2009) The revival of scopolamine reversal for the assessment of cognition-enhancing drugs. In: Buccafusco JJ (ed) Methods of behavior analysis in neuroscience, 2nd edn. CRC, Boca Raton, Chapter 17
14. Burns A, Rossor M, Hecker J, Gauthier S, Petit H, Möller HJ, Rogers SL, Friedhoff LT (1999) The effects of donepezil in Alzheimer's disease - results from a multinational trial. Dement Geriatr Cogn Disord 10(3):237-244
15. Caccamo A, Oddo S, Billings LM, Green KN, Martinez-Coria H, Fisher A, LaFerla FM (2006) M1 receptors play a central role in modulating AD-like pathology in transgenic mice. Neuron 49(5):671-682
16. Cummings JL, Back C (1998) The cholinergic hypothesis of neuropsychiatric symptoms in Alzheimer's disease. Am J Geriatr Psychiatry 6(2 Suppl 1):S64-S78
17. Das UN (2007) Acetylcholinesterase and butyrylcholinesterase as possible markers of low-grade systemic inflammation. Med Sci Monit 13(12):RA214-RA221, Review
18. Davis AA, Fritz JJ, Wess J, Lah JJ, Levey AI (2010) Deletion of M1 muscarinic acetylcholine receptors increases amyloid pathology in vitro and in vivo. J Neurosci 30(12):4190-4196
19. Deng J, Shen C, Wang YJ, Zhang M, Li J, Xu ZQ, Gao CY, Fang CQ, Zhou HD (2010) Nicotine exacerbates tau phosphorylation and cognitive impairment induced by amyloid-beta 25-35 in rats. Eur J Pharmacol 637(1-3):83-88
20. Dewachter I, Van Dorpe J, Smeijers L, Gilis M, Kuipéri C, Laenen I, Caluwaerts N, Moechars D, Checler F, Vanderstichele H, Van Leuven F (2000) Aging increased amyloid peptide and caused amyloid plaques in brain of old APP/V717I transgenic mice by a different mechanism than mutant presenilin1. J Neurosci 20(17):6452-6458
21. Dong H, Csernansky CA, Martin MV, Bertchume A, Vallera D, Csernansky JG (2005) Acetylcholinesterase inhibitors ameliorate behavioral deficits in the Tg2576 mouse model of Alzheimer's disease. Psychopharmacology (Berlin) 181(1):145-152
22. Dong H, Yuede CM, Coughlan CA, Murphy KM, Csernansky JG (2009) Effects of donepezil on amyloid-beta and synapse density in the Tg2576 mouse model of Alzheimer's disease. Brain Res 1303:169-178
23. Feldman H, Gauthier S, Hecker J, Vellas B, Subbiah P, Whalen E, Donepezil MSAD Study Investigators Group (2001) A 24-week, randomized, double-blind study of donepezil in moderate to severe Alzheimer's disease. Neurology 57(4):613-620
24. Feldman H, Gauthier S, Hecker J, Vellas B, Xu Y, Ieni JR, Schwam EM, Donepezil MSAD Study Investigators Group (2005) Efficacy and safety of donepezil in patients with more severe Alzheimer's disease: a subgroup analysis from a randomized, placebo-controlled trial. Int J Geriatr Psychiatry 20(6):559-569
25. Fisher A (2012) Cholinergic modulation of amyloid precursor protein processing with emphasis on M1 muscarinic receptor: perspectives and challenges in treatment of Alzheimer's disease. J Neurochem 120(Suppl 1):22-33
26. Gordon MN, Holcomb LA, Jantzen PT, DiCarlo G, Wilcock D, Boyett KW, Connor K, Melachrino J, O'Callaghan JP, Morgan D (2002) Time course of the development of Alzheimer-like pathology in the doubly transgenic PS1+APP mouse. Exp Neurol 173:183-195
27. Hashimoto M, Kazui H, Matsumoto K, Nakano Y, Yasuda M, Mori E (2005) Does donepezil treatment slow the progression of hippocampal atrophy in patients with Alzheimer's disease? Am J Psychiatry 162(4):676-682
28. Hebert LE, Scherr PA, Bienias JL, Bennett DA, Evans DA (2003) Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch Neurol 60(8):1119-1122
29. Heneka MT, Sastre M, Dumitrescu-Ozimek L, Dewachter I, Walter J, Klockgether T, Van Leuven F (2005) Focal glial activation coincides with increased BACE1 activation and precedes amyloid plaque deposition in APP[V717I] transgenic mice. J Neuroinflammation 2(22)
30. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C, Younkin S, Hsiao K, Duff K (1998) Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4:97-100
31. Hwang J, Hwang H, Lee HW, Suk K (2010) Microglia signaling as a target of donepezil. Neuropharmacology 58(7):1122-1129, Epub 2010 Feb 11
