Natural amyloid-beta oligomers acutely impair the formation of a contextual fear memory in mice

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Kittelberger, Kara A ^a   Piazza, Fabrizio ^a   Tesco, Giuseppina ^a   Reijmers, Leon G ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; DIMER; MONOMER; MUTANT PROTEIN; OLIGOMER; POLYMER; TETRAMER; TRIMER; UNCLASSIFIED DRUG; PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BRAIN VENTRICLE; CONDITIONING; CONTROLLED STUDY; ELECTRIC SHOCK; FEAR; MEMORY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; ALGORITHM; ANIMAL; AVOIDANCE BEHAVIOR; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; CHO CELL; CRICETULUS; DRUG EFFECT; EVALUATION; HAMSTER; MALE; MEMORY DISORDER; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PSYCHOLOGICAL ASPECT; RECOGNITION;

MUS;

ALGORITHMS; AMYLOID BETA-PEPTIDES; ANIMALS; AVOIDANCE LEARNING; CHO CELLS; CRICETINAE; CRICETULUS; FEAR; MALE; MEMORY; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; PEPTIDE FRAGMENTS; PHYSICAL CONDITIONING, ANIMAL; PROTEIN MULTIMERIZATION; RECOGNITION (PSYCHOLOGY);

EID: 84855373098     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029940     Document Type: Article

References (38)

