Viewpoint: Crosstalks between neurofibrillary tangles and amyloid plaque formation

Ageing Research Reviews

Volumn 12, Issue 1, 2013, Pages 174-181

  Luan, Kailie ^a   Rosales, Jesusa L ^b   Lee, Ki Young ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Alzheimer's disease; Amyloid plaques; Tau kinases

Indexed keywords

ABELSON KINASE; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1; BUNGAROTOXIN RECEPTOR; CELL RECEPTOR; CYCLIN DEPENDENT KINASE 5; CYTOKINE; GAMMA SECRETASE; GLYCOGEN SYNTHASE KINASE 3BETA; KINESIN; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUROTROPHIN RECEPTOR P75; PROTEASOME; REACTIVE OXYGEN METABOLITE; TAU PROTEIN; UBIQUITIN;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; AMYLOID PLAQUE; BRAIN MITOCHONDRION; CARBOXY TERMINAL SEQUENCE; DISEASE COURSE; ENDOCYTOSIS; ENZYME ACTIVITY; HUMAN; INFLAMMATION; INTRACELLULAR SIGNALING; NERVE FIBER TRANSPORT; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; UPREGULATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; HUMANS; NEUROFIBRILLARY TANGLES; PLAQUE, AMYLOID; TAU PROTEINS;

EID: 84867366979     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2012.06.002     Document Type: Review

References (117)

1. Alvarez R., Toro A., Caceres, Maccioni R.B. Inhibition of tau phosphorylating protein kinase cdk5 prevents beta-amyloid-induced neuronal death. FEBS Lett. 1999, 459:421-426.
2. Alzheimer A. About a peculiar disease of the cerebral cortex (Translated by L. Jarvik and H. Greenson). Alzheimer Dis. Assoc. Disord. 1907, 1:3-8.
3. Anisman H. Cascading effects of stressors and inflammatory immune system activation: implications for major depressive disorder. J. Psychiatr. Neurosci. 2009, 34:4-20.
4. Aronov D., Aranda G., Behar L., Ginzburg I. Visualization of translated tau protein in the axons of neuronal P19 cells and characterization of tau RNP granules. J. Cell Sci. 2002, 115:3817-3827.
5. Avila J., Lucas J.J., Perez M., Hernandez F. Role of tau protein in both physiological and pathological conditions. Physiol. Rev. 2004, 84:361-384.
6. Balleza-Tapia H., Peña F. Pharmacology of the intracellular pathways activated by amyloid beta protein. Mini Rev. Med. Chem. 2009, 9:724-740.
7. Blurton-Jones M., LaFerla F.M. Pathways by which Aβ facilitates tau pathology. Curr. Alzheimer Res. 2006, 3:437-448.
8. Bu G., Cam J., Zerbinatti C. LRP in amyloid-β production and metabolism. Ann. N. Y. Acad. Sci. 2006, 1086:35-53.
9. Busciglio J., Gabuzda D.H., Matsudaira P., Yankner B.A. Generation of β-amyloid in the secretory pathway in neuronal and nonneuronal cells. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:2092-2096.
10. Butterfield D.A., Abdul H.M., Opii W., Newman S.F., Joshi G., Ansari M.A., Sultana R. Pin1 in Alzheimer's disease. J. Neurochem. 2006, 98:1697-1706.
11. Butterfield D.A., Perluigi M., Reed T., Muharib T., Hughes C.P., Robinson R.A.S., Sultana R. Redox proteomics in selected neurodegenerative disorders: from its infancy to future applications. Antioxid. Redox Signal. 2012, [Epub ahead of print].
12. Calcutt N.A., Cooper M.E., Kern T.S., Schmidt A.M. Therapies for hyperglycaemia-induced diabetic complications: from animal models to clinical trials. Nat. Rev. Drug Discov. 2009, 8:417-429.
13. Chen J.X., Yan S.S. Role of mitochondrial amyloid-beta in Alzheimer's disease. J. Alzheimers Dis. 2010, 20:569-578.
14. Chung C.W., Song Y.H., Kim I.K., Yoon W.J., Ryu B.R., Jo D.G., Woo H.N., Kwon Y.K., Kim H.H., Gwag B.J., Mook-Jung I.H., Jung Y.K. Proapoptotic effects of tau cleavage product generated by caspase-3. Neurobiol. Dis. 2001, 8:162-172.
