Tauopathies

Cellular and Molecular Life Sciences

Volumn 64, Issue 17, 2007, Pages 2219-2233

  Hernandez F ^a   Avila, J ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Alzheimer's disease; FTDP 17; Paired helical filaments; Tau; Tauopathies

Indexed keywords

DOXYCYCLINE; LITHIUM; MINOCYCLINE; PROTEIN INHIBITOR; TAU PROTEIN;

ALZHEIMER DISEASE; BIPOLAR DEPRESSION; DEGENERATIVE DISEASE; DEMENTIA; DOWN SYNDROME; HUMAN; MISSENSE MUTATION; NERVE FIBER TRANSPORT; NEUROTOXICITY; NIEMANN PICK DISEASE; PARKINSONISM; PICK PRESENILE DEMENTIA; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REVIEW;

ALZHEIMER DISEASE; HUMANS; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; TAU PROTEINS; TAUOPATHIES;

EID: 34548301393     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-007-7220-x     Document Type: Review

References (210)

1. Avila, J., Lucas, J. J., Perez, M. and Hernandez, F. (2004) Role of tau protein in both physiological and pathological conditions. Physiol. Rev. 84, 361-384.
2. Goedert, M., Spillantini, M. G., Potier, M. C., Ulrich, J. and Crowther, R. A. (1989) Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain. EMBO J. 8, 393-399.
3. Himmler, A. (1989) Structure of the bovine tau gene: alternatively spliced transcripts generate a protein family. Mol. Cell. Biol. 9, 1389-1396.
4. Lee, G., Cowan, N. and Kirschner, M. (1988) The primary structure and heterogeneity of tau protein from mouse brain. Science 239, 285-288.
5. Drubin, D. G. and Kirschner, M. W. (1986) Tau protein function in living cells. J. Cell. Biol. 103, 2739-2746.
6. Arrasate, M., Perez, M. and Avila, J. (2000) Tau dephosphorylation at tau-1 site correlates with its association to cell membrane [In Process Citation]. Neurochem. Res. 25, 43-50.
7. Maas, T., Eidenmuller, J. and Brandt, R. (2000) Interaction of tau with the neural membrane cortex is regulated by phosphorylation at sites that are modified in paired helical filaments. J. Biol. Chem. 275, 15733-15740.
8. Grundke, I. I., Iqbal, K., Quinlan, M., Tung, Y. C., Zaidi, M. S. and Wisniewski, H. M. (1986) Microtubule-associated protein tau: a component of Alzheimer paired helical filaments. J. Biol. Chem. 261, 6084-6089.
9. Wood, J. G., Mirra, S. S., Pollock, N. J. and Binder, L. I. (1986) Neurofibrillary tangles of Alzheimer disease share antigenic determinants with the axonal microtubule-associated protein tau (tau) [published erratum appears in Proc. Natl. Acad. Sci. USA 1986 Dec;83(24):9773]. Proc. Natl. Acad. Sci. USA 83, 4040-4043.
10. Kosik, K. S., Joachim, C. L. and Selkoe, D. J. (1986) Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc. Natl. Acad. Sci. USA 83, 4044-4048.
11. Ihara, Y., Nukina, N., Miura, R. and Ogawara, M. (1986) Phosphorylated tau protein is integrated into paired helical filaments in Alzheimer's disease. J. Biochem. (Tokyo) 99, 1807-1810.
12. Wischik, C. M., Novak, M., Edwards, P. C., Klug, A., Tichelaar, W. and Crowther, R. A. (1988) Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc. Natl. Acad. Sci. USA 85, 4884-4888.
13. Goedert, M., Wischik, C. M., Crowther, R. A., Walker, J. E. and Klug, A. (1988) Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: identification as the microtubule-associated protein tau. Proc. Natl. Acad. Sci. USA 85, 4051-4055.
14. Montejo de Garcini, E., Serrano, L. and Avila, J. (1986) Self assembly of microtubule associated protein tau into filaments resembling those found in Alzheimer disease. Biochem. Biophys. Res. Commun. 141, 790-796.
15. Wolozin, B. L., Pruchnicki, A., Dickson, D. W. and Davies, P. (1986) A neuronal antigen in the brains of Alzheimer patients. Science 232, 648-650.
16. Lee, V. M., Balin, B. J., Otvos, L., Jr. and Trojanowski, J. Q. (1991) A68: a major subunit of paired helical filaments and derivatized forms of normal Tau. Science 251, 675-678.
