Postsynaptic dysfunction is associated with spatial and object recognition memory loss in a natural model of Alzheimer's disease

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 34, 2012, Pages 13835-13840

  Ardiles, Álvaro O ^a   Tapia Rojas, Cheril C ^b   Mandal, Madhuchhanda ^c   Alexandre, Frédéric ^d   Kirkwood, Alfredo ^c   Inestrosa, Nibaldo C ^b   Palacios, Adrian G ^a  

^a UNIVERSIDAD DE VALPARAÍSO   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d INRIA   (France)

Author keywords

Aging; Hippocampus; Memory dysfunction; Neural plasticity; T maze

Indexed keywords

AMYLOID BETA PROTEIN; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DYSFUNCTION; CONTROLLED STUDY; DISEASE ASSOCIATION; NERVE CELL PLASTICITY; NEUROPATHOLOGY; NONHUMAN; OBJECT RECOGNITION; OCTODON DEGUS; POSTSYNAPTIC DYSFUNCTION; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RODENT; SPATIAL RECOGNITION; VISUAL MEMORY;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; MAZE LEARNING; MEMORY; MEMORY DISORDERS; MODELS, BIOLOGICAL; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; OCTODON; PATTERN RECOGNITION, PHYSIOLOGICAL; PHOSPHORYLATION; TAU PROTEINS; TIME FACTORS;

EID: 84865305651     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1201209109     Document Type: Article

References (58)