1. Selkoe DJ, (2008) Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav Brain Res 192: 106-113.
2. Krafft GA, Klein WL, (2010) ADDLs and the signaling web that leads to Alzheimer's disease. Neuropharmacology 59: 230-242.
3. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, et al. (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30: 572-580.
4. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, et al. (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46: 860-866.
5. Van Dam D, D'Hooge R, Staufenbiel M, Van Ginneken C, Van Meir F, et al. (2003) Age-dependent cognitive decline in the APP23 model precedes amyloid deposition. European Journal of Neuroscience 17: 388-396.
6. 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 U S A 103: 5161-5166.
7. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, et al. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440: 352-357.
8. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, et al. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-842.
9. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, et al. (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8: 79-84.
10. Lauren J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM, (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457: 1128-1132.
11. Renner M, Lacor PN, Velasco PT, Xu J, Contractor A, et al. (2010) Deleterious effects of amyloid beta oligomers acting as an extracellular scaffold for mGluR5. Neuron 66: 739-754.
12. Cisse M, Halabisky B, Harris J, Devidze N, Dubal DB, et al. (2011) Reversing EphB2 depletion rescues cognitive functions in Alzheimer model. Nature 469: 47-52.
13. Balducci C, Beeg M, Stravalaci M, Bastone A, Sclip A, et al. (2010) Synthetic amyloid-β oligomers impair long-term memory independently of cellular prion protein. Proceedings of the National Academy of Sciences 107: 2295-2300.
14. Cisse M, Sanchez PE, Kim DH, Ho K, Yu GQ, et al. (2011) Ablation of cellular prion protein does not ameliorate abnormal neural network activity or cognitive dysfunction in the j20 line of human amyloid precursor protein transgenic mice. J Neurosci 31: 10427-10431.
15. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, et al. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416: 535-539.
16. Li S, Hong S, Shepardson NE, Walsh DM, Shankar GM, et al. (2009) Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 62: 788-801.
17. Paravastu AK, Qahwash I, Leapman RD, Meredith SC, Tycko R, (2009) Seeded growth of beta-amyloid fibrils from Alzheimer's brain-derived fibrils produces a distinct fibril structure. Proc Natl Acad Sci U S A 106: 7443-7448.
18. Reed MN, Hofmeister JJ, Jungbauer L, Welzel AT, Yu C, et al. (2009) Cognitive effects of cell-derived and synthetically derived Abeta oligomers. Neurobiol Aging doi:10.1016/j.neurobiolaging.2009.1011.1007.
19. Wang Q, Walsh DM, Rowan MJ, Selkoe DJ, Anwyl R, (2004) Block of long-term potentiation by naturally secreted and synthetic amyloid β-peptide in hippocampal slices is mediated via activation of the kinases c-jun n-terminal kinase, cyclin-dependent kinase 5, and p38 mitogen-activated protein kinase as well as metabotropic glutamate receptor type 5. The Journal of Neuroscience 24: 3370-3378.
20. Hamann S, Monarch ES, Goldstein FC, (2002) Impaired fear conditioning in Alzheimer's disease. Neuropsychologia 40: 1187-1195.
21. Hoefer M, Allison SC, Schauer GF, Neuhaus JM, Hall J, et al. (2008) Fear conditioning in frontotemporal lobar degeneration and Alzheimer's disease. Brain 131: 1646-1657.
22. Dineley KT, Xia X, Bui D, Sweatt JD, Zheng H, (2002) Accelerated plaque accumulation, associative learning deficits, and up-regulation of alpha 7 nicotinic receptor protein in transgenic mice co-expressing mutant human presenilin 1 and amyloid precursor proteins. J Biol Chem 277: 22768-22780.
23. Phillips RG, LeDoux JE, (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106: 274-285.
24. Cirrito JR, May PC, O'Dell MA, Taylor JW, Parsadanian M, et al. (2003) In vivo assessment of brain interstitial fluid with microdialysis reveals plaque-associated changes in amyloid-beta metabolism and half-life. J Neurosci 23: 8844-8853.
25. Kuperstein I, Broersen K, Benilova I, Rozenski J, Jonckheere W, et al. (2010) Neurotoxicity of Alzheimer's disease A[beta] peptides is induced by small changes in the A[beta]42 to A[beta]40 ratio. EMBO J 29: 3408-3420.
26. Granic I, Masman MF, Kees Mulder C, Nijholt IM, Naude PJ, et al. (2010) LPYFDa neutralizes amyloid-beta-induced memory impairment and toxicity. J Alzheimers Dis 19: 991-1005.
27. Freir DB, Fedriani R, Scully D, Smith IM, Selkoe DJ, et al. (2010) Abeta oligomers inhibit synapse remodelling necessary for memory consolidation. Neurobiol Aging.
28. O'Shea S, Smith I, McCabe O, Cronin M, Walsh D, et al. (2008) Intracerebroventricular Administration of Amyloid β-protein Oligomers Selectively Increases Dorsal Hippocampal Dialysate Glutamate Levels in the Awake Rat. Sensors 8: 7428-7437.
29. Roh JH, Qiu A, Seo SW, Soon HW, Kim JH, et al. (2011) Volume reduction in subcortical regions according to severity of Alzheimer's disease. J Neurol.
30. Puzzo D, Privitera L, Leznik E, Fa M, Staniszewski A, et al. (2008) Picomolar Amyloid-{beta} Positively Modulates Synaptic Plasticity and Memory in Hippocampus. J Neurosci 28: 14537-14545.
31. Podlisny MB, Ostaszewski BL, Squazzo SL, Koo EH, Rydell RE, et al. (1995) Aggregation of secreted amyloid beta-protein into sodium dodecyl sulfate-stable oligomers in cell culture. J Biol Chem 270: 9564-9570.
32. Walsh DM, Townsend M, Podlisny MB, Shankar GM, Fadeeva JV, et al. (2005) Certain Inhibitors of Synthetic Amyloid β-Peptide (Aβ) Fibrillogenesis Block Oligomerization of Natural Aβ and Thereby Rescue Long-Term Potentiation. The Journal of Neuroscience 25: 2455-2462.
33. Townsend M, Shankar GM, Mehta T, Walsh DM, Selkoe DJ, (2006) Effects of secreted oligomers of amyloid β-protein on hippocampal synaptic plasticity: a potent role for trimers. The Journal of Physiology 572: 477-492.
34. Poling A, Morgan-Paisley K, Panos JJ, Kim EM, O'Hare E, et al. (2008) Oligomers of the amyloid-beta protein disrupt working memory: confirmation with two behavioral procedures. Behav Brain Res 193: 230-234.
35. Townsend M, Cleary JP, Mehta T, Hofmeister J, Lesne S, et al. (2006) Orally available compound prevents deficits in memory caused by the Alzheimer amyloid-beta oligomers. Ann Neurol 60: 668-676.
36. O'Hare E, Scopes DI, Treherne JM, Norwood K, Spanswick D, et al. (2010) RS-0406 arrests amyloid-beta oligomer-induced behavioural deterioration in vivo. Behav Brain Res 210: 32-37.
37. Shankar GM, Welzel AT, McDonald JM, Selkoe DJ, Walsh DM, (2011) Isolation of Low-n Amyloid beta-Protein Oligomers from Cultured Cells, CSF, and Brain. Methods Mol Biol 670: 33-44.
38. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176.