Pathways by which Aβ facilitates tau pathology

Current Alzheimer Research

Volumn 3, Issue 5, 2006, Pages 437-448

  Blurton Jones, Mathew ^a   LaFerla, Frank M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amyloid; Axonal transport; Inflammation; Neurofibrillary tangles; Oligomer; PHF; Phosphorylation; Proteasome

Indexed keywords

AMYLOID BETA PROTEIN; PROTEASOME; TAU PROTEIN;

ALZHEIMER DISEASE; HISTOPATHOLOGY; INFLAMMATION; NERVE DEGENERATION; NERVE FIBER TRANSPORT; NEUROFIBRILLARY TANGLE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; ANIMAL; CHEMICALLY INDUCED DISORDER; ENZYME ACTIVATION; HISTORY; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; SENILE PLAQUE; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; AXONAL TRANSPORT; ENZYME ACTIVATION; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; INFLAMMATION; NEUROFIBRILLARY TANGLES; PROTEASOME ENDOPEPTIDASE COMPLEX; SENILE PLAQUES; SIGNAL TRANSDUCTION; TAU PROTEINS;

EID: 33846047004     PISSN: 15672050     EISSN: None     Source Type: Journal    
DOI: 10.2174/156720506779025242     Document Type: Review

References (146)

1. Alzheimer, A.Ü.e.e.E.d.H. and the task of validating novel late-onset AD rinde. Allg Zeitschr Psychiatr Psychiatr-Gerichtl Med. 109, Über eine eigenartige Erkrankung der Hirnrinde. Allg Zeitschr Psychiatr Psychiatr-Gerichtl Med 109: 146-148 (1907).
2. Billings LM, Oddo S, Green KN, McGaugh JL and LaFerla FM, Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45: 675-88 (2005).
3. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, et al. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8: 79-84 (2005).
4. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416: 535-9 (2002).
5. Roberson ED, Scearce-Levie K, Yan F, Yu G and Mucke L. Tau reduction ameliorates behavioral and pathological abnormalities in APP transgenic mice. Society for Neuroscience Abstracts 206.6: (2005).
6. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440: 352-7 (2006).
7. Glenner GG. and Wong CW. Alzheimer's disease-initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem.Biophys Res Comm 120: 885-890 (1984).
8. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL and Beyreuther K. Amyloid plaque core protein in Alzheimer-disease and Down syndrome. Proc Natl Acad Sci USA 82: 4245-4249 (1985).
9. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM and Binder LI. Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83: 4913-7 (1986).
10. Delacourte A and Defossez A, Alzheimer's disease: Tau proteins, the promoting factors of microtubule assembly, are major components of paired helical filaments. J Neurol Sci 76: 173-86 (1986).
11. Kosik KS, Joachim CL and Selkoe DJ. Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc Natl Acad Sci USA 83: 4044-8 (1986).
12. Hardy J, and Selkoe DJ, The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353-6 (2002).
13. Lewis J, Dickson DW, Lin WL, Chisholm L, Corral A, Jones G, et al. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293: 1487-91 (2001).
14. Gotz J, Chen F, van Dorpe J and Nitsch RM. Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils. Science 293: 1491-5 (2001).
15. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, et al. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39: 409-21 (2003).
16. St George-Hyslop PH and Petit A. Molecular biology and genetics of Alzheimer's disease. C R Biol 328: 119-30 (2005).
17. Tanzi RE, Gusella JF, Watkins PC, Bruns GAP, St.Geroge-Hyslop P, Van Keuren ML, et al. Amyloid beta protein gene: cDNA, mRNA distribution, and genetic linkage near the Alzheimer locus. Science 235: 880-884 (1987).
18. Goldgaber D, Lerman MI, McBride OW, Saffiotti U and Gajdusek DC. Characterization and chromosomal localization of a cDNA encoding brain amyloid of Alzheimer's disease. Science 235: 877-80 (1987).
19. Levy E, Carman MD, Fernandez-Madrid IJ, Power MD, Lieberburg I, van Duinen SG, et al. Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type. Science 248: 1124-6 (1990).
20. Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, Fidani L, et al. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349: 704-6 (1991).
21. Tandon A, Rogaeva E, Mullan M and St George-Hyslop PH. Molecular genetics of Alzheimer's disease: the role of beta-amyloid and the presenilins. Curr Opin Neurol 13: 377-84 (2000).