15. Cleveland D.W., Hwo S.Y., Kirschner M.W. Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J. Mol. Biol. 1977, 116:227-247.
16. Cook D.G., Forman M.S., Sung J.C., Leight S., Kolson D.L., Iwatsubo T., Lee V.M., Doms R.W. Alzheimer's Aβ(1-42) is generated in the endoplasmic reticulum/intermediate compartment of NT2N cells. Nat. Med. 1997, 3:1021-1023.
17. Combs C.K., Karlo J.C., Kao S.C., Landreth G.E. Beta-Amyloid stimulation of microglia and monocytes results in TNF alpha dependent expression of inducible nitric oxide synthase and neuronal apoptosis. J. Neurosci. 2001, 21:1179-1188.
18. Cruz J.C., Tseng H.C., Goldman J.A., Shih H., Tsai L.H. Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron 2003, 40:471-483.
19. Czapski G.A., Gassowska M., Songin M., Radecka U.D., Strosznajder J.B. Alterations of cyclin dependent kinase 5 expression and phosphorylation in amyloid precursorprotein (APP)-transfected PC12 cells. FEBS Lett. 2011, 585:1243-1248.
20. Da Cruz e Silva E.F., Da Cruz e Silva O.A. Protein phosphorylation and APP metabolism. Neurochem. Res. 2003, 28:1553-1561.
21. Deane R., Du Yan S., Submamaryan R.K., LaRue B., Jovanovic S., Hogg E., Welch D., Manness L., Lin C., Yu J., Zhu H., Ghiso J., Frangione B., Stern A., Schmidt A.M., Armstrong D.L., Arnold B., Liliensiek B., Nawroth P., Hofman F., Kindy M., Stern D., Zlokovic B. RAGE mediates amyloid-β peptide transport across the blood-brain barrier and accumulation in brain. Nat. Med. 2003, 9:907-913.
22. Delacourte A., Defossez A. Alzheimer's disease: Tau proteins, the promoting factors of microtubule assembly, are major components of paired helical filaments. J. Neurol. Sci. 1986, 76:173-186.
23. Ebneth A., Godemann R., Stamer K., Illenberger S., Trinczek B., Mandelkow E. Overexpression of tau protein inhibits kinesin dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J. Cell Biol. 1998, 143:777-794.
24. Galimberti D., Baron P., Meda L., Prat E., Scarpini, Delgado R., Catania A., Lipton J.M., Scarlato G. 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. 1999, 263:251-256.
25. Gamblin T.C., Chen F., Zambrano A., Abraha A., Lagalwar S., Guillozet A.L., Lu M., Fu Y., Garcia-Sierra F., LaPointe N., Miller R., Berry R.W., Binder L.I., Cryns V.L. Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:10032-10037.
26. Garwood C.J., Pooler A.M., Atherton J., Hanger D.P., Noble W. Astrocytes are important mediators of Aβ induced neurotoxicity and tau phosphorylation in primary culture. Cell Death Dis. 2011, 2:e167.
27. Glenner G.G., Wong C.W. Alzheimer's disease-initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 1984, 120:885-890.
28. Gong C.X., Singh T.J., Grundke-Iqbal I., Iqbal K. Phosphoprotein phosphatase activities in Alzheimer's disease brain. J. Neurochem. 1993, 61:921-927.
29. Gong C.X., Singh T.J., Grundke-Iqbal I., Iqbal K. Alzheimer's disease abnormally phosphorylated tau is dephosphorylated by protein phosphatase-2B (calcineurin). J. Neurochem. 1994, 62:803-806.
30. Götz J., Lim Y.A., Ke Y.D., Eckert A., Ittner L.M. Dissecting toxicity of tau and beta-amyloid. Neurodegener. Dis. 2010, 7:10-12.
31. Grimm H.S., Beher D., Lichtenthaler S.F., Shearman M.S., Beyreuther K., Hartmann T. γ-Secretase cleavage site specificity differs for intracellular and secretory amyloid β. J. Biol. Chem. 2003, 278:13077-13085.
32. Gregori L., Hainfeld J.F., Simon M.N., Goldgaber D. Binding of amyloid beta protein to the 20 S proteasome. J. Biol. Chem. 1997, 272:58-62.