32. Jeon S, Bose S, Hur J, Jun K, Kim YK, Cho KS, Koo BS (2011) A modified formulation of Chinese traditional medicine improves memory impairment and reduces Aβ level in the Tg-APPswe/PS1dE9 mouse model of Alzheimer's disease. J Ethnopharmacol 137(1):783-789
33. Krishnan KR, Charles HC, Doraiswamy PM, Mintzer J, Weisler R, Yu X, Perdomo C, Ieni JR, Rogers S (2003) Randomized, placebo-controlled trial of the effects of donepezil on neuronal markers and hippocampal volumes in Alzheimer's disease. Am J Psychiatry 160(11):2003-2011
34. Lenz RA, Baker JD, Locke C, Rueter LE, Mohler EG, Wesnes K, Abi-Saab W, Saltarelli MD (2012) The scopolamine model as a pharmacodynamic marker in early drug development. Psychopharmacology (Berlin) 220(1):97-107
35. Lindner MD, Hogan JB, Hodges DB Jr, Orie AF, Chen P, Corsa JA, Leet JE, Gillman KW, Rose GM, Jones KM, Gribkoff VK (2006) Donepezil primarily attenuates scopolamine-induced deficits in psychomotor function, with moderate effects on simple conditioning and attention, and small effects on working memory and spatial mapping. Psychopharmacology (Berlin) 188(4):629-640
36. Lopez OL, Becker JT, Saxton J, Sweet RA, Klunk W, DeKosky ST (2005) Alteration of a clinically meaningful outcome in the natural history of Alzheimer's disease by cholinesterase inhibition. J Am Geriatr Soc 53(1):83-87
37. Lu PH, Edland SD, Teng E, Tingus K, Petersen RC, Cummings JL, Alzheimer's Disease Cooperative Study Group (2009) Donepezil delays progression to AD in MCI subjects with depressive symptoms. Neurology 72(24):2115-2121
38. Masuoka T, Kamei C (2009) The role of nicotinic receptors in the amelioration of cholinesterase inhibitors in scopolamine-induced memory deficits. Psychopharmacology (Berlin) 206(2):259-265
39. Medeiros R, Kitazawa M, Caccamo A, Baglietto-Vargas D, Estrada-Hernandez T, Cribbs DH, Fisher A, LaFerla FM (2011) Loss of muscarinic M1 receptor exacerbates Alzheimer's disease-like pathology and cognitive decline. Am J Pathol 179(2):980-991
40. Moechars D, Dewachter I, Lorent K, Reversé D, Baekelandt V, Naidu A, Tesseur I, Spittaels K, Haute CV, Checler F, Godaux E, Cordell B, Van Leuven F (1999) Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J Biol Chem 274(10):6483-6492
41. Mohs RC, Doody RS, Morris JC, Ieni JR, Rogers SL, Perdomo CA, Pratt RD, "312" Study Group (2001) A 1-year, placebo-controlled preservation of function survival study of donepezil in AD patients. Neurology 57(3):481-488
42. Morris RG, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297(5868):681-683
43. Morris M, Maeda S, Vossel K, Mucke L (2011) The many faces of tau. Neuron 70(3):410-426
44. Mullan M (2000) Genetic contributions to causes of Alzheimer's disease: current perspectives and future directions, pp 307-309. In: New insights into genetics and pathophysiology of Alzheimer's disease: what are the clinical and therapeutic implications? J Clin Psychiatry 61(4):307-15
45. Nitsch RM, Deng M, Tennis M, Schoenfeld D, Growdon JH (2000) The selective muscarinic M1 agonist AF102B decreases levels of total Aβ in cerebrospinal fluid of patients with Alzheimer's disease. Ann Neurol 48(6):913-918
46. Noh MY, Koh SH, Kim Y, Kim HY, Cho GW, Kim SH (2009) Neuroprotective effects of donepezil through inhibition of GSK-3 activity in amyloid-beta-induced neuronal cell death. J Neurochem 108(5):1116-1125
47. Oddo S, Caccamo A, Green KN, Liang K, Tran L, Chen Y, Leslie FM, LaFerla FM (2005) Chronic nicotine administration exacerbates tau pathology in a transgenic model of Alzheimer's disease. Proc Natl Acad Sci U S A 102(8):3046-3051
48. Raskind MA, Peskind ER, Wessel T, Yuan W (2000) Galantamine in AD: a 6-month randomized, placebo-controlled trial with a 6-month extension. The Galantamine USA-1 Study Group. Neurology 54(12):2261-2268
49. Rogers SL, Farlow MR, Doody RS, Mohs R, Friedhoff LT (1998) A 24-week, double-blind, placebo-controlled trial of donepezil in patients with Alzheimer's disease. Donepezil Study Group. Neurology 50(1):136-145