22. Sherrington R, Rogaev EI, Liang Y, Rogaeva EA, Levesque G, Ikeda M, et al. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375: 754-60 (1995).
23. Levy-Lahad E, Wasco W, Poorkaj P, Romano DM, Oshima J, Pettingell WH, et al. Candidate gene for the chromosome 1 familial Alzheimer's disease locus. Science 269: 973-7 (1995).
24. Rogaev EI, Sherrington R, Rogaeva EA, Levesque G, Ikeda M, Liang Y, et al. Familial Alzheimer's disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene. Nature 376: 775-8 (1995).
25. Selkoe DJ, Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81: 741-66 (2001).
26. Selkoe D and Kopan R, Notch and Presenilin: regulated intramembrane proteolysis links development and degeneration. Annu Rev Neurosci 26: 565-97 (2003).
27. De Strooper B, Aph-1 Pen-2 and Nicastrin with Presenilin generate an active gamma-Secretase complex. Neuron 38: 9-12 (2003).
28. Younkin SG. The role of A beta 42 in Alzheimer's disease. J Physiol Paris 92: 289-92 (1998).
29. Jarrett JT, Berger EP and Lansbury PT Jr. The carboxy terminus of the beta amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease. Biochemistry 32: 4693-7 (1993).
30. Jarrett JT, Berger EP and Lansbury PT Jr , The C-terminus of the beta protein is critical in amyloidogenesis. Ann N Y Acad Sci 695: 144-8 (1993).
31. Iwatsubo T, Odaka A, Suzuki N, Mizusawa H, Nukina N and Ihara Y. Visualization of A beta 42(43) and A beta 40 in senile plaques with end-specific A beta monoclonals: evidence that an initially deposited species is A beta 42(43). Neuron 13: 45-53 (1994).
32. Gravina SA, Ho L, Eckman CB, Long KE, Otvos L Jr, Younkin LH, et al. Amyloid beta protein (A beta) in Alzheimer's disease brain. Biochemical and immunocytochemical analysis with antibodies specific for forms ending at A beta 40 or A beta 42(43). J Biol Chem 270: 7013-6 (1995).
33. Takashima S Down syndrome. Curr Opin Neurol 10: 148-52 (1997).
34. Rovelet-Lecrux A, Hannequin D, Raux G, Le Meur N, Laquerriere A, Vital A, et al. APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat Genet 38: 24-6 (2006).
35. Theuns J, Brouwers N, Engelborghs S, Sleegers K, Bogaerts V, Corsmit E, et al. Promoter mutations that increase amyloid precursor-protein expression are associated with Alzheimer disease. Am J Hum Genet 78: 936-46 (2006).
36. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300: 486-9 (2003).
37. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, et al. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95: 6448-53 (1998).
38. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, Lomakin A, et al. Amyloid beta-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J Biol Chem 274: 25945-52 (1999).
39. Nilsberth C, Westlind-Danielsson A, Eckman CB, Condron MM, Axelman K, Forsell C, et al. The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Abeta protofibril formation. Nat Neurosci 4: 887-93 (2001).
40. Whalen BM, Selkoe DJ and Hartley DM. Small non-fibrillar assemblies of amyloid beta-protein bearing the Arctic mutation induce rapid neuritic degeneration. Neurobiol Dis 20: 254-66 (2005).
41. Hutton M, Missense and splice site mutations in tau associated with FTDP-17: multiple pathogenic mechanisms. Neurology 56: S21-5 (2001).
42. Stoothoff WH and Johnson GV, Tau phosphorylation: physiological and pathological consequences. Biochim Biophys Acta 1739: 280-97 (2005).
43. Lovestone S. and Reynolds CH. The phosphorylation of tau: a critical stage in neurodevelopment and neurodegenerative processes. Neuroscience 78: 309-24 (1997).
44. Lee G, Thangavel R, Sharma VM, Litersky JM, Bhaskar K, Fang SM, et al. Phosphorylation of tau by fyn: implications for Alzheimer's disease. J Neurosci 24: 2304-12 (2004).
45. Derkinderen P, Scales TM, Hanger DP, Leung KY, Byers HL, Ward MA, et al. Tyrosine 394 is phosphorylated in Alzheimer's paired helical filament tau and in fetal tau with c-Abl as the candidate tyrosine kinase. J Neurosci 25: 6584-93 (2005).
