Antibodies against β-amyloid reduce Aβ oligomers, glycogen synthase kinase-3β activation and τ phosphorylation in vivo and in vitro

Journal of Neuroscience Research

Volumn 83, Issue 3, 2006, Pages 374-384

  Ma, Qiu Lan ^a,c   Lim, Giselle P ^a,c   Harris White, Marni E ^a,c   Yang, Fusheng ^a,c   Ambegaokar, Surendra S ^a,c   Ubeda, Oliver J ^a,c   Glabe, Charles G ^d   Teter, Bruce ^a,c   Frautschy, Sally A ^a,b,c   Cole, Greg M ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's disease; Amyloid; Immunoneutralization; Neurofibrillary tangles; Passive immunization

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN ANTIBODY; AMYLOID BETA PROTEIN ANTIBODY 4G8; AMYLOID BETA PROTEIN ANTIBODY 6E10; GLYCOGEN SYNTHASE KINASE 3BETA; OLIGOMER; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CELL CULTURE; CELL LINE; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; CULTURE MEDIUM; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; MALE; MOUSE; NEUROFIBRILLARY TANGLE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OSMOTIC MINIPUMP; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE;

AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANALYSIS OF VARIANCE; ANIMALS; ANTIBODIES; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; CEREBRAL CORTEX; ENZYME ACTIVATION; ENZYME REACTIVATORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, TRANSGENIC; NEUROBLASTOMA; PEPTIDE FRAGMENTS; PHOSPHORYLATION; RANDOM ALLOCATION; SENILE PLAQUES; SILVER STAINING; TAU PROTEINS;

EID: 31844439888     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.20734     Document Type: Article

References (60)

