Synthetic amyloid-β oligomers impair long-term memory independently of cellular prion protein

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

Volumn 107, Issue 5, 2010, Pages 2295-2300

  Balducci, Claudia ^a   Beeg, Marten ^a   Stravalaci, Matteo ^a   Bastone, Antonio ^a   Sclip, Alessandra ^a   Biasini, Emiliano ^a,b   Tapella, Laura ^a,b   Colombo, Laura ^a   Manzoni, Claudia ^a   Borsello, Tiziana ^a   Chiesa, Roberto ^a,b   Gobbi, Marco ^a   Salmona, Mario ^a   Forloni, Gianluigi ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b DULBECCO TELETHON INSTITUTE   (Italy)

Author keywords

Alzheimer; Neurotoxicity; Object recognition test; Protein aggregation; Surface plasmon resonance

Indexed keywords

AMYLOID BETA PROTEIN ANTIBODY; AMYLOID BETA PROTEIN[1-42]; PRION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; LONG TERM MEMORY; MALE; MEMORY DISORDER; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; COGNITION DISORDERS; HUMANS; INJECTIONS, INTRAVENTRICULAR; MALE; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONAL PLASTICITY; PEPTIDE FRAGMENTS; PRIONS; PROTEIN BINDING; PRPC PROTEINS; SURFACE PLASMON RESONANCE;

MUS;

EID: 76649093635     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0911829107     Document Type: Article

References (55)

