Protofibrillar intermediates of amyloid β-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons

Journal of Neuroscience

Volumn 19, Issue 20, 1999, Pages 8876-8884

  Hartley, Dean M ^a,b   Walsh, Dominic M ^a   Ye, Chianping P ^a   Diehl, Thekla ^a   Vasquez, Sara ^a   Vassilev, Peter M ^a   Teplow, David B ^a   Selkoe, Dennis J ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD INSTITUTES OF MEDICINE   (United States)

Author keywords

Alzheimer; Amyloid protein; Electrophysiology; Fibrillogenesis; Neurodegeneration; Neurotoxicity

Indexed keywords

AMYLOID BETA PROTEIN;

ACTION POTENTIAL; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; EXCITATORY POSTSYNAPTIC POTENTIAL; MEMBRANE DEPOLARIZATION; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RAT; SENILE PLAQUE;

EID: 0033570337     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-20-08876.1999     Document Type: Article

References (47)

1. Aksenova MV, Aksenov MY, Buttcrficld DA, Carncy JM (1996) α-1-antichymotrypsin interaction with Aβ (1-40) inhibits fibril formation hut does not affect the peptide toxicity. Neurosci Lett 211:45-48.
2. Anderton BH, Callahan L, Coleman P, Davies P, Flood D, Jicha GA, Ohm T, Weaver C (1998) Dendritic changes in Alzheimer's disease and factors that may underlie these changes. Prog Neurobiol 55:595-609.
3. Arispe N, Pollard HB, Rojas E (1993) Giant multilevel cation channels formed by Alzheimer disease amyloid β-protein [Aβ P-(1-40)] in hilayer membranes. Proc Natl Acad Sei USA 90:10573-10577.
4. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TV, Hyman BT, Younkin SG, Hsiao KK (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2:271-276.
5. Cummings JL, Vinters H V, Cole GM, Khachaturian ZS (1998) Alzheimcr's disease: etiologies, pathophysiology, cognitive reserve, and treatment opportunities. Neurology 51:S2-S17.
6. Dickson DW (1997) The pathogenesis of senile plaques. J Neuropathol Exp Neurol 56:321-339.
7. Esiri M, Hyman B, Beyreuther K, Masters C (1997) Aging and dementia. In: Greenfleld's neuropathology, Vol 2 (Graham D, Lantos P, eds), pp 153-233. London: Arnold.
8. Estus S, Tucker HM, van Rooyen C, Wright S, Brigham EF, Wogulis M, Rydel RE (1997) Aggregated amyloid-β protein induces cortical neu ronal apoptosis and concomitant apoptotic pattern of gene induction. J Neurosci 17:7736-7745.
9. Giulian D, Haverkarap LJ, Yu JH, Karshin W, Tom D, Li J, Kirkpatrick J, Kuo LM, Roher AE (1996) Specific domains of β-amyloid from Alzheimer plaque elicit neuron killing in human microglia. J Neurosci 16:6021-6037.
10. Gomez-Isla T, Price JL, McKeel Jr DW, Morris JC, Growdon JH, Hyman BT (1996) Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci 16:4491-4500.
11. Gravina SA, Ho L, Eckman CB, Long KE, Otvos Jr L, Younkin LH, Suzuki N, Younkin SG (1995) Amyloid β protein (Aβ) in Alzheimer's disease brain. Biochemical and immunocytochemical analysis with antibodies specific for forms ending at Aβ 40 or Aβ 42(43). J Biol Chem 270:7013-7016.
12. Harper JD, Lansbury Jr PT (1997) Models of amyloid seeding in Alzheimer's disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu Rev Biochem 66:385-407.
