Synaptic targeting by Alzheimer's-related amyloid β oligomers

Journal of Neuroscience

Volumn 24, Issue 45, 2004, Pages 10191-10200

  Lacor, Pascale N ^a   Buniel, Maria C ^a   Chang, Lei ^a   Fernandez, Sara J ^a   Gong, Yuesong ^a   Viola, Kirsten L ^a   Lambert, Mary P ^a   Velasco, Pauline T ^a   Bigio, Eileen H ^b   Finch, Caleb E ^c   Krafft, Grant A ^d   Klein, William L ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d Acumen Pharmaceuticals   (United States)

Author keywords

ADDLs; Amyloid; Arc; Dendritic spines; Immediate early gene; Synapse

Indexed keywords

AMYLOID BETA PROTEIN; ANTIBODY; OLIGOMER;

ALZHEIMER DISEASE; AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DEMENTIA; FRACTIONATION; GENE OVEREXPRESSION; HIPPOCAMPUS; IMAGE ANALYSIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; LONG TERM POTENTIATION; MOUSE; NERVE CELL; NERVE CELL NECROSIS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; RAT;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; BINDING SITES; CEREBRAL CORTEX; CEREBROSPINAL FLUID PROTEINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOSKELETAL PROTEINS; FEMALE; HIPPOCAMPUS; HUMANS; MALE; NERVE TISSUE PROTEINS; NEURONS; PEPTIDE FRAGMENTS; PROTEIN BINDING; RATS; SYNAPSES; TISSUE EXTRACTS;

EID: 20844458090     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3432-04.2004     Document Type: Article

References (64)