46. Ho GJ, Hashimoto M, Adame A, Izu M, Alford MF, Thal LJ, et al. Altered p59Fyn kinase expression accompanies disease progression in Alzheimer's disease: implications for its functional role. Neurobiol Aging 26: 625-35 (2005).
47. Swatton JE, Sellers LA, Faull RL, Holland A, Iritani S and Bahn S, Increased MAP kinase activity in Alzheimer's and Down syndrome but not in schizophrenia human brain. Eur J Neurosci 19: 2711-9 (2004).
48. Griffin RJ, Moloney A, Kelliher M, Johnston JA, Ravid R, Dockery P, et al. Activation of Akt/PKB, increased phosphorylation of Akt substrates and loss and altered distribution of Akt and PTEN are features of Alzheimer's disease pathology. J Neurochem 93: 105-17 (2005).
49. Ferrer I, Barrachina M and Puig B. Glycogen synthase kinase-3 is associated with neuronal and glial hyperphosphorylated tau deposits in Alzheimer's disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Acta Neuropathol (Berl) 104: 583-91 (2002).
50. Pei JJ, Braak E, Braak H, Grundke-Iqbal I, Iqbal K, Winblad B, et al. Localization of active forms of C-jun kinase (JNK) and p38 kinase in Alzheimer's disease brains at different stages of neurofibrillary degeneration. J Alzheimers Dis 3: 41-48 (2001).
51. Sengupta A, Kabat J, Novak M, Wu Q, Grundke-Iqbal I and Iqbal K. Phosphorylation of tau at both Thr 231 and Ser 262 is required for maximal inhibition of its binding to microtubules. Arch Biochem Biophys 357: 299-309 (1998).
52. Drewes G, Trinczek B, Illenberger S, Biernat J, Schmitt-Ulms G, Meyer HE, et al. Microtubule-associated protein/microtubule affinity-regulating kinase (p110mark). A novel protein kinase that regulates tau-microtubule interactions and dynamic instability by phosphorylation at the Alzheimer-specific site serine 262. J Biol Chem 270: 7679-88 (1995).
53. Bramblett GT, Goedert M, Jakes R, Merrick SE, Trojanowski JQ and Lee VM, Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10: 1089-99 (1993).
54. Goedert M, Jakes R, Crowther RA, Six J, Lubke U, Vandermeeren M, et al. The abnormal phosphorylation of tau protein at Ser-202 in Alzheimer disease recapitulates phosphorylation during development. Proc Natl Acad Sci USA 90: 5066-70 (1993).
55. Brion JP, Smith C, Couck AM, Gallo JM and Anderton BH. Developmental changes in tau phosphorylation: fetal tau is transiently phosphorylated in a manner similar to paired helical filament-tau characteristic of Alzheimer's disease. J Neurochem 61: 2071-80 (1993).
56. Necula M and Kuret J. Site-specific pseudophosphorylation modulates the rate of tau filament dissociation. FEBS Lett 579: 1453-7 (2005).
57. Necula M and Kuret J. Pseudophosphorylation and glycation of tau protein enhance but do not trigger fibrillization in vitro. J Biol Chem 279: 49694-703 (2004).
58. Cruz JC, Tseng HC, Goldman JA, Shih H and Tsai LH. Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron 40: 471-83 (2003).
59. Perez M, Hernandez F, Lim F, Diaz-Nido J and Avila J. Chronic lithium treatment decreases mutant tau protein aggregation in a transgenic mouse model. J Alzheimers Dis 5: 301-8 (2003).
60. Noble W, Planel E, Zehr C, Olm V, Meyerson J, Suleman F, et al. Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc Natl Acad Sci USA 102: 6990-5 (2005).
61. Mawal-Dewan M, Henley J, Van de Voorde A, Trojanowski JQ. and Lee VM. The phosphorylation state of tau in the developing rat brain is regulated by phosphoprotein phosphatases. J Biol Chem 269: 30981-7 (1994).
62. Liu F, Iqbal K, Grundke-Iqbal I, Rossie S and Gong CX. Dephosphorylation of tau by protein phosphatase 5: impairment in Alzheimer's disease. J Biol Chem 280: 1790-6 (2005).