33. Grundke-Iqbal I., Iqbal K., Tung Y.C., Quinlan M., Wisniewski H.M., Binder L.I. Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:4913-4917.
34. Hardy J.A., Higgins G.A. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992, 256:184-185.
35. Haglund K., Dikic I. Ubiquitylation and cell signaling. EMBO J. 2005, 24:3353-3359.
36. Hanger D.P., Hughes K., Woodgett J.R., Brion J.P., Anderton B.H. Glycogen synthase kinase-3 induces Alzheimer's disease-like phosphorylation of tau: Generation of paired helical filament epitopes and neuronal localisation of the kinase. Neurosci. Lett. 1992, 147:58-62.
37. Han S.H., Kim Y.H., Mook-Jung I. RAGE: the beneficial and deleterious effects by diverse mechanisms of actions. Mol. Cell. 2011, 31:91-97.
38. Hartmann T., Bieger S.C., Bruhl B., Tienari P.J., Ida N., Allsop D., Roberts G.W., Masters C.L., Dotti C.G., Unsicker K., Beyreuther K. Distinct sites of intracellular production for Alzheimer's disease Aβ 40/42 amyloid peptides. Nat. Med. 1997, 3:1016-10120.
39. Higuchi M., Iwata N., Matsuba Y., Takano J., Suemoto T., Maeda J., Ji B., Ono M., Staufenbiel M., Suhara T., Saido T.C. Mechanistic involvement of the calpain-calpastatin system in Alzheimer neuropathology. FASEB J. 2011, 25:1-14.
40. Hollenbeck P.J. Phosphorylation of neuronal kinesin heavy and light chains in vivo. J. Neurochem. 1993, 60:2265-2275.
41. Iqbal K., Alonso Adel C., Chen S., Chohan M.O., El-Akkad E., Gong C.X., Khatoon S., Li B., Liu F., Rahman A., Tanimukai H., Grundke-Iqbal I. Tau pathology in Alzheimer disease and other tauopathies. Biochim. Biophys. Acta 2005, 1739:198-210.
42. Iqbal K., Grundke-Iqbal I. Molecular mechanism of alzheimer's neurofibrillary degeneration and therapeutic intervention. Ann. N. Y. Acad. Sci. 1996, 777:132-138.
43. Ishihara T., Hong M., Zhang B., Nakagawa Y., Lee M.K., Trojanowski J.Q., Lee V.M. Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 1999, 24:751-762.
44. Ittner A., Ke Y.D., van Eersel J., Gladbach A., Götz J., Ittner L.M. Brief update on different roles of tau in neurodegeneration. IUBMB Life. 2011, 63:495-502.
45. Kamal A., Almenar-Queralt A., LeBlanc J.F., Roberts E.A., Goldstein L.S. Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 2001, 414:643-648.
46. Keck S., Nitsch R., Grune T., Ullrich O. Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J. Neurochem. 2003, 85:115-122.
47. Keller J.N., Hanni K.B., Markesbery W.R. Impaired proteasome function in Alzheimer's disease. J. Neurochem. 2000, 75:436-439.
48. Khatoon S., Grundke-Iqbal I., Iqbal K. Levels of normal and abnormally phosphorylated tau in different cellular and regional compartments of Alzheimer disease and control brains. FEBS Lett. 1994, 351:80-84.
49. Kimberly W.T., Zheng J.B., Town T., Flavell R.A., Selkoe D.J. Physiological regulation of the β-amyloid precursor protein signaling domain by c-Jun N-terminal kinase JNK3 during neuronal differentiation. J. Neurosci. 2005, 25:5533-5543.
50. Kinoshita A., Fukumoto H., Shah T., Whelan C.M., Irizarry M.C., Hyman B.T. Demonstration by FRET of BACE interaction with the amyloid precursor protein at the cell surface and in early endosomes. J. Cell Sci. 2003, 16:3339-3346.
51. Kirschenbaum F., Hsu S.C., Cordell B., McCarthy J.V. Substitution of a glycogen synthase kinase-3beta phosphorylation site in presenilin 1 separates presenilin function from beta-catenin signaling. J. Biol. Chem. 2001, 276:7366-7375.