50. Romberg C, Mattson MP, Mughal MR, Bussey TJ, Saksida LM (2011) Impaired attention in the 3xTgAD mouse model of Alzheimer's disease: rescue by donepezil (Aricept). J Neurosci 31(9):3500-3507
51. Sabbagh MN, Walker DG, Reid RT, Stadnick T, Anand K, Lue LF (2008) Absence of effect of chronic nicotine administration on amyloid beta peptide levels in transgenic mice overexpressing mutated human APP (Sw, Ind). Neurosci Lett 448(2):217-220
52. Selkoe DJ (2008) Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav Brain Res 192(1):106-113
53. Seltzer B (2005) Donepezil: a review. Expert Opin Drug Metab Toxicol 1(3):527-536, Review
54. Takada Y, Yonezawa A, Kume T, Katsuki H, Kaneko S, Sugimoto H, Akaike A (2003) Nicotinic acetylcholine receptor-mediated neuroprotection by donepezil against glutamate neurotoxicity in rat cortical neurons. J Pharmacol Exp Ther 306(2):772-777
55. Takata K, Kitamura Y, Saeki M, Terada M, Kagitani S, Kitamura R, Fujikawa Y, Maelicke A, Tomimoto H, Taniguchi T, Shimohama S (2010) Galantamine-induced amyloid-{beta} clearance mediated via stimulation of microglial nicotinic acetylcholine receptors. J Biol Chem 285(51):40180-40191
56. Terwel D, Muyllaert D, Dewachter I, Borghgraef P, Croes S, Devijver H, Van Leuven F (2008) Amyloid activates GSK-3beta to aggravate neuronal tauopathy in bigenic mice. Am J Pathol 172(3):786-798
57. Toyn JH, Lin XA, Thompson MW, Guss V, Meredith JE Jr, Sankaranarayanan S, Barrezueta N, Corradi J, Majumdar A, Small DL, Hansard M, Lanthorn T, Westphal RS, Albright CF (2010) Viable mouse gene ablations that robustly alter brain Aβ levels are rare. BMC Neurosci 11:143
58. Tsunekawa H, Noda Y, Mouri A, Yoneda F, Nabeshima T (2008) Synergistic effects of selegiline and donepezil on cognitive impairment induced by amyloid beta (25-35). Behav Brain Res 190(2):224-232
59. Tyagi E, Agrawal R, Nath C, Shukla R (2007) Effect of anti-dementia drugs on LPS induced neuroinflammation in mice. Life Sci 80(21):1977-1983
60. Van Dam D, Abramowski D, Staufenbiel M, De Deyn PP (2005) Symptomatic effect of donepezil, rivastigmine, galantamine and memantine on cognitive deficits in the APP23 model. Psychopharmacology (Berlin) 180(1):177-190
61. Van Dam D, Coen K, De Deyn PP (2008) Cognitive evaluation of disease-modifying efficacy of donepezil in the APP23 mouse model for Alzheimer's disease. Psychopharmacology (Berlin) 197(1):37-43
62. Watanabe T, Iwasaki K, Ishikane S, Naitou T, Yoshimitsu Y, Yamagata N, Ozdemir MB, Takasaki K, Egashira N, Mishima K, Fujiwara M (2008) Spatial memory impairment without apoptosis induced by the combination of beta-amyloid oligomers and cerebral ischemia is related to decreased acetylcholine release in rats. J Pharmacol Sci 106(1):84-91
63. Watt AD, Perez KA, Rembach A, Sherrat NA, Hung LW, Johanssen T, McLean CA, Kok WM, Hutton CA, Fodero-Tavoletti M, Masters CL, Villemagne VL, Barnham KJ (2013) Oligomers, fact or artefact? SDS-PAGE induces dimerization of β-amyloid in human brain samples. Acta Neuropathol 125(4):549-564
64. Wilkinson D, Schindler R, Schwam E, Waldemar G, Jones RW, Gauthier S, Lopez OL, Cummings J, Xu Y, Feldman HH (2009) Effectiveness of donepezil in reducing clinical worsening in patients with mild-to-moderate Alzheimer's disease. Dement Geriatr Cogn Disord 28(3):244-251
65. Winblad B (2009) Donepezil in severe Alzheimer's disease. Am J Alzheimers Dis Other Dement 24(3):185-192
66. Winblad B, Engedal K, Soininen H, Verhey F, Waldemar G, Wimo A, Wetterholm AL, Zhang R, Haglund A, Subbiah P, 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
67. Yoshiyama Y, Kojima A, Ishikawa C, Arai K (2010) Anti-inflammatory action of donepezil ameliorates tau pathology, synaptic loss, and neurodegeneration in a tauopathy mouse model. J Alzheimers Dis 22(1):295-306
68. Zhou J, Fu Y, Tang XC (2001) Huperzine A and donepezil protect rat pheochromocytoma cells against oxygen-glucose deprivation. Neurosci Neurosci Lett 306(1-2):53-56