1. Allison DW, Chervin AS, Gelfand VI, Craig AM (2000) Postsynaptic scaffolds of excitatory and inhibitory synapses in hippocampal neurons: maintenance of core components independent of actin filaments and microtubules. J Neurosci 20:4545-4554.
2. Butterfield DA (2003) Amyloid beta-peptide [1-42]-associated free radical-induced oxidative stress and neurodegeneration in Alzheimer's disease brain: mechanisms and consequences. Curr Med Chem 10:2651-2659.
3. Buttini M, Yu GQ, Shockley K, Huang Y, Jones B, Masliah E, Mallory M, Yeo T, Longo FM, Mucke L (2002) Modulation of Alzheimer-like synaptic and cholinergic deficits in transgenic mice by human apolipoprotein E depends on isoform, aging, and overexpression of amyloid β peptides but not on plaque formation. J Neurosci 22:10539-10548.
4. Caughey B, Lansbury Jr PT (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu Rev Neurosci 26:267-298.
5. Chang L, Bakhos L, Wang Z, Venton DL, Klein WL (2003) Femtomole immunodetection of synthetic and endogenous amyloid-β oligomers and its application to Alzheimer's disease drug candidate screening. J Mol Neurosci 20:305-313.
6. Chin J, Palop JJ, Yu GQ, Kojima N, Masliah E, Mucke L (2004) Fyn kinase modulates synaptotoxicity, but not aberrant sprouting, in human amyloid precursor protein transgenic mice. J Neurosci 24:4692-4697.
7. Chromy BA, Nowak RJ, Lambert MP, Viola KL, Chang L, Velasco PT, Jones BW, Fernandez SJ, Lacor PN, Horowitz P, Finch CE, Krafft GA, Klein WL (2003) Self-assembly of Abeta(1-42) into globular neurotoxins. Biochemistry 42:12749-12760.
8. Cirelli C, Tononi G (2000) Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system. J Neurosci 20:9187-9194.
9. Coyle JT (1987) Alzheimer's disease. In: Encyclopedia of neuroscience (Adelman G, ed), pp 29-31. Stuttgart: Birkhäuser.
10. Crick F (1982) Do dendritic spines twitch? Trends Neurosci 5:44-46.
11. Dickey CA, Loring JF, Montgomery J, Gordon MN, Eastman PS, Morgan D (2003) Selectively reduced expression of synaptic plasticity-related genes in amyloid precursor protein plus presenilin-1 transgenic mice. J Neurosci 23:5219-5226.
12. Dodart JC, Bales KR, Cannon KS, Greene SJ, DeMattos RB, Mathis C, DeLong CA, Wu S, Wu X, Holtzman DM, Paul SM (2002) Immunization reverses memory deficits without reducing brain Abeta burden in Alzheimer's disease model. Nat Neurosci 5:452-457.
13. Drake J, Link CD, Butterfield DA (2003) Oxidative stress precedes fibrillar deposition of Alzheimer's disease amyloid beta-peptide (1-42) in a transgenic Caenorhabditis elegans model. Neurobiol Aging 24:415-420.
14. Fiala JC, Spacek J, Harris KM (2002) Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res Brain Res Rev 39:29-54.
15. Fong DK, Rao A, Crump FT, Craig AM (2002) Rapid synaptic remodeling by protein kinase C: reciprocal translocation of NMDA receptors and calcium/calmodulin-dependent kinase II. J Neurosci 22:2153-2164.
16. Freeman WM, Brebner K, Lynch WJ, Patel KM, Robertson DJ, Roberts DC, Vrana KE (2002) Changes in rat frontal cortex gene expression following chronic cocaine. Brain Res Mol Brain Res 104:11-20.
17. Fujimoto T, Tanaka H, Kumamaru E, Okamura K, Miki N (2004) Arc interacts with microtubules/microtubule-associated protein 2 and attenuates microtubule-associated protein 2 immunoreactivity in the dendrites. J Neurosci Res 76:51-63.
18. Gibson WW, Eckert GP, Igbavboa U, Muller WE (2003) Amyloid beta-protein interactions with membranes and cholesterol: causes or casualties of Alzheimer's disease. Biochim Biophys Acta 1610:281-290.
19. Gong Y, Chang L, Viola KL, Lacor PN, Lambert MP, Finch CE, Krafft GA, Klein WL (2003) Alzheimer's disease-affected brain: presence of oligomeric Aβ ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc Natl Acad Sci USA 100:10417-10422.
20. Gouras GK, Tsai J, Naslund J, Vincent B, Edgar M, Checler F, Greenfield JP, Haroutunian V, Buxbaum JD, Xu H, Greengard P, Relkin NR (2000) Intraneuronal Abeta42 accumulation in human brain. Am J Pathol 156:15-20.
21. Gurowski JF (2002) Insights into immediate-early gene function in hippocampal memory consolidation using antisense oligonucleotide and fluorescent imaging approaches. Hippocampus 12:86-104.
22. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF, Barnes CA (2000) Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20:3993-4001.
23. Hainfellner JA, Liberski PP, Guiroy DC, Cervenakova L, Brown P, Gajdusek DC, Budka H (1997) Pathology and immunocytochemistry of a kuru brain. Brain Pathol 7:547-553.
24. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356.
25. Hardy JA, Higgins GA (1992) Alzheimer's disease: the amyloid cascade hypothesis. Science 256:184-185.
26. Hock C, Konietzko U, Streffer JR, Tracy J, Signorell A, Muller-Tillmanns B, Lemke U, Henke K, Moritz E, Garcia E, Wollmer MA, Umbricht D, de Quervain DJ, Hofmann M, Maddalena A, Papassotiropoulos A, Nitsch RM (2003) Antibodies against beta-amyloid slow cognitive decline in Alzheimer's disease. Neuron 38:547-554.
27. Hsia AY, Masliah E, McConlogue L, Yu GQ, Tatsuno G, Hu K, Kholodenko D, Malenka RC, Nicoll RA, Mucke L (1999) Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 96:3228-3233.
28. 2+/calmodulin-dependent protein kinase II within post-synaptic dendritic spines of cultured hippocampal neurons. J Biol Chem 275:27165-27171.