1. Selkoe DJ (2001) Alzheimer's disease: Genes, proteins, and therapy. Physiol Rev 81: 741-766.
2. Götz J, Ittner LM (2008) Animal models of Alzheimer's disease and frontotemporal dementia. Nat Rev Neurosci 9:532-544.
3. Philipson O, et al. (2010) Animal models of amyloid-beta-related pathologies in Alzheimer's disease. FEBS J 277:1389-1409.
4. Jacobsen JS, 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.
5. Selkoe DJ (2008) Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav Brain Res 192:106-113.
6. KleinWL, Krafft GA, Finch CE (2001) Targeting small Abeta oligomers: The solution to an Alzheimer's disease conundrum? Trends Neurosci 24:219-224.
7. Lesné S, et al. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440:352-357.
8. Shankar GM, et al. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14:837-842.
9. Oddo S, et al. (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: Intracellular Abeta and synaptic dysfunction. Neuron 39:409-421.
10. Duff K, Suleman F (2004) Transgenic mouse models of Alzheimer's disease: How useful have they been for therapeutic development? Brief Funct Genomics Proteomics 3:47-59.
11. Dodart JC, Mathis C, Bales KR, Paul SM (2002) Does my mouse have Alzheimer's disease? Genes Brain Behav 1:142-155.
12. Johnstone EM, Chaney MO, Norris FH, Pascual R, Little SP (1991) Conservation of the sequence of the Alzheimer's disease amyloid peptide in dog, polar bear and five other mammals by cross-species polymerase chain reaction analysis. Brain Res Mol Brain Res 10:299-305.
13. Sarasa M, Pesini P (2009) Natural non-transgenic animal models for research in Alzheimer's disease. Curr Alzheimer Res 6:171-178.
14. Braidy N, et al. (2011) Recent rodent models for Alzheimer's disease: Clinical implications and basic research. J Neural Transm 119:173-195.
15. Beck M, Bigl V, Rossner S (2003) Guinea pigs as a nontransgenic model for APP processing in vitro and in vivo. Neurochem Res 28:637-644.
16. Bons N, Rieger F, Prudhomme D, Fisher A, Krause KH (2006) Microcebus murinus: A useful primate model for human cerebral aging and Alzheimer's disease? Genes Brain Behav 5:120-130.
17. Inestrosa NC, et al. (2005) Human-like rodent amyloid-beta peptide determines Alzheimer pathology in aged wild-type Octodon degu. Neurobiol Aging 26:1023-1028.
18. van Groen T, et al. (2011) Age-related brain pathology in Octodon degu: Blood vessel, white matter and Alzheimer-like pathology. Neurobiol Aging 32:1651-1661.
19. Fitzjohn SM, et al. (2001) Age-related impairment of synaptic transmission but normal long-term potentiation in transgenic mice that overexpress the human APP695SWE mutant form of amyloid precursor protein. J Neurosci 21:4691-4698.
20. Hsia AY, et al. (1999) Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 96:3228-3233.
21. Wang H, Megill A, He K, Kirkwood A, Lee H-K (2012) Consequences of inhibiting amyloid precursor protein processing enzymes on synaptic function and plasticity. Neural Plast 2012:272374.
22. Chang EH, et al. (2006) AMPA receptor downscaling at the onset of Alzheimer's disease pathology in double-knockin mice. Proc Natl Acad Sci USA 103:3410-3415.
23. Ting JT, Kelley BG, Lambert TJ, Cook DG, Sullivan JM (2007) Amyloid precursor protein overexpression depresses excitatory transmission through both presynaptic and postsynaptic mechanisms. Proc Natl Acad Sci USA 104:353-358.
24. Middei S, et al. (2010) Learning discloses abnormal structural and functional plasticity at hippocampal synapses in the APP23 mouse model of Alzheimer's disease. Learn Mem 17:236-240.
25. Kayed R, et al. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300:486-489.
26. Arriagada PV, Growdon JH, Hedley-Whyte ET, Hyman BT (1992) Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42:631-639.
27. Otvos L, Jr., et al. (1994) Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404. J Neurosci Res 39:669-673.
28. Goedert M, Jakes R, Vanmechelen E (1995) Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205. Neurosci Lett 189: 167-169.
29. Palop JJ, Mucke L (2010) Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: From synapses toward neural networks. Nat Neurosci 13:812-818.
30. Larson ME, Lesné SE (2012) Soluble Aβ oligomer production and toxicity. J Neurochem 120(Suppl 1):125-139.
31. Cleary JP, et al. (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8:79-84.
32. De Felice FG, et al. (2007) Abeta oligomers induce neuronal oxidative stress through an N-methyl-D-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J Biol Chem 282:11590-11601.
33. Cenini G, et al. (2010) Generation of reactive oxygen species by beta amyloid fibrils and oligomers involves different intra/extracellular pathways. Amino Acids 38: 1101-1106.
34. Lacor PN, et al. (2007) Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 27:796-807.
35. Lacor PN, et al. (2004) Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J Neurosci 24:10191-10200.
36. Laurén 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.
37. Renner M, et al. (2010) Deleterious effects of amyloid beta oligomers acting as an extracellular scaffold for mGluR5. Neuron 66:739-754.
38. Walsh DM, et al. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535-539.
39. Townsend M, Shankar GM, Mehta T, Walsh DM, Selkoe DJ (2006) Effects of secreted oligomers of amyloid beta-protein on hippocampal synaptic plasticity: A potent role for trimers. J Physiol 572:477-492.
40. Cheng IH, et al. (2007) Accelerating amyloid-beta fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models. J Biol Chem 282: 23818-23828.
41. Reed MN, et al. (2011) Cognitive effects of cell-derived and synthetically derived Abeta oligomers. Neurobiol Aging 32:1784-1794.
42. Bernstein SL, et al. (2009) Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat Chem 1:326-331.
43. Pavía J, de Ceballos ML, Sanchez de la Cuesta F (1998) Alzheimer's disease: Relationship between muscarinic cholinergic receptors, beta-amyloid and tau proteins. Fundam Clin Pharmacol 12:473-481.
44. Oddo S, et al. (2006) Reduction of soluble Abeta and tau, but not soluble Abeta alone, ameliorates cognitive decline in transgenic mice with plaques and tangles. J Biol Chem 281:39413-39423.
45. Rank KB, et al. (2002) Direct interaction of soluble human recombinant tau protein with Abeta 1-42 results in tau aggregation and hyperphosphorylation by tau protein kinase II. FEBS Lett 514:263-268.
46. Zempel H, Thies E, Mandelkow E, Mandelkow EM (2010) Abeta oligomers cause localized Ca(2+) elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J Neurosci 30:11938-11950.
47. Decker H, Lo KY, Unger SM, Ferreira ST, Silverman MA (2010) Amyloid-beta peptide oligomers disrupt axonal transport through an NMDA receptor-dependent mechanism that is mediated by glycogen synthase kinase 3beta in primary cultured hippocampal neurons. J Neurosci 30:9166-9171.
48. Shipton OA, et al. (2011) Tau protein is required for amyloid beta-induced impairment of hippocampal long-term potentiation. J Neurosci 31:1688-1692.
49. Gu Z, Liu W, Yan Z (2009) Beta-amyloid impairs AMPA receptor trafficking and function by reducing Ca2+/calmodulin-dependent protein kinase II synaptic distribution. J Biol Chem 284:10639-10649.
50. Almeida CG, et al. (2005) Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses. Neurobiol Dis 20:187-198.
51. Kamenetz F, et al. (2003) APP processing and synaptic function. Neuron 37:925-937.
52. Lazarov O, Lee M, Peterson DA, Sisodia SS (2002) Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J Neurosci 22:9785-9793.
53. Zhang C, et al. (2009) Presenilins are essential for regulating neurotransmitter release. Nature 460:632-636.
54. Boric K, Muñoz P, Gallagher M, Kirkwood A (2008) Potential adaptive function for altered long-term potentiation mechanisms in aging hippocampus. J Neurosci 28: 8034-8039.
55. Lee HK, Min SS, Gallagher M, Kirkwood A (2005) NMDA receptor-independent long-term depression correlates with successful aging in rats. Nat Neurosci 8: 1657-1659.
56. Rosenzweig ES, Barnes CA (2003) Impact of aging on hippocampal function: Plasticity, network dynamics, and cognition. Prog Neurobiol 69:143-179.
57. Willig F, et al. (1987) Short-term memory, exploration and locomotor activity in aged rats. Neurobiol Aging 8:393-402.
58. Lukaszewska I, Radulska A (1994) Object recognition is not impaired in old rats. Acta Neurobiol Exp (Warsz) 54:143-150.