63. Vogelsberg-Ragaglia V, Schuck T, Trojanowski JQ and Lee VM .PP2A mRNA expression is quantitatively decreased in Alzheimer's disease hippocampus. Exp Neurol 168: 402-12 (2001).
64. Sontag E, Luangpirom A, Hladik C, Mudrak I, Ogris E, Speciale S, et al. Altered expression levels of the protein phosphatase 2A ABalphaC enzyme are associated with Alzheimer disease pathology. J Neuropathol Exp Neurol 63: 287-301 (2004).
65. Kins S, Crameri A, Evans DR, Hemmings BA, Nitsch RM. and Gotz J. Reduced protein phosphatase 2A activity induces hyperphosphorylation and altered compartmentalization of tau in transgenic mice. J Biol Chem 276: 38193-200 (2001).
66. Takashima A, Noguchi K, Sato K, Hoshino T and Imahori K. Tau protein kinase I is essential for amyloid beta-protein-induced neurotoxicity. Proc Natl Acad Sci USA 90: 7789-93 (1993).
67. Busciglio J, Lorenzo A, Yeh J and Yankner BA. beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14: 879-88 (1995).
68. Alvarez A, Toro R, Caceres A and Maccioni RB. Inhibition of tau phosphorylating protein kinase cdk5 prevents beta-amyloid-induced neuronal death. FEBS Lett 459: 421-6 (1999).
69. Takashima A, Honda T, Yasutake K, Michel G, Murayama O, Murayama M, et al. 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: 317-23 (1998).
70. Rapoport M, Dawson HN, Binder LI, Vitek MP and Ferreira A. Tau is essential to beta -amyloid-induced neurotoxicity. Proc Natl Acad Sci USA 99: 6364-9 (2002).
71. Michaelis ML, Ranciat N, Chen Y, Bechtel M, Ragan R, Hepperle M, et al. Protection against beta-amyloid toxicity in primary neurons by paclitaxel (Taxol). J Neurochem 70: 1623-7 (1998).
72. Ferrari A, Hoerndli F, Baechi T, Nitsch RM and Gotz J. beta-amyloid induces PHF-like tau filaments in tissue culture. J Biol Chem: (2003).
73. Pennanen L and Gotz J. Different tau epitopes define Abeta42-mediated tau insolubility. Biochem Biophys Res Commun 337: 1097-101 (2005).
74. Puig B, Gomez-Isla T, Ribe E, Cuadrado M, Torrejon-Escribano B, Dalfo E, et al. Expression of stress-activated kinases c-Jun N-terminal kinase (SAPK/JNK-P) and p38 kinase (p38-P), and tau hyperphosphorylation in neurites surrounding betaA plaques in APP Tg2576 mice. Neuropathol Appl Neurobiol 30: 491-502 (2004).
75. Hwang DY, Cho JS, Lee SH, Chae KR, Lim HJ, Min SH, et al. Aberrant expressions of pathogenic phenotype in Alzheimer's diseased transgenic mice carrying NSE-controlled APPsw. Exp Neurol 186: 20-32 (2004).
76. Masliah E and Rockenstein E. Genetically altered transgenic models of Alzheimer's disease. J Neural Transm Suppl 59: 175-83 (2000).
77. Ma QL, Lim GP, Harris-White ME, Yang F, Ambegaokar SS, Ubeda OJ, et al. Antibodies against beta-amyloid reduce abeta oligomers, glycogen synthase kinase-3beta activation and tau phosphorylation in vivo and in vitro. J Neurosci Res: (2005).
78. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, Van Slegtenhorst M, et al. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 25: 402-5 (2000).
79. Oddo S, Billings L, Kesslak JP, Cribbs DH and LaFerla FM. Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 43: 321-32 (2004).
80. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al. Inflammation and Alzheimer's disease. Neurobiol Aging 21: 383-421 (2000).
81. Wyss-Coray T and Mucke L. Inflammation in neurodegenerative disease - a double-edged sword. Neuron 35: 419-32 (2002).
82. Griffin WST, Stanley LC, Ling C, White L, MacLeod V, Perrot LJ, et al. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc Natl Acad Sci USA 86: 7611-7615 (1989).
83. Duffy PE, Rapport M and Graf L, Glial fibrillary acidic protein and Alzheimer-type senile dementia. Neurology 30: 778-82 (1980).
