Effects of secreted oligomers of amyloid β-protein on hippocampal synaptic plasticity: A potent role for trimers

Journal of Physiology

Volumn 572, Issue 2, 2006, Pages 477-492

  Townsend, Matthew ^a   Shankar, Ganesh M ^a   Mehta, Tapan ^a   Walsh, Dominic M ^b   Selkoe, Dennis J ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; OLIGOMER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENATURATION; FEMALE; GEL PERMEATION CHROMATOGRAPHY; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; SENSITIVITY ANALYSIS; WILD TYPE; ADULT; CYTOPLASM VESICLE; IN VITRO STUDY; IN VIVO STUDY; JUVENILE ANIMAL; LONG TERM POTENTIATION; METABOLIC INHIBITION; PRESYNAPTIC VESICLE; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DENATURATION; SIZE EXCLUSION CHROMATOGRAPHY; WILD TYPE MOUSE;

AMYLOID BETA-PROTEIN; ANIMALS; BLOTTING, WESTERN; CHROMATOGRAPHY, GEL; CHROMOSOME PAIRING; ELECTROPHYSIOLOGY; FEMALE; HEAT; HIPPOCAMPUS; IMMUNOPRECIPITATION; LONG-TERM POTENTIATION; MALE; MICE; NEURONAL PLASTICITY; POLYMERS; PROTEIN DENATURATION;

EID: 33645505550     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2005.103754     Document Type: Article

References (56)

