Galantamine slows down plaque formation and behavioral decline in the 5XFAD mouse model of Alzheimer's disease

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Bhattacharya, Soumee ^a   Haertel, Christin ^a   Maelicke, Alfred ^b   Montag, Dirk ^a  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^b Galantos Pharma GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; GALANTAMINE; CHOLINESTERASE INHIBITOR;

5XFAD MOUSE; AGE DISTRIBUTION; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AVOIDANCE BEHAVIOR; BEHAVIOR; BRAIN; CELL ACTIVATION; COGNITION; CONTROLLED STUDY; DENSITY; DRUG DOSE COMPARISON; DRUG MEGADOSE; DRUG TOLERABILITY; ENTORHINAL CORTEX; FEMALE; GLIOSIS; HIPPOCAMPUS; INFANT; LIGHT DARK CYCLE; LONG TERM CARE; LOW DRUG DOSE; MALE; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; OPEN FIELD BEHAVIOR; PHENOTYPE; PLAQUE DENSITY; SEX DIFFERENCE; TREATMENT OUTCOME; ANIMAL; ANIMAL BEHAVIOR; DISEASE MODEL; DRUG EFFECTS; MAZE TEST; NERVE CELL; PATHOLOGY; PLAQUE, AMYLOID; PSYCHOLOGY;

ALZHEIMER DISEASE; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CHOLINESTERASE INHIBITORS; DISEASE MODELS, ANIMAL; FEMALE; GALANTAMINE; MALE; MAZE LEARNING; MICE; NEURONS; PLAQUE, AMYLOID; SEX FACTORS;

EID: 84896782077     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089454     Document Type: Article

References (62)

1. Karran E, Mercken M, De Strooper B (2011) The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics. Nat Rev Drug Discov 10: 698-712.
2. Citron M (2004) Strategies for disease modification in Alzheimer's disease. Nat Rev Neurosci 5: 677-685.
3. Koffie RM, Meyer-Luehmann M, Hashimoto T, Adams KW, Mielke ML, et al. (2009) Oligomeric amyloid β associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc Natl Acad Sci USA 106: 4012-4017.
4. Spires TL, Meyer-Luehmann M, Stern EA, McLean PJ, Skoch J, et al. (2005) Dendritic spine abnormalities in APP transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci 25: 7278-7287. (Pubitemid 41113944)
5. Knowles RB, Wyart C, Buldyrev SV, Cruz L, Urbanc B, et al. (1999) Plaque-induced neurite abnormalities: Implications for disruption of neural networks in Alzheimer's disease. Proc Natl Acad Sci USA 96: 5274-5279. (Pubitemid 29214573)
6. Schilling S, Zeitschel U, Hoffmann T, Heiser U, Francke M, et al. (2008) Glutaminyl cyclase inhibition attenuates pyroglutamate Aβ and Alzheimer's disease-like pathology in vivo. Nat Med 14: 1106-1111.
7. Citron M (2010) Alzheimer's disease: strategies for disease modification. Nat Rev Drug Discov 9: 387-398.
8. Patel L, Grossberg GT (2011) Combination therapy for Alzheimer's disease. Drugs Aging 28: 539-546.
9. Maelicke A, Samochock M, Jostock R, Fehrenbacher A, Ludwig J, et al. (2001) Allosteric Sensitization of Nicotinic Receptors by Galantamine, a New Treatment Strategy for Alzheimer's Disease. Biol Psychiatry 49: 279-288. (Pubitemid 32178437)
10. Peng X, Gerzanich V, Anand R, Wang F, Lindstrom J (1997) Chronic nicotine treatment up-regulates alpha3 and alpha7 acetylcholine receptor subtypes expressed by the human neuroblastoma cell line SH-SY5Y. Mol Pharmacol 51: 776-784. (Pubitemid 27224682)
11. Court JA, Perry EK (1994) CNS nicotine receptors. Possible therapeutic targets in neurodegenerative disorders. CNS Drugs 2: 216-233.