1. Alvarez G, Munoz-Montano JR, Satrustegui J, Avila J, Bogonez E, Diaz-Nido J. 1999. Lithium protects cultured neurons against beta-amyloid-induced neurodegeneration. FEBS Lett 453:260-264.
2. Alvarez G, Munoz-Montano JR, Satrustegui J, Avila J, Bogonez E, Diaz-Nido J. 2002. Regulation of τ phosphorylation and protection against beta-amyloid-induced neurodegeneration by lithium. Possible implications for Alzheimer's disease. Bipolar Disord 4:153-165.
3. Avila J, Dominguez J, Diaz-Nido J (1994) Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. Int J Dev Biol 38:13-25.
4. Bard F, Barbour R, Cannon C, Carretto R, Fox M, Games D, Guido T, Hoenow K, Hu K, Johnson-Wood K, Khan K, Kholodenko D, Lee C, Lee M, Motter R, Nguyen M, Reed A, Schenk D, Tang P, Vasquez N, Seubert P, Yednock T. 2003. Epitope and isotype specificities of antibodies to beta-amyloid peptide for protection against Alzheimer's disease-like neuropathology. Proc Natl Acad Sci USA 100:2023-2028.
5. Bard F, Cannon C, Barbour R, Burke R, Games D, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Lieberburg I, Motter R, Nguyen M, Soriano F, Vasquez N, Weiss K, Welch B, Seubert P, Schenk D, Yednock T. 2000. Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat Med 6:916-919.
6. Brendza RP, Bacskai BJ, Cirrito JR, Simmons KA, Skoch JM, Klunk WE, Mathis CA, Bales KR, Paul SM, Hyman BT, Holtzman DM. 2005. Anti-Abeta antibody treatment promotes the rapid recovery of amyloid-associated neuritic dystrophy in PDAPP transgenic mice. J Clin Invest 115:428-433.
7. Busciglio J, Lorenzo A, Yeh J, Yankner BA. 1995. Beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14:879-888.
8. Caceres A, Kosik KS. 1990. Inhibition of neurite polarity by tau; antisense oligonucleotides in primary cerebellar neurons. Nature 343:461-463.
9. Calon F, Lim GP, Yang F, Morihara T, Teter B, Ubeda O, Rostaing P, Triller A, Salem N, Jr., Ashe KH, Frautschy SA, Cole GM. 2004. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 43:633-645.
10. 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.
11. Chun D, Gall CM, Bi X, Lynch G. 2001. Evidence that integrins contribute to multiple stages in the consolidation of long term potentiation in rat hippocampus. Neuroscience 105:815-829.
12. 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.
13. Esmaeli-Azad B, McCarty JH, Feinstein SC. 1994. Sense and antisense transfection analysis of tau function: tau influences net microtubule assembly, neurite outgrowth and neuritic stability. J Cell Sci 107:869-879.
14. Frautschy SA, Hu W, Kim P, Miller SA, Chu T, Harris-White ME, Cole GM. 2001. Phenolic anti-inflammatory antioxidant reversal of Abeta-induced cognitive deficits and neuropathology. Neurobiol Aging 22:993-1005.
15. Funato H, Enya M, Yoshimura M, Morishima-Kawashima M, Ihara Y. 1999. Presence of sodium dodecyl sulfate-stable amyloid beta-protein dimers in the hippocampus CA1 not exhibiting neurofibrillary tangle formation. Am J Pathol 155:23-28.
16. Gary DS, Milhavet O, Camandola S, Mattson MP. 2003. Essential role for integrin linked kinase in Akt-mediated integrin survival signaling in hippocampal neurons. J Neurochem 84:878-890.
17. Gelinas DS, DaSilva K, Fenili D, St. George-Hyslop P, McLaurin J. 2004. Immunotherapy for Alzheimer's disease. Proc Natl Acad Sci USA 101(Suppl):14657-14662.
18. Greenberg SG, Davies P, Schein JD, Binder LI. 1992. Hydrofluoric acid-treated tau PHF proteins display the same biochemical properties as normal tau. J Biol Chem 267:564-569.
19. Gotz J, Chen F, van Dorpe J, Nitsch RM. 2001. Formation of neurofibrillary tangles in P3011 tau; transgenic mice induced by Abeta 42 fibrils. Science 293:1491-1495.
20. Harada A, Oguchi K, Okabe S, Kuno J, Terada S, Ohshima T, Sato-Yoshitake R, Takei Y, Noda T, Hirokawa N. 1994. Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 369:488-491.
21. Hardy JA, Higgins GA. 1992. Alzheimer's disease: the amyloid cascade hypothesis. Science 256:184-185.
22. 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.
23. Hye A, Kerr F, Archer N, Foy C, Poppe M, Brown R, Hamilton G, Powell J, Anderton B, Lovestone S. 2005. Glycogen synthase kinase-3 is increased in white cells early in Alzheimer's disease. Neurosci Lett 373:1-4.
24. Iqbal K, Zaidi T, Bancher C, Grundke-Iqbal I. 1994. Alzheimer paired helical filaments. Restoration of the biological activity by dephosphorylation. FEBS Lett 349:104-108.
25. SW Transgenic mice develop age-related Aβ deposits and neuropil abnormalities, but no neuronal loss in CA1. J Neuropathol Exp Neurol 56:965-973.
26. Janus C, Heslin D, French J, Mount HTJ, Nixon RA, Mercken M, Bergeron C, Fraser PE, St. George-Hyslop P, Westaway D. 2000. Aβ peptide immunization reduces behavioral impairment and plaques in a model of Alzheimer's disease. Nature 408:979-986.
27. 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.
28. Klein WL, Krafft GA, Finch CE. 2001. Targeting small Aβ oligomers: the solution to an Alzheimer's disease conundrum? TINS 24:219-224.
29. Koenigsknecht J, Landreth G. 2004. Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism. J Neurosci 24:9838-9846.