52. Koo E.H., Sisodia S.S., Archer D.R., Martin L.J., Weidemann A., Beyreuther K., Fischer P., Masters C.L., Price D.L. Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:1561-1565.
53. Koo E.H., Squazzo S.L. Evidence that production and release of amyloid β protein involves the endocytic pathway. J. Biol. Chem. 1994, 269:17386-17389.
54. Kumar S., Walter J. Phosphorylation of amyloid beta (Aβ) peptides- A trigger for formation of toxic aggregates in Alzheimer's disease. Aging 2011, 3:803-812.
55. Ladner C.J., Czech J., Maurice J., Lorens S.A., Lee J.M. Reduction of calcineurin enzymatic activity in Alzheimer's disease: correlation with neuropathologic changes. J. Neuropathol. Exp. Neurol. 1996, 55:924-931.
56. LaFerla F.M., Oddo S. Alzheimer's disease: Ab, tau and synaptic dysfunction. Trends Mol. Med. 2005, 11:170-176.
57. LaFerla F.M., Green K.N., Oddo S. Intracellular amyloid-β in Alzheimer's disease. Nat. Rev. Neurosci. 2007, 8:499-509.
58. Lazarov O., Lee M., Peterson D.A., Sisodia S.S. Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J. Neurosci. 2002, 22:9785-9793.
59. Lazarov O., Morfini G.A., Lee E.B., Farah M.H., Szodorai A., DeBoer S.R., Koliatsos V.E., Kins S., Lee V.M., Wong P.C., Price D.L., Brady S.T., Sisodia S.S. Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: revisited. J. Neurosci. 2005, 25:2386-2395.
60. Lee K.Y., Clark A.W., Rosales J.L., Chapman K., Fung T., Johnston R.N. Elevated neuronal Cdc2-like kinase activity in the Alzheimer disease brain. Neurosci. Res. 1999, 1:21-29.
61. Lee T.H., Pastorino L., Lu K.P. Peptidyl-prolyl cis-trans isomerase Pin1 in ageing, cancer and Alzheimer disease. Expert. Rev. Mol. Med. 2011, 13:e21.
62. Lee M.S., Kao S.C., Lemere C.A., Xia W., Tseng H.C., Zhou Y., Neve R., Ahlijanian M.K., Tsai L.H. APP processing is regulated by cytoplasmic phosphorylation. J. Cell Biol. 2003, 163:83-95.
63. Lee S.J., Liyanage U., Bickel P.E., Xia W., Lansbury P.T., Kosik K.S. A detergent-insoluble membrane compartment contains Aβ in vivo. Nat. Med. 1998, 4:730-734.
64. Lewis J., Dickson D.W., Lin W.L., Chisholm L., Corral A., Jones G., Yen S.H., Sahara N., Skipper L., Yager D., Eckman C., Hardy J., Hutton M., McGowan E. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 2001, 293:1487-1491.
65. Lin H., Lin T.Y., Juang J.L. c-Abl deregulates Cdk5 kinase activity and subcellular localization in Drosophila neurodegeneration. Cell Death Differ. 2007, 14:607-615.
66. Li Y., Liu L., Barger S.W., Griffin W.S. Interleukin-1 mediates pathological effects of microglia on tau phosphorylation and on synaptophysin synthesis in cortical neurons through a p38-MAPK pathway. J. Neurosci. 2003, 23:1605-1611.
67. Li X.H., Lv B.L., Xie J.Z., Liu J., Zhou X.W., Wang J.Z. AGEs induce Alzheimer-like tau pathology and memory deficit via RAGE-mediated GSK-3 activation. Neurobiol. Aging 2011, 1-11.
68. Ma S.L., Pastorino L., Zhou X.Z., Lu K.P. Prolyl isomerase Pin1 promotes amyloid precursor protein (APP) turnover by inhibiting glycogen synthase kinase-3β (GSK3β) activity: novel mechanism for Pin1 to protect against Alzheimer disease. J. Biol. Chem. 2012, 287:6969-6973.
69. Mandelkow E.M., Thies E., Trinczek B., Biernat J., Mandelkow E. MARK/PAR1 kinase is a regulator of microtubule-dependent transport in axons. J. Cell Biol. 2004, 167:99-110.