29. Katzman R, Terry R, DeTeresa R, Brown T, Davies P, Fuld P, Renbing X, Peck A (1988) Clinical, pathological, and neurochemical changes in dementia: a subgroup with preserved mental status and numerous neocortical plaques. Ann Neurol 23:138-144.
30. Kaufmann WE, Moser HW (2000) Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 10:981-991.
31. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogen esis. Science 300:486-489.
32. Kelly MP, Deadwyler SA (2003) Experience-dependent regulation of the immediate-early gene arc differs across brain regions. J Neurosci 23:6443-6451.
33. Kirkitadze MD, Bitan G, Teplow DB (2002) Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies. J Neurosci Res 69:567-577.
34. Klein WL (2002) Aβ toxicity in Alzheimer's disease: globular oligomers (ADDLs) as new vaccine and drug targets. Neurochem Int 41:345-352.
35. Klein WL (2004) Cytotoxic intermediates in the fibrillation pathway: Aβ oligomers in Alzheimer's disease as a case study. In: Protein misfolding, aggregation and conformational diseases (Uversky V, ed). New York: Kluwer Academic/Plenum, in press.
36. Klein WL, Krafft GA, Finch CE (2001) Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci 24:219-224.
37. Kotilinek LA, Bacskai B, Westerman M, Kawarabayashi T, Younkin L, Hyman BT, Younkin S, Ashe KH (2002) Reversible memory loss in a mouse transgenic model of Alzheimer's disease. J Neurosci 22:6331-6335.
38. Kovacs GG, Head MW, Hegyi I, Bunn TJ, Flicker H, Hainfellner JA, McCardle L, Laszlo L, Jarius C, Ironside JW, Budka H (2002) Immunohistochemistry for the prion protein: comparison of different monoclonal antibodies in human prion disease subtypes. Brain Pathol 12:1-11.
39. Kuo YM, Emmerling MR, Vigo-Pelfrey C, Kasunic TC, Kirkpatrick JB, Murdoch GH, Ball MJ, Roher AE (1996) Water-soluble Abeta (N-40, N-42) oligomers in normal and Alzheimer disease brains. J Biol Chem 271:4077-4081.
40. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95:6448-6453.
41. Lambert MP, Viola KL, Chromy BA, Chang L, Morgan TE, Yu J, Venton DL, Krafft GA, Finch CE, Klein WL (2001) Vaccination with soluble Abeta oligomers generates toxicity-neutralizing antibodies. J Neurochem 79:595-605.
42. Link W, Konietzko U, Kauselmann G, Krug M, Schwanke B, Frey U, Kuhl D (1995) Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci USA 92:5734-5738.
43. Lyford GL, Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14:433-445.
44. Mattson MP (2004) Pathways towards and away from Alzheimer's disease. Nature 430:631-639.
45. McLaurin J, Chakrabartty A (1996) Membrane disruption by Alzheimer beta-amyloid peptides mediated through specific binding to either phospholipids or gangliosides. Implications for neurotoxicity. J Biol Chem 271:26482-26489.
46. Moga DE, Calhoun ME, Chowdhury A, Worley P, Morrison JH, Shapiro ML (2004) Activity-regulated cytoskeletal-associated protein is localized to recently activated excitatory synapses. Neuroscience 125:7-11.
47. Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, Tatsuno G, Hu K, Kholodenko D, Johnson-Wood K, McConlogue L (2000) High-level neuronal expression of aβ 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 20:4050-4058.
48. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39:409-421.
49. Rao A, Craig AM (2000) Signaling between the actin cytoskeleton and the postsynaptic density of dendritic spines. Hippocampus 10:527-541.
50. Rao A, Kim E, Sheng M, Craig AM (1998) Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J Neurosci 18:1217-1229.
51. Schenk D (2002) Amyloid-beta immunotherapy for Alzheimer's disease: the end of the beginning. Nat Rev Neurosci 3:824-828.
52. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298:789-791.
53. Sheng M, Pak DT (1999) Glutamate receptor anchoring proteins and the molecular organization of excitatory synapses. Ann NY Acad Sci 868:483-493.
54. Steward O, Worley PF (2001) A cellular mechanism for targeting newly synthesized mRNAs to synaptic sites on dendrites. Proc Natl Acad Sci USA 98:7062-7068.
55. Sweatt JD (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76:1-10.
56. Tong L, Thornton PL, Balazs R, Cotman CW (2001) Beta-amyloid-(1-42) impairs activity-dependent cAMP-response element-binding protein signaling in neurons at concentrations in which cell survival is not compromised. J Biol Chem 276:17301-17306.
57. Van Dam D, D'Hooge R, Staufenbiel M, Van Ginneken C, Van Meir F, De Deyn PP (2003) Age-dependent cognitive decline in the APP23 model precedes amyloid deposition. Eur J Neurosci 17:388-396.
58. Verdier Y, Zarandi M, Penke B (2004) Amyloid beta-peptide interactions with neuronal and glial cell plasma membrane: binding sites and implications for Alzheimer's disease. J Pept Sci 10:229-248.
59. Walsh DM, Selkoe DJ (2004) Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44:181-193.
60. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535-539.
61. Wang HW, Pasternak JF, Kuo H, Ristic H, Lambert MP, Chromy B, Viola KL, Klein WL, Stine WB, Krafft GA, Trommer BL (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.
62. 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. J Neurosci 24:3370-3378.
63. Weiner HL, Selkoe DJ (2002) Inflammation and therapeutic vaccination in CNS diseases. Nature 420:879-884.
64. Yuste R, Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24:1071-1089.