12. Kihara T, Shimohama S, Urushitani M, Sawada H, Kimura J, et al. (1998) Stimulation of alpha4beta2 nicotinic acetylcholine receptors inhibits beta-amyloid toxicity. Brain Res 792: 331-334. (Pubitemid 28267549)
13. Villarroya M, García AG, Marco-Contelles J, López MG (2007) An update on the pharmacology of galantamine. Expert Opin Investig Drugs 16: 1987-1998. (Pubitemid 351403729)
14. Lenzken SC, Lanni C, Govoni S, Lucchelli A, Schettini G, et al. (2007) Nicotinic component of galantamine in the regulation of amyloid precursor protein processing. Chem Biol Interact 165: 138-145. (Pubitemid 46091660)
15. Matharu B, Gibson G, Parsons R, Huckerby TN, Moore SA, et al. (2009) Galantamine inhibits beta-amyloid aggregation and cytotoxicity. J Neurol Sci 280: 49-58.
16. Takata K, Kitamura Y, Saeki M, Terada M, Kagitani S, et al. (2010) Galantamine-induced Amyloid-β Clearance Mediated via Stimulation of Microglial Nicotinic Acetylcholine Receptors. J Biol Chem 285: 40180-40191.
17. Wallin ÅK, Wattmo C, Minthon L (2011) Galantamine treatment in Alzheimer's disease: response and long-term outcome in a routine clinical setting. Neuropsychiatr Dis Treat 7: 565-576.
18. Kavanagh S, Gaudig M, Van Baelen B, Adami M, Delgado A, et al. (2011) Galantamine and behavior in Alzheimer disease: analysis of four trials. Acta Neurol Scand 124: 302-308.
19. Keller C, Kadir A, Forsberg A, Porras O, Nordberg A (2011) Long-term effects of galantamine treatment on brain functional activities as measured by PET in Alzheimer's disease patients. J Alz Dis 24: 109-123.
20. Oakley H, Cole SL, Logan S, Maus E, Shao P, et al. (2006) Intraneuronal β-Amyloid Aggregates, Neurodegeneration, and Neuron Loss in Transgenic Mice with Five Familial Alzheimer's Disease Mutations: Potential Factors in Amyloid Plaque Formation. J Neurosci 26: 10129-10140. (Pubitemid 44527407)
21. Ohno M, Cole SL, Yasvoina M, Zhao J, Citron M, et al. (2007) BACE1 gene deletion prevents neuron loss and memory deficits in 5XFAD APP/PS1 transgenic mice. Neurobiol Dis 26: 134-145. (Pubitemid 46436493)
22. Shukla V, Zheng YL, Mishra SK, Amin ND, Steiner J, et al. (2013) A truncated peptide from p35, a Cdk5 activator, prevents Alzheimer's disease phenotypes in model mice. FASEB J 27: 174-186.
23. Wirths O, Erck C, Martens H, Harmeier A, Geumann C, et al. (2010) Identification of low molecular weight pyroglutamate Aβ oligomers in Alzheimer's disease: a novel tool for therapy and diagnosis. J Biol Chem 285: 41517-41524.
24. Jawhar S, Trawicka A, Jenneckens C, Bayer TA, Wirths O (2012) Motor deficits, neuron loss, and reduced anxiety coinciding with axonal degeneration and intraneuronal Aβ aggregation in the 5XFAD mouse model of Alzheimer's disease. Neurobiol Aging 33: 196. e29-40.
25. Montag-Sallaz M, Schachner M, Montag D (2002) Misguided axonal projections, NCAM180 mRNA upregulation, and altered behavior in mice deficient for the Close Homolog of L1 (CHL1). Mol Cell Biol 22: 7967-7981. (Pubitemid 35217305)
26. Montag-Sallaz M, Montag D (2003) Severe cognitive and motor coordination deficits in Tenascin-R-deficient mice. Genes Brain Behav 2: 20-31. (Pubitemid 36717660)
27. Wishaw IQ, Haun F, Kolb B (1999) Analysis of behavior in laboratory rodents. In : Windhorst, U. & Johansson, H., eds. Modern Techniques in Neurosci Berlin Springer 1243-1275.