70. Mattson M.P., Goodman Y. Different amyloidogenic peptides share a similar mechanism of nerutoxicity involving reactive oxygen species and calcium. Brain Res. 1995, 676:219-224.
71. Mazzitelli S., Xu P., Ferrer I., Davis R.J., Tournier C. The loss of c-Jun N-terminal protein kinase activity prevents the amyloidogenic cleavage of amyloid precursor protein and the formation of amyloid plaques in vivo. J. Neurosi. 2011, 31:16969-16976.
72. Melov S., Adlard P.A., Morten K., Johnson F., Golden T.R., Hinerfeld D., Schilling B., Mavros C., Masters C.L., Volitakis I., Li Q.X., Laughton K., Hubbard A., Cherny R.A., Gibson B., Bush A.I. Mitochondrial oxidative stress causes hyperphosphorylation of tau. PLoS One 2007, 2:e536.
73. Mizuguchi M., Ikeda K., Kim S.U. Differential distribution of cellular forms of β-amyloid precursor protein in murine glial cell cultures. Brain Res. 1992, 84:219-225.
74. Morishima-Kawashima M., Hasegawa M., Takio K., Suzuki M., Yoshida H., Watanabe A., Titani K., Ihara Y. Hyperphosphorylation of tau in PHF. Neurobiol. Aging 1995, 16:365-380.
75. 1-42 in neurons is facilitated by the α7 nicotinic acetylcholine receptor in Alzheimer's disease. Neuroscience 2002, 110:199-211.
76. Nakamura K., Greenwood A., Binder L., Bigio E.H., Denial S., Nicholson L., Zhou X.Z., Lu K.P. Proline isomer-specific antibodies reveal the early pathogenic tau conformation in Alzheimer's disease. Cell 2012, 149:232-244.
77. Noble W., Planel E., Zehr C., Olm V., Meyerson J., Suleman F., Gaynor K., Wang L., LaFrancois J., Feinstein B., Burns M., Krishnamurthy P., Wen Y., Bhat R., Lewis J., Dickson D., Duff K. Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:6990-6995.
78. Noble W., Garwood C., Stephenson J., Kinsey A.M., Hanger D.P., Anderton B.H. Minocycline reduces the development of abnormal tau species in models of Alzheimer's disease. FASEB J. 2009, 23:739-750.
79. Nguyen K.C., Rosales J.L., Barboza M., Lee K.Y. Controversies over p25 in Alzheimer's disease. J. Alzheimers Dis. 2002, 2:123-126.
80. Oddo S., Caccamo A., Kitazawa M., Tseng B.P., LaFerla F.M. Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol. Aging 2003, 24:1063-1070.
81. Oddo S., Caccamo A., Cheng D., Jouleh B., Torp R., LaFerla F.M. Genetically augmenting tau levels does not modulate the onset or progression of Abeta pathology in transgenic mice. J. Neurochem. 2007, 102:1053-1063.
82. Oddo S., Billings L., Kesslak J.P., Cribbs D.H., LaFerla F.M. Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 2004, 43:321-332.
83. Oh S., Hong H.S., Hwang E., Sim H.J., Lee W., Shin S.J., Mook-Jung I. Amyloid peptide attenuates the proteasome activity in neuronal cells. Mech. Ageing Dev. 2005, 126:1292-1299.
84. Perez M., Hernandez F., Lim F., Diaz-Nido J., Avila J. Chronic lithium treatment decreases mutant tau protein aggregation in a transgenic mouse model. J. Alzheimers Dis. 2003, 5:301-308.
85. Peterson D.W., Ando D.M., Taketa D.A., Zhou H., Dahlquist F.W., Lew J. No difference in kinetics of tau or histone phosphorylation by CDK5/p25 versus CDK5/p35 in vitro. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:2884-2889.
86. Petrucelli L., Dickson D., Kehoe K., Taylor J., Snyder H., Grover A., De Lucia M., McGowan E., Lewis J., Prihar G., Kim J., Dillmann W.H., Browne S.E., Hall A., Voellmy R., Tsuboi Y., Dawson T.M., Wolozin B., Hardy J., Hutton M. CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation. Hum. Mol Genet. 2005, 13:703-714.