30. Kumar-Singh S, Dewachter I, Moechars D, Lubke U, De Jonghe C, Ceuterick C, Checler F, Naidu A, Cordell B, Cras P, Van Broeckhoven C, Van Leuven F. 2000. Behavioral disturbances without amyloid deposits in mice overexpressing human amyloid precursor protein with Flemish (A692G) or Dutch (E693Q) mutation. Neurobiol Dis 7:9-22.
31. 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.
32. 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.
33. Lee VM, Trojanowski JQ. 1999. Neurodegenerative tauopathies: human disease and transgenic mouse models. Neuron 24:507-510.
34. Lesné S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH. 2005. A specific amyloid-β assembly in the brain impairs memory. Nature (in press).
35. Lewis J, Dickson DW, Lin W-L, Chisholm L, Corral A, Jones G, Yen S-H, Sahara N, Skipper L, Yager D, Eckman C, Hardy J, Hutton J, McGowan E. 2001. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293:1487-1491.
36. Lim GP, Calon F, Morihara T, Yang F, Teter B, Ubeda O, Salem N Jr, Frautschy SA, Cole GM. 2005. A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. J Neurosci 25:3032-3040.
37. Lim GP, Yang F, Chu T, Chen P, Beech W, Teter B, Tran T, Ubeda O, Ashe KH, Frautschy SA, Cole GM. 2000. Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease. J Neurosci 20:5709-5714.
38. Lorenzo A, Yankner BA. 1994. Beta-amyloid neurotoxicity requires fibril formation and is inhibited by congo red. Proc Natl Acad Sci USA 91:12243-12247.
39. Lovestone S, Reynolds CH. 1997. The phosphorylation of tau: a critical stage in neurodevelopment and neurodegenerative processes. Neuroscience 78:309-324.
40. Lovestone S, Davis DR, Webster MT, Kaech S, Brion JP, Matus A, Anderton BH. 1999. Lithium reduces tau phosphorylation: effects in living cells and in neurons at therapeutic concentrations. Biol Psychiatry 45:995-1003.
41. Lovestone S, Reynolds CH, Latimer D, Davis DR, Anderton BH, Gallo JM, Hanger D, Mulot S, Marquardt B, Stabel S, et al. 1994. Alzheimer's disease-like phosphorylation of the microtubule-associated protein τ by glycogen synthase kinase-3 in transfected mammalian cells. Curr Biol 4:1077-1086.
42. 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.
43. McLean CA, Chemy 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.
44. Moechars D, Lorent K, DeStrooper B, Dewachter I, VanLeuven F. 1996. Expression in brain of amyloid precursor protein mutated in the alpha-secretase site causes disturbed behavior, neuronal degeneration and premature death in transgenic mice. EMBO J 15:1265-1274.
45. Morgan D, Diamond DM, Gottschall PE, Ugen KE, Dickey C, Hardy J, Duff K, Jantzen P, DiCarlo G, Wilcock D, Connor K, Hatcher J, Hope C, Gordon M, Arendash GW. 2000. Aβ peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 408:982-985.
46. Mucke L, Yu GQ, McConlogue L, Rockenstein EM, Abraham CR, Masliah E. 2000. Astroglial expression of human alpha(1)-antichymotrypsin enhances Alzheimer-like pathology in amyloid protein precursor transgenic mice. Am J Pathol 157:2003-2010.
47. Munoz-Montano JR, Moreno FJ, Avila J, Diaz-Nido J. 1997. Lithium inhibits Alzheimer's disease-like tau protein phosphorylation in neurons. FEBS Lett 411:183-188.
48. 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.
49. Pei JJ, Braak E, Braak H, Grundke-Iqbal I, Iqbal K, Winblad B, Cowburn RF. 1999. Distribution of active glycogen synthase kinase 3beta (GSK-3beta) in brains staged for Alzheimer disease neurofibrillary changes. J Neuropathol Exp Neurol 58:1010-1019.
50. Pike CJ, Burdick D, Walencewicz AJ, Glabe CG, Cotman CW. 1993. Neurodegeneration induced by beta-amyloid peptides in vitro: the role of peptide assembly state. J Neurosci 13:1676-1687.
51. Selkoe DJ. 1999. Translating cell biology into therapeutic advances in Alzheimer's disease. Nature 399:A23-31.
52. Spillantini MG, Goedert M. 1998. Tau protein pathology in neurodegenerative diseases. Trends Neurosci 21:428-433.
53. Takashima A, Honda T, Yasutake K, Michel G, Murayama O, Murayama M, Ishiguro K, Yamaguchi H. 1998. Activation of tau protein kinase I/glycogen synthase kinase-3beta by amyloid beta peptide (25-35) enhances phosphorylation of tau in hippocampal neurons. Neurosci Res 31:317-323.
54. Tomidokoro Y, Ishiguro K, Harigaya Y, Matsubara E, Ikeda M, Park JM, Yasutake K, Kawarabayashi T, Okamoto K, Shoji M. 2001. Abeta amyloidosis induces the initial stage of tau accumulation in APP(Sw) mice. Neurosci Lett 299:169-172.
55. Wagner U, Wiederholt M. 1996. Membrane voltage and whole-cell currents in cultured pericytes of control rats and rats with retinal dystrophy. Curr Eye Res 15:1045-1053.
56. 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.
57. 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.
58. Westerman MA, Cooper-Blacketer D, Mariash A, Kotilinek L, Kawara-bayashi T, Younkin LH, Carlson GA, Younkin SG, Ashe KH. 2002. The relationship between Abeta and memory in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 22:1858-1867.
59. Yang F, Mak K, Vinters HV, Frautschy SA, Cole GM. 1994. Monoclonal antibody to the C-terminus of beta-amyloid. Neuroreport 5:2117-2120.
60. Yang F, Lim GP, Begum AN, Ubeda OJ, Simmons MR, Ambegaokar SS, Chen PP, Kayed R, Glabe CG, Frautschy SA, Cole GM. 2005. Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J Biol Chem 280:5892-5901.