28. Rogers DC, Fisher EM, Brown SD, Peters J, Hunter AJ, et al. (1997) Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm Genome 8: 711-713. (Pubitemid 127739700)
29. Montag-Sallaz M, Montag D (2003) Learning-induced arg 3.1 expression in the mouse brain. Learn Mem 10: 99-107. (Pubitemid 36418720)
30. Comery TA, Martone RL, Aschmies S, Atchison KP, Diamantidis G, et al. (2005) Acute gamma-secretase inhibition improves contextual fear conditioning in the Tg2576 mouse model of Alzheimer's disease. J. Neurosci 25: 8898-8902. (Pubitemid 41384457)
31. Jacobsen JS, Wu CC, Redwine JM, Comery TA, Arias R, et al. (2006) Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 103: 5161-5166.
32. Sun A, Nguyen XV, Bing G (2002) Comparative analysis of an improved thioflavin-s stain, Gallyas silver stain, and immunohistochemistry for neurofibrillary tangle demonstration on the same sections. J Histochem Cytochem 50: 463-472. (Pubitemid 34250585)
33. Sturchler-Pierrat C, Staufenbiel M (2000) Pathogenic mechanisms of Alzheimer's disease analyzed in the APP23 transgenic mouse model. Ann N Y Acad Sci 920: 134-139. (Pubitemid 32056562)
34. Lewis J, Dickson DW, Lin WL, Chisholm L, Corral A, et al. (2001) Enhanced Neurofbrillary Degeneration in Transgenic Mice Expressing Mutant Tau and APP. Science 293: 1487-1491. (Pubitemid 32801551)
35. Callahan MJ, Lipinski WJ, Bian F, Durham RA, Pack A, et al. (2001) Augmented Senile Plaque Load in Aged Female b-Amyloid Precursor Protein-Transgenic Mice. Am J Pathol 158: 1173-1177. (Pubitemid 32221809)
36. Guntern R, Bouras C, Hof PR, Vallet PG (1992) An improved thioflavine S method for staining neurofibrillary tangles and senile plaques in Alzheimer's disease. Experientia 48: 8-10.
37. Annunziata I, Patterson A, Helton D, Hu H, Moshiach S, et al. (2013) Lysosomal NEU1 deficiency affects amyloid precursor protein levels and amyloid-β secretion via deregulated lysosomal exocytosis. Nat Commun 4: 2734.
38. Wengenack TM, Reyes DA, Curran GL, Borowski BJ, Lin J, et al. (2011) Regional differences in MRI detection of amyloid plaques in AD transgenic mouse brain. Neuroimage 54: 113-122.
39. Gomez-Isla T, Price JL, McKeel DW Jr, Morris JC, Growdon JH, et al. (1996) Profound Loss of Layer II Entorhinal Cortex Neurons Occurs in Very Mild Alzheimer's Disease. J Neurosci 16: 4491-4500. (Pubitemid 26243044)
40. Vassar RJ, Oakley H, Krishnamurthy S, Maus E, Shao P, et al. (2005) 5XFAD Tg mice that express five FAD mutations have high-cerebral aβ42 levels, rapid amyloid deposition, and intraneuronal aβ. Soc Neurosci Abstr 587: 2.
41. Grimm A, Lim YA, Mensah-Nyagan AG, Götz J, Eckert A (2012) Alzheimer's disease, Oestrogen and mitochondria: an ambiguous relationship. Mol Neurobiol 46: 151-160.
42. Schaeffer S, Wirths O, Multhaup G, Bayer TA (2007) Gender dependent APP processing in a transgenic mouse model of Alzheimer's disease. J Neural Transm 114: 387-394. (Pubitemid 46328658)
43. Sergi G, Rui MD, Coin A, Inelmen EM, Manzato E (2013) Weight loss and Alzheimer's disease: temporal and aetiologic connections. Proc Nutri Soc 72: 160-165.
44. Webster SJ, Bachstetter AD, Van Eldik LJ (2013) Comprehensive behavioral characterization of an APP/PS-1 double knock-in mouse model of Alzheimer's disease. Alzheimers Res Ther 5: 28.