87. Pigino G., Morfini G., Pelsman A., Mattson M.P., Brady S.T., Busciglio J. Alzheimer's presenilin 1 mutations impair kinesin-based axonal transport. J. Neurosci. 2003, 23:4499-4508.
88. Ploia C., Sclip A., Colombo A., Repici M., Gardoni F., Luca M.D., Forloni G., Antoniou X., Borsello T. Role of glycogen synthase kinase-3β in APP hyperphosphorylation induced by NMDA stimulation in cortical neurons. Pharmaceuticals 2010, 3:42-58.
89. Quintanilla R.A., Orellana D.I., Gonzalez-Billault C., Maccioni R.B. Interleukin-6 induces Alzheimer-type phosphorylation of tau protein by deregulating the cdk5/p35 pathway. Exp. Cell Res. 2004, 295:245-257.
90. Rapoport S.I. Hydrogen magnetic resonance spectroscopy in Alzheimer's disease. Lancet Neurol. 2002, 1:82.
91. Resende R., Ferreiro E., Pereira C., Oliveira C.R. ER stress is involved in Abeta-induced GSK-3beta activation and tau phosphorylation. J. Neurosci. Res. 2008, 86:2091-2099.
92. Ribe E.M., Perez M., Puig B., Gich I., Lim F., Cuadrado M., Sesma T., Catena S., Sánchez B., Nieto M., Gómez-Ramos P., Morán M.A., Cabodevilla F., Samaranch L., Ortiz L., Pérez A., Ferrer I., Avila J., Gómez-Isla T. Accelerated amyloid deposition, neurofibrillary degeneration and neuronal loss in double mutant APP/tau transgenic mice. Neurobiol. Dis. 2005, 20:814-822.
93. Rissman R.A., Poon W.W., Blurton-Jones M., Oddo S., Torp R., Vitek M.P., LaFerla F.M., Rohn T.T., Cotman C.W. Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J. Clin. Invest. 2004, 1141:121-130.
94. Roy S., Zhang B., Lee V.M., Trojanowski J.Q. Axonal transport defects: a common theme in neurodegenerative diseases. Acta Neuropathol. Berl. 2005, 109:5-13.
95. Sahara N., Murayama M., Mizoroki T., Urushitani M., Imai Y., Takahashi R., Murata S., Tanaka K., Takashima A. In vivo evidence of CHIP up-regulation attenuating tau aggregation. J. Neurochem. 2005, 94:1254-1263.
96. Schindowski K., Bretteville A., Leroy K., Begard S., Brion J.P., Hamdane M., Buée L. Alzheimer's disease-like tau neuropathology leads to memory deficits and loss of functional synapses in a novel mutated tau transgenic mouse without any motor deficits. Am. J. Pathol. 2006, 169:599-616.
97. Shimura H., Schwartz D., Gygi S.P., Kosik K.S. CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J. Biol. Chem. 2004, 279:4869-4876.
98. Stamer K., Vogel R., Thies E., Mandelkow E., Mandelkow E.M. Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J. Cell Biol. 2002, 156:1051-1063.
99. Standen C.L., Brownlees J., Grerson A.J., Kesavapany S., Lau K.F., McLoughlin D.M., Miller C.C. Phosphorylation of thr(668) in the cytoplasmic domain of the Alzheimer's disease amyloid precursor protein by stress-activated protein kinase 1b (Jun N-terminal kinase-3). J. Neurochem. 2001, 76:316-320.
100. Sun K.H., de Pablo Y., Vincent F., Shah K. Deregulated Cdk5 promotes oxidative stress and mitochondrial dysfunction. J. Neurochem. 2008, 107:265-278.
101. Susanne P.J., Pritchard A.V., Dolan G.V., Johnson W. The toxicity of tau in Alzheimer disease: turnover, targets and potential therapeutics. J. Cell Mol. Med. 2011, 20:1-15.
102. Tan J., Town T., Mori T., Wu Y., Saxe M., Crawford F., Mullan M. CD45 opposes beta-amyloid peptide-induced microglial activation via inhibition of p44/42 mitogen-activated protein kinase. J. Neurosci. 2000, 20:7587-7594.
103. Taru H., Iijima K., Hase M., Kirino Y., Yagi Y., Suzuki T. Interaction of Alzheimer's beta -amyloid precursor family proteins with scaffold proteins of the JNK signaling cascade. J. Biol. Chem. 2002, 277:20070-20078.