1. Barghorn S, Nimmrich V, Striebinger A, Krantz C, Keller P, Janson B, Bahr M, Schmidt M, Bitner RS, Harlan J, Barlow E, Ebert U & Hillen H (2005). Globular amyloid beta-peptide oligomer -a homogenous and stable neuropathological protein in Alzheimer's disease. J Neurochem 95, 834-847.
2. Billings LM, Oddo S, Green KN, McGaugh JL & LaFerla FM (2005). Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45, 675-688.
3. Chang L, Bakhos L, Wang Z, Venton DL & Klein WL (2003). Femtomole immunodetection of synthetic and endogenous amyloid-beta oligomers and its application to Alzheimer's disease drug candidate screening. J Mol Neurosci 20, 305-313.
4. Chen QS, Wei WZ, Shimahara T & Xie CW (2002). Alzheimer amyloid beta-peptide inhibits the late phase of long-term potentiation through calcineurin-dependent mechanisms in the hippocampal dentate gyrus. Neurobiol Learn Mem 77, 354-371.
5. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ & Ashe KH (2005). Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8, 79-84.
6. Collin C, Miyaguchi K & Segal M (1997). Dendritic spine density and LTP induction in cultured hippocampal slices. J Neurophysiol 77, 1614-1623.
7. Davies CA, Mann DM, Sumpter PQ & Yates PO (1987). A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer's disease. J Neurol Sci 78, 151-164.
8. Deane R, Du Yan S, Submamaryan RK, LaRue B, Jovanovic S, Hogg E, Welch D, Manness L & Lin C, Yu J, Zhu H, Ghiso J, Frangione B, Stern A, Schmidt AM, Armstrong DL, Arnold B, Liliensiek B, Nawroth P, Hofman F, Kindy M, Stern D & Zlokovic B (2003). RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med 9, 907-913.
9. DeMattos RB, Bales KR, Cummins DJ, Dodart JC, Paul SM & Holtzman DM (2001). Peripheral anti-A beta antibody alters CNS and plasma A beta clearance and decreases brain A beta burden in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 98, 8850-8855.
10. Dodart JC, Bales KR, Gannon 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.
11. Ehlers MD (2003). Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6, 231-242.
12. Glenner GG & Wong CW (1984). Alzheimer's disease: Initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120, 885-890.
13. Gotz J, Chen F, Van Dorpe J & Nitsch RM (2001). Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils. Science 293, 1491-1495.
14. Hardy J & Selkoe DJ (2002). The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356.
15. 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 U S A 96, 3228-3233.
16. Kang HJ & Schuman EM (1995). Neurotrophin-induced modulation of synaptic transmission in the adult hippocampus. J Physiol Paris 89, 11-22.
17. 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 pathogenesis. Science 300, 486-489.
18. Kim JH, Anwyl R, Suh YH, Djamgoz MB & Rowan MJ (2001). Use-dependent effects of amyloidogenic fragments of (beta)-amyloid precursor protein on synaptic plasticity in rat hippocampus in vivo. J Neurosci 21, 1327-1333.
19. Kirschner DA, Abraham C & Selkoe DJ (1986). X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-beta conformation. Proc Natl Acad Sci U S A 83, 503-507.
20. Klyubin I, Walsh DM, Lemere CA, Cullen WK, Shankar GM, Betts V, Spooner ET, Jiang L, Anwyl R, Selkoe DJ & Rowan MJ (2005). Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat Med 11, 556-561.
21. Koistinaho M, Ort M, Cimadevilla JM, Vondrous R, Cordell B, Koistinaho J, Bures J & Higgins LS (2001). Specific spatial learning deficits become severe with age in beta-amyloid precursor protein transgenic mice that harbor diffuse beta-amyloid deposits but do not form plaques. Proc Natl Acad Sci U S A 98, 14675-14680.
22. Kokubo H, Kayed R, Glabe CG & Yamaguchi H (2005). Soluble Abeta oligomers ultrastructurally localize to cell processes and might be related to synaptic dysfunction in Alzheimer's disease brain. Brain Res 1031, 222-228.
23. Kossel AH, Williams CV, Schweizer M & Kater SB (1997). Afferent innervation influences the development of dendritic branches and spines via both activity-dependent and non-activity-dependent mechanisms. J Neurosci 17, 6314-6324.
24. 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 U S A 95, 6448-6453.
25. Lavados M, Farias G, Rothhammer F, Guillon M, Mujica MC, Maccioni C & Maccioni RB (2005). ApoE alleles and tau markers in patients with different levels of cognitive impairment. Arch Med Res 36, 474-479.
26. Lewis J, Dickson DW, Lin WL, Chisholm L, Corral A, Jones G, Yen SH, Sahara N, Skipper L, Yager D, Eckman C, Hardy J, Hutton M & McGowan E (2001). Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293, 1487-1491.
27. Lu B & Chow A (1999). Neurotrophins and hippocampal synaptic transmission and plasticity. J Neurosci Res 58, 76-87.
28. Lu W, Man H, Ju W, Trimble WS, MacDonald JF & Wang YT (2001). Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29, 243-254.
29. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L, Beach T, Kurth JH, Rydel RE & Rogers J (1999). Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155, 853-862.
30. Lynch MA (2004). Long-term potentiation and memory. Physiol Rev 84, 87-136.
31. Masliah E, Mallory M, Alford M, DeTeresa R, Hansen LA, McKeel DW Jr & Morris JC (2001). Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease. Neurology 56, 127-129.
32. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, Bush AI & Masters CL (1999). Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46, 860-866.
33. Mehta PD, Pirttila T, Mehta SP, Sersen EA, Aisen PS & Wisniewski HM (2000). Plasma and cerebrospinal fluid levels of amyloid beta proteins 1-40 and 1-42 in Alzheimer disease. Arch Neurol 57, 100-105.
34. Motter R, Vigo-Pelfrey C, Kholodenko D, Barbour R, Johnson-Wood K, Galasko D, Chang L, Miller B, Clark C, Green R & et al. (1995). Reduction of beta-amyloid peptide42 in the cerebrospinal fluid of patients with Alzheimer's disease. Ann Neurol 38, 643-648.
35. Moyer JR Jr & Brown TH (1998). Methods for whole-cell recording from visually preselected neurons of perirhinal cortex in brain slices from young and aging rats. J Neurosci Meth 86, 35-54.
36. 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 abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation. J Neurosci 20, 4050-4058.
37. Neuhoff H, Roeper J & Schweizer M (1999). Activity-dependent formation of perforated synapses in cultured hippocampal neurons. Eur J Neurosci 11, 4241-4250.
38. Oddo S, Billings L, Kesslak JP, Cribbs DH & LaFerla FM (2004). Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 43, 321-332.
39. 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.
40. Papa M & Segal M (1996). Morphological plasticity in dendritic spines of cultured hippocampal neurons. Neuroscience 71, 1005-1011.
41. Podlisny MB, Ostaszewski BL, Squazzo SL, Koo EH, Rydell RE, Teplow DB & Selkoe DJ (1995). Aggregation of secreted amyloid beta-protein into sodium dodecyl sulfate-stable oligomers in cell culture. J Biol Chem 270, 9564-9570.
42. Podlisny MB, Walsh DM, Amarante P, Ostaszewski BL, Stimson ER, Maggio JE, Teplow DB & Selkoe DJ (1998). Oligomerization of endogenous and synthetic amyloid beta-protein at nanomolar levels in cell culture and stabilization of monomer by Congo red. Biochemistry 37, 3602-3611.
43. Selkoe DJ (2002). Alzheimer's disease is a synaptic failure. Science 298, 789-791.
44. Streit WJ (2004). Microglia and Alzheimer's disease pathogenesis. J Neurosci Res 77, 1-8.
45. Sudo S, Shiozawa M, Cairns NJ & Wada Y (2005). Aberrant accentuation of neurofibrillary degeneration in the hippocampus of Alzheimer's disease with amyloid precursor protein 717 and presenilin-1 gene mutations. J Neurol Sci 234, 55-65.
46. 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.
47. 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.
48. Walsh DM, Townsend M, Podlisny MB, Shankar GM, Fadeeva JV, Agnaf OE, Hartley DM & Selkoe DJ (2005). Certain inhibitors of synthetic amyloid beta-peptide (Abeta) fibrillogenesis block oligomerization of natural Abeta and thereby rescue long-term potentiation. J Neurosci 25, 2455-2462.
49. Walsh DM, Tseng BP, Rydel RE, Podlisny MB & Selkoe DJ (2000). The oligomerization of amyloid beta-protein begins intracellularly in cells derived from human brain. Biochemistry 39, 10831-10839.
50. 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.
51. Wang Q, Walsh DM, Rowan MJ, Selkoe DJ & Anwyl R (2004). Block of long-term potentiation by naturally secreted and synthetic amyloid beta-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.
52. Wolfe MS, Xia W, Ostaszewski BL, Diehl TS, Kimberly WT & Selkoe DJ (1999). Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature 398, 513-517.
53. Xia W, Zhang J, Kholodenko D, Citron M, Podlisny MB, Teplow DB, Haass C, Seubert P, Koo EH & Selkoe DJ (1997). Enhanced production and oligomerization of the 42-residue amyloid beta-protein by Chinese hamster ovary cells stably expressing mutant presenilins. J Biol Chem 272, 7977-7982.
54. Yasuda H, Barth AL, Stellwagen D & Malenka RC (2003). A developmental switch in the signaling cascades for LTP induction. Nat Neurosci 6, 15-16.
55. Zhang H, Gong B, Liu S, Fa M, Ninan I, Staniszewski A & Arancio O (2005). Synaptic fatigue is more pronounced in the APP/PS1 transgenic mouse model of Alzheimer's disease. Curr Alzheimer Res 2, 137-140.
56. Zucker RS & Regehr WG (2002). Short-term synaptic plasticity. Calcium- and activity-dependent synaptic plasticity. Annu Rev Physiol 64, 355-405.