84. Sheng JG, Mrak RE and Griffin WS. Microglial interleukin-1 alpha expression in brain regions in Alzheimer's disease: correlation with neuritic plaque distribution. Neuropathol Appl Neurobiol 21: 290-301 (1995).
85. Combs CK, Karlo JC, Kao SC and Landreth GE. beta-Amyloid stimulation of microglia and monocytes results in TNFalpha-dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J Neurosci 21: 1179-88 (2001).
86. Tan J, Town T, Mori T, Wu Y, Saxe M, Crawford F, et al. CD45 opposes beta-amyloid peptide-induced microglial activation via inhibition of p44/42 mitogen-activated protein kinase. J Neurosci 20: 7587-94 (2000).
87. Galimberti D, Baron P, Meda L, Prat E, Scarpini E, Delgado R, et al. Alpha-MSH peptides inhibit production of nitric oxide and tumor necrosis factor-alpha by microglial cells activated with beta-amyloid and interferon gamma. Biochem Biophys Res Commun 263: 251-6 (1999).
88. Ishizuka K, Kimura T, Igata-yi R, Katsuragi S, Takamatsu J and Miyakawa T. Identification of monocyte chemoattractant protein-1 in senile plaques and reactive microglia of Alzheimer's disease. Psychiatry Clin Neurosci 51: 135-8 (1997).
89. Yamamoto M, Horiba M, Buescher JL, Huang D, Gendelman HE, Ransohoff RM, et al. Overexpression of monocyte chemotactic protein-1/CCL2 in beta-amyloid precursor protein transgenic mice show accelerated diffuse beta-amyloid deposition. Am J Pathol 166: 1475-85 (2005).
90. Janelsins MC, Mastrangelo MA, Oddo S, LaFerla FM, Federoff HJ and Bowers WJ. Early correlation of microglial activation with enhanced tumor necrosis factor-alpha and monocyte chemoattractant protein-1 expression specifically within the entorhinal cortex of triple transgenic Alzheimer's disease mice. J Neuroinflammation 2: 23 (2005).
91. Rogers J, Cooper NR, Webster S, Schultz J, McGeer PL, Styren SD, et al. Complement activation by beta-amyloid in Alzheimer disease. Proc Natl Acad Sci USA 89: 10016-20 (1992).
92. Jiang H, Burdick D, Glabe CG, Cotman CW and Tenner AJ. beta-Amyloid activates complement by binding to a specific region of the collagen-like domain of the C1q A chain. J Immunol 152: 5050-9 (1994).
93. Chen S, Frederickson RC and Brunden KR. Neuroglial-mediated immunoinflammatory responses in Alzheimer's disease: complement activation and therapeutic approaches. Neurobiol Aging 17: 781-7 (1996).
94. Afagh A, Cummings BJ, Cribbs DH, Cotman CW and Tenner AJ. Localization and cell association of C1q in Alzheimer's disease brain. Exp Neurol 138: 22-32 (1996).
95. Wyss-Coray T, Yan F, Lin AH, Lambris JD, Alexander JJ, Quigg RJ, et al. Prominent neurodegeneration and increased plaque formation in complement-inhibited Alzheimer's mice. Proc Natl Acad Sci U S A 99: 10837-42 (2002).
96. Koenigsknecht-Talboo J and Landreth GE. Microglial phagocytosis induced by fibrillar beta-amyloid and IgGs are differentially regulated by proinflammatory cytokines. J Neurosci 25: 8240-9 (2005).
97. Wilcock DM, Rojiani A, Rosenthal A, Levkowitz G, Subbarao S, Alamed J, et al. Passive amyloid immunotherapy clears amyloid and transiently activates microglia in a transgenic mouse model of amyloid deposition. J Neurosci 24: 6144-51 (2004).
98. Hock C, Konietzko U, Papassotiropoulos A, Wollmer A, Streffer J, von Rotz, RC, et al. Generation of antibodies specific for beta-amyloid by vaccination of patients with Alzheimer disease. Nat Med 8: 1270-5 (2002).
99. Masliah E, Hansen L, Adame A, Crews L, Bard F, Lee C, et al. Abeta vaccination effects on plaque pathology in the absence of encephalitis in Alzheimer disease. Neurology 64: 129-31 (2005).
100. Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, Guido T, et al. Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400: 173-7 (1999).
101. Morgan, D., Diamond, D.M., Gottschall, P.E., Ugen, K.E., Dickey, C., Hardy, J., et al., A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 408: 982-5 (2000).