1. Lue LF, et al. (1999) Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155:853-862.
2. McLean CA, et al. (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46:860-866.
3. Lambert MP, et al. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95:6448-6453.
4. 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.
5. 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.
6. Wang HW, et al. (2002) Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res 924: 133-140.
7. 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.
8. Mucke L, et al. (2000) High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation. J Neurosci 20:4050-4058.
9. Cleary JP, et al. (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8:79-84.
10. Lesné S, et al. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440:352-357.
11. Poling A, et al. (2008) Oligomers of the amyloid-beta protein disrupt working memory: Confirmation with two behavioral procedures. Behav Brain Res 193: 230-234.
12. Shankar GM, et al. (2007) Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 27:2866-2875.
13. 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.
14. De Felice FG, et al. (2009) Protection of synapses against Alzheimer's-linked toxins: Insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc Natl Acad Sci USA 106:1971-1976.
15. 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.
16. Snyder EM, et al. (2005) Regulation of NMDA receptor trafficking by amyloid-beta. Nat Neurosci 8:1051-1058.
17. 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.
18. Huang SM, et al. (2006) Neprilysin-sensitive synapse-associated amyloid-beta peptide oligomers impair neuronal plasticity and cognitive function. J Biol Chem 281: 17941-17951.
19. Mouri A, et al. (2007) Oral vaccination with a viral vector containing Abeta cDNA attenuates age-related Abeta accumulation and memory deficits without causing inflammation in a mouse Alzheimer model. FASEB J 21:2135-2148.
20. Scholtzova H, et al. (2008) Memantine leads to behavioral improvement and amyloid reduction in Alzheimer's-disease-model transgenic mice shown as by micromagnetic resonance imaging. J Neurosci Res 86:2784-2791.
21. Zhang L, et al. (2006) Learning-memory deficit with aging in APP transgenic mice of Alzheimer's disease and intervention by using tetrahydroxystilbene glucoside. Behav Brain Res 173:246-254.
22. Greene JD, Baddeley AD, Hodges JR (1996) Analysis of the episodic memory deficit in early Alzheimer's disease: Evidence from the doors and people test. Neuropsychologia 34:537-551.
23. Stine WB, Jr, Dahlgren KN, Krafft GA, LaDu MJ (2003) In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J Biol Chem 278:11612-11622.
24. Klyubin I, et al. (2005) Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat Med 11:556-561.
25. Squire LR, Wixted JT, Clark RE (2007) Recognition memory and the medial temporal lobe: A new perspective. Nat Rev Neurosci 8:872-883.
26. McGaugh JL (2000) Memory-a century of consolidation. Science 287:248-251.
27. Sara SJ (2000) Retrieval and reconsolidation: Toward a neurobiology of remembering. Learn Mem 7:73-84.
28. Cleary J, Hittner JM, Semotuk M, Mantyh P, O'Hare E (1995) Beta-amyloid(1-40) effects on behavior and memory. Brain Res 682:69-74.
29. Frautschy SA, et al. (2001) Phenolic anti-inflammatory antioxidant reversal of Abetainduced cognitive deficits and neuropathology. Neurobiol Aging 22:993-1005.
30. McDonald MP, Dahl EE, Overmier JB, Mantyh P, Cleary J (1994) Effects of an exogenous beta-amyloid peptide on retention for spatial learning. Behav Neural Biol 62:60-67.
31. O'Hare E, et al. (1999) Delayed behavioral effects following intrahippocampal injection of aggregated A beta (1-42). Brain Res 815:1-10.
32. Sweeney WA, Luedtke J, McDonald MP, Overmier JB (1997) Intrahippocampal injections of exogenous beta-amyloid induce postdelay errors in an eight-arm radial maze. Neurobiol Learn Mem 68:97-101.
33. Cooke SF, Bliss TV (2006) Plasticity in the human central nervous system. Brain 129: 1659-1673.
34. Collingridge GL, Isaac JT, Wang YT (2004) Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 5:952-962.
35. Lüscher C, Nicoll RA, Malenka RC, Muller D (2000) Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 3:545-550.
36. Hsieh H, et al. (2006) AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52:831-843.
37. Lacor PN, et al. (2004) Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J Neurosci 24:10191-10200.
38. Almeida CG, et al. (2005) Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses. Neurobiol Dis 20:187-198.
39. De Felice FG, et al. (2008) Alzheimer's disease-type neuronal tau hyperphosphorylation induced by A beta oligomers. Neurobiol Aging 29:1334-1347.
40. Irvine GB, El-Agnaf OM, Shankar GM, Walsh DM (2008) Protein aggregation in the brain: The molecular basis for Alzheimer's and Parkinson's diseases. Mol Med 14: 451-464.
41. Reed JM, Squire LR (1997) Impaired recognition memory in patients with lesions limited to the hippocampal formation. Behav Neurosci 111:667-675.
42. Zola SM, et al. (2000) Impaired recognition memory in monkeys after damage limited to the hippocampal region. J Neurosci 20:451-463.
43. Hammond RS, Tull LE, Stackman RW (2004) On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiol Learn Mem 82:26-34.
44. Kanaani J, Prusiner SB, Diacovo J, Baekkeskov S, Legname G (2005) Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hippocampal neurons in vitro. J Neurochem 95:1373-1386.
45. Santuccione A, Sytnyk V, Leshchyns'ka I, Schachner M (2005) Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J Cell Biol 169:341-354.
46. Parkin ET, et al. (2007) Cellular prion protein regulates beta-secretase cleavage of the Alzheimer's amyloid precursor protein. Proc Natl Acad Sci USA 104:11062-11067.
47. Sohma Y, Sasaki M, Hayashi Y, Kimura T, Kiso Y (2004) Novel and efficient synthesis of difficult sequence-containing peptides through O-N intramolecular acyl migration reaction of O-acyl isopeptides. Chem Commun (Camb) (1):124-125.
48. Coin I, Beyermann M, Bienert M (2007) Solid-phase peptide synthesis: From standard procedures to the synthesis of difficult sequences. Nat Protoc 2:3247-3256.
49. Taniguchi A, et al. (2009) "Click peptide": pH-triggered in situ production and aggregation of monomer Abeta1-42. ChemBioChem 10:710-715.
50. Taniguchi A, et al. (2007) 'O-Acyl isopeptide method' for peptide synthesis: Solvent effects in the synthesis of Abeta1-42 isopeptide using 'O-acyl isodipeptide unit'. J Pept Sci 13:868-874.
51. Bravman T, et al. (2006) Exploring "one-shot" kinetics and small molecule analysis using the ProteOn XPR36 array biosensor. Anal Biochem 358:281-288.
52. Kascsak RJ, et al. (1987) Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J Virol 61:3688-3693.
53. Langeveld JP, et al. (2006) Rapid and discriminatory diagnosis of scrapie and BSE in retro-pharyngeal lymph nodes of sheep. BMC Vet Res 2:19-32.
54. Chiesa R, Piccardo P, Ghetti B, Harris DA (1998) Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron 21:1339-1351.
55. Büeler H, et al. (1993) Mice devoid of PrP are resistant to scrapie. Cell 73:1339-1347.