45. Tong Y, Xu Y, Scearce-Levie K, Ptácek LJ, Fu YH (2010) COL25A1 triggers and promotes Alzheimer's disease-like pathology in vivo. Neurogenet 11: 41-52.
46. Lalonde R, Fukuchi K, Strazielle C (2012) APP transgenic mice for modelling behavioral and psychological symptoms of dementia (BPSD). Neurosci Biobehav Rev 36: 1357-1375.
47. Ohno M, Chang L, Tseng W, Oakley H, Citron M, et al. (2006) Temporal memory deficits in Alzheimer's mouse models: rescue by genetic deletion of BACE1. Eur Jour Neurosci 23: 251-260.
48. Kimura R, Ohno M (2009) Impairments in remote memory stabilization precede hippocampal synaptic and cognitive failures in 5XFAD Alzheimer mouse model. Neurobiol Dis 33: 229-235.
49. Jessen F, Kucharsk C, Fries T, Papassotiropoulos A, Hoenig K, et al. (2001) Sensory Gating Deficit Expressed by a Disturbed Suppression of the P50 Event-Related Potential in Patients With Alzheimer's Disease. Am J Psychiatry 158: 1319-1321. (Pubitemid 32717710)
50. Cancelli I, Cadore IP, Merlino G, Valentinis L, Moratti U, et al. (2006) Sensory gating deficit assessed by P50/Pb middle latency event related potential in Alzheimer's disease. J Clin Neurophys 23: 421-425. (Pubitemid 44506940)
51. Wang H, He J, Zhang R, Zhu S, Wang J, et al. (2012) Sensorimotor gating and memory deficits in an APP/PS1 double transgenic mouse model of Alzheimer's disease. Beh Brain Res 233: 237-243.
52. Prvulovic D, Hampel H, Pantel J (2010) Galantamine for Alzheimer's disease. Expert Opin. Drug Metab Toxicol 6: 345-354.
53. Seltzer B (2010) Galantamine-ER for the treatment of mild-to-moderate Alzheimer's disease. Clin Interv Aging 5: 1-6.
54. Singh M, Kaur M, Kukreja H, Chugh R, Silakari O, et al. (2013) Acetylcholinesterase inhibitors as Alzheimer therapy: From nerve toxins to neuroprotection. Eur J Med Chem 70: 165-188.
55. Rao PPN, Mohamed T, Osman W (2013) Investigating the binding interactions of galantamine with b-amyloid peptide. Bioorg Med Chem Lett 23: 239-243.
56. Unger C, Svedberg MM, Yu WF, Hedberg MM, Nordberg A (2006) Effect of subchronic treatment of memantine, galantamine, and nicotine in the brain of Tg2576 (APPswe) transgenic mice. J Pharmacol Exp Ther 317: 30-36.
57. Demattos RB, Lu J, Tang Y, Racke MM, Delong CA, et al. (2012) A plaque-specific antibody clears existing β-amyloid plaques in Alzheimer's disease mice. Neuron 76: 908-920.
58. Becker JA, Hedden T, Carmasin J, Maye J, Rentz DM, et al. (2011) Amyloid-β associated cortical thinning in clinically normal elderly. Ann Neurol 69: 1032-1042.
59. Chételat G, Villemagne VL, Villain N, Jones G, Ellis KA, et al. (2012) Accelerated cortical atrophy in cognitively normal elderly with high β-amyloid deposition. Neurol 78: 477-484.
60. Kalinin S, Polak PE, Lin SX, Sakharkar AJ, Pandey SC, et al. (2012) The noradrenaline precursor L-DOPS reduces pathology in a mouse model of Alzheimer's disease. Neurobiol Aging 33: 1651-1663.
61. Li C, Zhao R, Gao K, Wei Z, Yin MY, et al. (2011) Astrocytes: implications for neuroinflammatory pathogenesis of Alzheimer's disease. Curr Alzheimer Res 8: 67-80.
62. Maelicke A, Hoeffle-Maas A, Ludwig J, Maus A, Samochocki M, et al. (2010) Memogain is a galantamine pro-drug having dramatically reduced adverse effects and enhanced efficacy. J Mol Neurosci 40: 135-137.