102. Gasparini L, Ongini E and Wenk G. Non-steroidal anti-inflammatory drugs (NSAIDs) in Alzheimer's disease: old and new mechanisms of action. J Neurochem 91: 521-36 (2004).
103. Quintanilla RA, Orellana DI, Gonzalez-Billault C and Maccioni RB. Interleukin-6 induces Alzheimer-type phosphorylation of tau protein by deregulating the cdk5/p35 pathway. Exp Cell Res 295: 245-57 (2004).
104. Li Y, Liu L, Barger SW and Griffin WS. Interleukin-1 mediates pathological effects of microglia on tau phosphorylation and on synaptophysin synthesis in cortical neurons through a p38-MAPK pathway. J Neurosci 23: 1605-11 (2003).
105. Saez TE, Pehar M, Vargas M, Barbeito L and Maccioni RB. Astrocytic nitric oxide triggers tau hyperphosphorylation in hippocampal neurons. In Vivo 18: 275-80 (2004).
106. Sheng JG, Zhu SG, Jones RA, Griffin WS and Mrak RE. Interleukin-1 promotes expression and phosphorylation of neurofilament and tau proteins in vivo. Exp Neurol 163: 388-91 (2000).
107. Sheng JG, Jones RA, Zhou XQ, McGinness JM, Van Eldik LJ, Mrak RE, et al. Interleukin-1 promotion of MAPK-p38 overexpression in experimental animals and in Alzheimer's disease: potential significance for tau protein phosphorylation. Neurochem Int 39: 341-8 (2001).
108. Hayes A, Thaker U, Iwatsubo T, Pickering-Brown SM and Mann DM. Pathological relationships between microglial cell activity and tau and amyloid beta protein in patients with Alzheimer's disease. Neurosci Lett 331: 171-4 (2002).
109. Kitazawa M, Oddo S, Yamasaki TR, Green KN and LaFerla FM. Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease. J Neurosci 25: 8843-53 (2005).
110. Haglund, K. and Dikic, I., Ubiquitylation and cell signaling. Embo J 24: 3353-9 (2005).
111. Ciechanover A and Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 40: 427-46 (2003).
112. Mori H, Kondo J and Ihara Y. Ubiquitin is a component of paired helical filaments in Alzheimer's disease. Science 235: 1641-4 (1987).
113. Perry G, Friedman R, Shaw G and Chau V. Ubiquitin is detected in neurofibrillary tangles and senile plaque neurites of Alzheimer disease brains. Proc Natl Acad Sci USA 84: 3033-6 (1987).
114. Kosik KS and Shimura H. Phosphorylated tau and the neurodegenerative foldopathies. Biochim Biophys Acta 1739: 298-310 (2005).
115. Shimura H, Schwartz D, Gygi SP and Kosik KS. CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J Biol Chem 279: 4869-76 (2004).
116. Sahara N, Murayama M, Mizoroki T, Urushitani M, Imai Y, Takahashi R, et al. In vivo evidence of CHIP up-regulation attenuating tau aggregation. J Neurochem 94: 1254-63 (2005).
117. Petrucelli L, Dickson D, Kehoe K, Taylor J, Snyder H, Grover A, et al. CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation. Hum Mol Genet 13: 703-14 (2004).
118. Qian SB, McDonough H, Boellmann F, Cyr DM and Patterson C. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 440: 551-5 (2006).
119. Keller JN, Hanni KB and Markesbery WR. Impaired proteasome function in Alzheimer's disease. J Neurochem 75: 436-9 (2000).
120. Keck S, Nitsch R, Grune T and Ullrich O. Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J Neurochem 85: 115-22 (2003).
121. Oh S, Hong HS, Hwang E, Sim HJ, Lee W, Shin SJ, et al. Amyloid peptide attenuates the proteasome activity in neuronal cells. Mech Ageing Dev 126: 1292-9 (2005).
122. Lopez Salon M, Pasquini L, Besio Moreno M, Pasquini JM and Soto E. Relationship between beta-amyloid degradation and the 26S proteasome in neural cells. Exp Neurol 180: 131-43 (2003).
123. Gregori L, Hainfeld JF, Simon MN and Goldgaber D. Binding of amyloid beta protein to the 20 S proteasome. J Biol Chem 272: 58-62 (1997).