13. Harper JD, Wong SS, Lieber CM, Lansbury Jr PT (1997a) Observation of metastable Aβ amyloid protofibrils by atomic force microscopy. Chem Biol 4:119-125.
14. Harper JD, Lieber CM, Lansbury Jr PT (1997b) Atomic force microscopic imaging of seeded fibril formation and fibril branching by the Alzheimer's disease amyloid-β protein. Chem Biol 4:951-959.
15. 2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J Neurosci 13:1993-2000.
16. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O'Carnpo K, Hardy J, Prada CM, Eckman C, Younkin S, Hsiao K, Duff K (1998) Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4:97-100.
17. Hsia A, Masliah E, McConlogue L, Yu G, Tatsuno g, Hu K, Kholodenko D, Malenka R, Nicoll R, Mucke L (1999) Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sei USA 96:3228-3233.
18. Hsiao K, Chapman P, Nilsen S, Ekman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
19. Johnson-Wood K, Lee M, Motter R, Hu K, Gordon G, Barbour R, Khan K, Gordon M, Tan H, Games D, Lieberburg I, Schenk D, Seubert P, McConlogue L (1997) Amyloid precursor protein processing and Aβ42 deposition in a transgenic mouse model of Alzheimer disease. Proc Natl Acad Sei USA 94:1550-1555.
20. Kawahara M, Arispe N, Kuroda Y, Rojas E (1997) Alzheimer's disease amyloid β-protein forms Zn(2+)-sensitive, cation-selective channels across excised membrane patches from hypothalamic neurons. Biophys J 73:67-75.
21. Klunk WE, PettegrewJW, Abraham DJ (1989) Quantitative evaluation of congo red binding to amyloid-like proteins with a β-pleated sheet conformation. J Histochem Cytochem 37:1273-1281.
22. Klunk WE, Jacob RF, Mason RP (1999) Quantifying amyloid β-peptide (Aβ) aggregation using the Congo red-Aβ (CR-aβ) spectrophotometric assay. Anal Biochem 266:66-76.
23. Kuo Y-M, Emmerling MR, Vigo-Pelfrey C, Kasunic TC, Kirkpatrick JB, Murdoch GH, Ball MJ, Roher AE (1996) Water-soluble Aβ (N-40, N-42) oligomers in normal and Alzheimer disease brains. J Biol Chem 271:4077-4081.
24. 1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sei USA 95:6448-6453.
25. Lemere CA, Blustzjan JK, Yamaguchi H, Wisniewski T, Saido TC, Selkoe DJ (1996) Sequence of deposition of heterogeneous amyloid β-peptides and Apo E in Down syndrome: implications for initial events in amyloid plaque formation. Neurobiol Dis 3:16-32.
26. Lorenzo A, Yankner B (1994) β-amyloid neurotoxicity requires fibril formation and is inhibited by Congo red. Proc Natl Acad Sei USA 91:12243-12247.
27. 2+ homeostasis and cell death. J Neurosci 15:6239-6249.
28. Mattson MP, Cheng B, Davis D, Bryant K, Liebcrburg I, Rydel RE (1992) β-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 12:379-389.
29. Mattson MP, TomaselliKJ, Rydel RE (1993) Calcium-destabilizing and neurodegenerative effects of aggregated β-amyloid peptide are attenuated by basic FGF. Brain Res 621:35-49.
30. Morris JC, Storandt M, McKeel Jr DW, Rubin EH, Price JL, Grant EA, Berg L (1996) Cerebral amyloid deposition and diffuse plaques in "normal" aging: evidence for presymptomatic and very mild Alzheimer's disease. Neurology 46:707-719.
31. Oda T, Wals P, Osterburg HH, Johnson SA, Pasinetti GM, Morgan TE, Rozovsky I, Stine WB, Snyder SW, Holzman TF, Krafft GA, Finch CE (1995) Clusterin (apoJ) alters the aggregation of amyloid β-peptide (Aβ 1-42) and forms slowly sedimenting Aβ complexes that cause oxidative stress. Exp Neurol 136:22-31.