104. Texidó L., Martín-Satué M., Alberdi E., Solsona C., Matute C. Amyloid β peptide oligomers directly activate NMDA receptors. Cell Calcium 2011, 49:184-190.
105. Trojanowski J.Q., Lee V.M. Phosphorylation of paired helical filament tau in Alzheimer's disease neurofibrillary lesions: focusing on phosphatases. FASEB J. 1995, 9:1570-1576.
106. Tseng B.P., Green K.N., Chan J.L., Blurton-Jones M., LaFerla F.M. Abeta inhibits the proteasome and enhances amyloid and tau accumulation. Neurobiol. Aging 2007, 29:1607-1618.
107. Utton M.A., Noble W.J., Hill J.E., Anderton B.H., Hanger D.P. Molecular motors implicated in the axonal transport of tau and alphasynuclein. J. Cell Sci. 2005, 118:4645-4654.
108. Van Eldik L.J., Thompson W.L., Ralay R.H., Behanna H.A., Martin W.D. Glia proinflammatory cytokine upregulation as a therapeutic target for neurodegenerative diseases: function-based and target-based discovery approaches. Int. Rev. Neurobiol. 2007, 82:277-296.
109. Wang J.Z., Gong C.X., Zaidi T., Grundke-Iqbal I., Iqbal K. Dephosphorylation of Alzheimer paired helical filaments by protein phosphatase-2A and -2B. J. Biol. Chem. 1995, 270:4854-4860.
110. Wertkin A.M., Turner R.S., Pleasure S.J., Golde T.E., Younkin S.G., Trojanowski J.Q., Lee V.M. Human neurons derived from a teratocarcinoma cell line express solely the 695-amino acid amyloid precursor protein and produce intracellular β-amyloid or A4 peptides. Proc. Natl. Acad. Sci. U. S. A. 1993, 901:9513-9517.
111. Wild-Bode C., Yamazaki T., Capell A., Leimer U., Steiner H., Ihara Y., Haass C. Intracellular generation and accumulation of amyloid beta-peptide terminating at amino acid 42. J. Biol. Chem. 1997, 272:16085-16088.
112. Yazawa H., Yu Z.X., Takeda L.Y., Gong W., Ferrans V.J., Oppenheim J.J., Li C.C., Wang J.M. β-amyloid peptide (Aβ42) is internalized via the G-protein-coupled receptor FPRL1 and forms fibrillar aggregates in macrophages. FASEB J. 2001, 15:2454-2462.
113. Yan R., Han P., Miao H., Greengard P., Xu H. The transmembrane domain of the Alzheimer's beta-secretase (BACE1) determines its late Golgi localization and access to beta-amyloid precursor protein (APP) substrate. J. Biol. Chem. 2001, 276:36788-36796.
114. Yao X.Q., Zhang X.X., Yin Y.Y., Liu B., Luo D.J., Liu D., Chen N.N., Ni Z.F., Wang X., Wang Q., Wang J.Z., Liu G.P. Glycogen synthase kinase-3β regulates Tyr307 phosphorylation of protein phosphatase-2A via protein tyrosine phosphatase 1B but not Src. Biochem. J. 2011, 437:335-344.
115. Zhang B., Higuchi M., Yoshiyama Y., Ishihara T., Forman M.S., Martinez D., Joyce S., Trojanowski J.Q., Lee V.M.Y. Retarded axonal transport of R406W mutant tau in transgenic mice with a neurodegenerative taupathy. J. Neurosci. 2004, 24:4657-4667.
116. Zhongtao Z., Lee Z., Mandiyan C.H., Borg V., Margolis J.P., Schlessinger B., Kuriyan J. Sequence-specific recognition of the internalization motif of the Alzheimer's amyloid precursor protein by the X11 PTB domain. J. EMBO 1997, 16:6141-6150.
117. Zukerberg L.R., Patrick G.N., Nikolic M., Humbert S., Wu C.L., Lanier L.M., Gertler F.B., Vidal M., Van Etten R.A., Tsi L.H. Cables links Cdk5 and c-Abl and facilitates Cdk5 tyrosine phosphorylation, kinase upregulation, and neurite outgrowth. Neuron 2000, 26:633-646.