124. Roy S, Zhang B, Lee VM and Trojanowski JQ. Axonal transport defects: a common theme in neurodegenerative diseases. Acta Neuropathol (Berl) 109: 5-13 (2005).
125. Stamer K, Vogel R, Thies E, Mandelkow E and Mandelkow EM. Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 156: 1051-63 (2002).
126. Lazarov O, Lee M, Peterson DA and Sisodia SS. Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J Neurosci 22: 9785-93 (2002).
127. Kamal A, Almenar-Queralt A, LeBlanc JF, Roberts EA and Goldstein LS. Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 414: 643-8 (2001).
128. Koo EH. Sisodia SS, Archer DR. Martin LJ, Weidemann A, Beyreuther K, et al. Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc Natl Acad Sci USA 87: 1561-5 (1990).
129. Kamal A, Stokin GB, Yang Z, Xia CH and Goldstein LS. Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28: 449-59 (2000).
130. Lazarov O, Morfini GA, Lee EB, Farah MH, Szodorai A, DeBoer SR, et al. Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: revisited. J Neurosci 25: 2386-95 (2005).
131. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, et al. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307: 1282-8 (2005).
132. Pigino G, Morfini G, Pelsman A, Mattson MP, Brady ST and Busciglio J. Alzheimer's presenilin 1 mutations impair kinesin-based axonal transport. J Neurosci 23: 4499-508 (2003).
133. Pigino GF and Brady ST. Beta-amyloid effects on kinesin function: novel model for pathogenesis in Alzheimer's disease. Society for Neuroscience Abstracts: (2005).
134. Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B and Mandelkow E. Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J Cell Biol 143: 777-94 (1998).
135. Mandelkow EM, Thies E, Trinczek B, Biernat J and Mandelkow E. MARK/PAR1 kinase is a regulator of microtubule-dependent transport in axons. J Cell Biol 167: 99-110 (2004).
136. Utton MA, Noble WJ, Hill JE, Anderton BH and Hanger DP. Molecular motors implicated in the axonal transport of tau and alpha-synuclein. J Cell Sci 118: 4645-54 (2005).
137. Aronov S, Aranda G, Behar L and Ginzburg I. Visualization of translated tau protein in the axons of neuronal P19 cells and characterization of tau RNP granules. J Cell Sci 115: 3817-27 (2002).
138. Aronov S, Aranda G, Behar L and Ginzburg I. Axonal tau mRNA localization coincides with tau protein in living neuronal cells and depends on axonal targeting signal. J Neurosci 21: 6577-87 (2001).
139. Oddo S, Caccamo A, Kitazawa M, Tseng BP and LaFerla FM. Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 24: 1063-70 (2003).
140. Khatoon S, Grundke-Iqbal I and Iqbal K. Levels of normal and abnormally phosphorylated tau in different cellular and regional compartments of Alzheimer disease and control brains. FEBS Lett 351: 80-4 (1994).
141. Ribe EM, Perez M, Puig B, Gich I, Lim F, Cuadrado M, et al. Accelerated amyloid deposition, neurofibrillary degeneration and neuronal loss in double mutant APP/tau transgenic mice. Neurobiol Dis 20: 814-22 (2005).
142. Goldsbury C, Mocanu MM, Thies E, Kaether C, Haass C, Keller P, et al. Inhibition of APP Trafficking by Tau Protein Does Not Increase the Generation of Amyloid-beta Peptides. Traffic: (2006).
143. Zhang B, Higuchi M, Yoshiyama Y, Ishihara T, Forman MS, Martinez D, et al. Retarded axonal transport of R406W mutant tau in transgenic mice with a neurodegenerative tauopathy. J Neurosci 24: 4657-67 (2004).
144. Ishihara T, Hong M, Zhang B, Nakagawa Y, Lee MK, Trojanowski JQ, et al. Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 24: 751-62 (1999).
145. Hardy J, Duff K, Hardy KG, Perez-Tur J and Hutton M. Genetic dissection of Alzheimer's disease and related dementias: amyloid and its relationship to tau. Nat Neurosci 1: 355-8 (1998).
146. Guo JP, Arai T, Miklossy J and McGeer PL Abeta and tau form soluble complexes that may promote self aggregation of both into the insoluble forms observed in Alzheimer's disease. Proc Natl Acad Sci USA 103: 1953-8 (2006).