32. Pike CJ, Walencewicz AJ, Glabe CG, Cotman CW (1991) In vitro aging of β-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res 563:311-314.
33. Pike CJ, Burdick D, Walencewicz AJ, Glabe CG, Cotman CW (1993) Neurodegeneration induced by β-amyloid peptides in vitro: the role of peptide assembly state. J Neurosci 13:1676-1687.
34. Pitschke M, Prior R, Haupt M, Riesner D (1998) Detection of single amyloid B-protein aggregates in the cerebrospinal fluid of Alzheimer's patients by fluorescence correlation spectroscopy. Nat Med 4:832-834.
35. Podlisny MB, Ostaszewski BL, Squazzo SL, Koo EH, Rydel RE, Teplow DB, Selkoe DJ (1995) Aggregation of secreted amyloid β-protein into SDS-stable oligomers in cell culture. J Biol Chem 270:9564-9570.
36. Podlisny MB, Walsh DM, Amarante P, Ostoszewski BL, Stimson ER, Maggio JE, Teplow DB, Selkoe DJ (1998) Oligomerization of endogenous and synthetic amyloid β-protein at nanomolar levels in cell culture and stabilization of monomer by Congo red. Biochemistry 37:3602-3611.
37. Roher AE, Chancy MO, Kuo Y-M, Webster SD, Stine WB, Haverkamp LJ, Woods AS, Cotter RJ, Tuohy JM, Knifft GA, Bonnell BS, Emmerling MR (1996) Morphology and toxicity of Aβ-(1-42) dimer derived from neuritic and vascular amyloid deposits of Alzheimer's disease. J Biol Chem 271:20631-20635.
38. Seilhcimer B, Bohrmann B, Bondolfl L, Müller F, Stüber D, Döbeli H (1997) The toxicity of the Alzheimer's β-amyloid peptide correlates with a distinct fiber morphology. J Struct Biol 119:59-71.
39. Sze CI, Troncoso JC, Kawas C, Mouton P, Price DL, Martin LJ (1997) Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimcr disease. J Ncuropathol Exp Neurol 56:933-944.
40. Teplow DB (1998) Structural and kinetic fea:ures of amyloid β-protein fibrillogenesis. Amyloid 5:121-42.
41. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30:572-580.
42. Walsh DM, Hartley DM, Kusumoto Y, Fezcui Y, Condron MM, Lomakin A, Benedek GB, Selkoe, DJ, Teplow DB (1999) Amyloid β-protein fibrillogenesis: structure and biological activity of protofibrillar intermediates. J Biol Chem 274:25945-25952.
43. Walsh DM, Lomakin A, Benedek GB, Maggio JE, Condron MM, Teplow DB (1997) Amyloid β-protein fibrillogenesis: detection of a protofibrillar intermediate. J Biol Chem 272:22364-22374.
44. Wood SJ, Maleeff B, Hart T, Wetzel R (1996) Physical, morphological and functional differences between pH 5.8 and 7.4 aggregates of the Alzheimer's amyloid peptide Aβ. J Mol Biol 256:870-877.
45. Wu J, Anwyl R, Rowan MJ (1995) β-Amyloid selectively augments NMDA receptor-mediated synaptic transm ssion in rat hippocampus. NeuroReport 6:2409-2413.
46. Xia W, Zhang J, Kholodenko D. Citron, M, Podlisny MB, Teplow DB, Haas C, Seubert P, Koo EH, Selkoe DJ (1997) Enhanced production and oligomerization of the 42-residue amyloid β-protein by Chinese hamster ovary cells stably expressing mutant presenilins. J Biol Chem 272:7977-7982.
47. Ye C, Ho-Pao CL, Kanazirska M, Quinn S. Rogers K, Seidman CE, Seidman JG, Brown EM, Vassilev PM (1997) Amyloid-β proteins activate Ca(2+)-permeable channels through calcium-sensing receptors. J Neurosci Res 47:547-554.