17. Grundke, I. I., Iqbal, K., Tung, Y. C., Quinlan, M., Wisniewski, H. M. and Binder, L. I. (1986) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. USA 83, 4913-4917.
18. Buee, L., Bussiere, T., Buee-Scherrer, V., Delacourte, A. and Hof, P. R. (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res. Brain Res. Rev. 33, 95-130.
19. Andreadis, A., Brown, W. M. and Kosik, K. S. (1992) Structure and novel exons of the human tau gene. Biochemistry 31, 10626-10633.
20. Neve, R. L., Harris, P., Kosik, K. S., Kurnit, D. M. and Donlon, T. A. (1986) Identification of cDNA clones for the human microtubule-associated protein tau and chromosomal localization of the genes for tau and microtubule-associated protein 2. Brain Res. 387, 271-280.
21. Sadot, E., Heicklenklein, A., Barg, J., Lazarovici, P. and Ginzburg, I. (1996) Identification of a tau promoter region mediating tissue-specific- regulated expression in PC12 cells. J. Mol. Biol. 256, 805-812.
22. D'souza, I., Yu, C.-E. and McMilan, P. (2006) A natural antisense gene regulates MAPT expression. Alzheimer Dementia 2, S29.
23. Andreadis, A., Broderick, J. A. and Kosik, K. S. (1995) Relative exon affinities and suboptimal splice site signals lead to non-equivalence of two cassette exon. Nucleic Acids Res. 23, 3585-3593.
24. Couchie, D., Mavilia, C., Georgieff, I. S., Liem, R. K., Shelanski, M. L. and Nunez, J. (1992) Primary structure of high molecular weight tau present in the peripheral nervous system. Proc. Natl. Acad. Sci. USA 89, 4378-4381.
25. Goedert, M., Spillantini, M. G. and Crowther, R. A. (1992) Cloning of a big tau microtubule-associated protein characteristic of the peripheral nervous system. Proc. Natl. Acad. Sci. USA 89, 1983-1987.
26. Kosik, K. S., Orecchio, L. D., Bakalis, S. and Neve, R. L. (1989) Developmentally regulated expression of specific tau sequences. Neuron 2, 1389-1397.
27. Goedert, M., Spillantini, M. G., Jakes, R., Rutherford, D. and Crowther, R. A. (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3, 519-526.
28. Brion, J. P., Smith, C., Couck, A. M., Gallo, J. M. and Anderton, B. H. (1993) 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, 2071-2080.
29. Bramblett, G. T., Goedert, M., Jakes, R., Merrick, S. E., Trojanowski, J. Q. and Lee, V. M. (1993) Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10, 1089-1099.
30. Goedert, M., Jakes, R., Crowther, R. A., Six, J., Lubke, U., Vandermeeren, M., Cras, P., Trojanowski, J. Q. and Lee, V. M. (1993) The abnormal phosphorylation of tau protein at Ser-202 in Alzheimer disease recapitulates phosphorylation during development. Proc. Natl. Acad. Sci. USA 90, 5066-5070.
31. Arioka, M., Tsukamoto, M., Ishiguro, K., Kato, R., Sato, K., Imahori, K. and Uchida, T. (1993) Tau protein kinase II is involved in the regulation of the normal phosphorylation state of tau protein. J. Neurochem. 60, 461-468.
32. Matsuo, E. S., Shin, R. W., Billingsley, M. L., Van deVoorde, A., O'Connor, M., Trojanowski, J. Q. and Lee, V. M. (1994) Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron 13, 989-1002.
33. Garver, T. D., Harris, K. A., Lehman, R. A. W., Lee, V. M. Y., Trojanowski, J. Q. and Billingsley, M. L. (1994) tau Phosphorylation in human, primate, and rat brain: Evidence that a pool of tau is highly phosphorylated in vivo and is rapidly dephosphorylated in vitro. J. Neurochem. 63, 2279-2287.
34. Grover, A., Houlden, H., Baker, M., Adamson, J., Lewis, J., Prihar, G., PickeringBrown, S., Duff, K. and Hutton, M. (1999) 5' splice site mutations in tau associated with the inherited dementia FTDP-17 affect a stem-loop structure that regulates alternative splicing of exon 10. J. Biol. Chem. 274, 15134-15143.
35. Hutton, M., Lendon, C. L., Rizzu, P., Baker, M., Froelich, S., Houlden, H., PickeringBrown, S., Chakraverty, S., Isaacs, A., Grover, A. et al. (1998) Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393, 702-705.
36. Spillantini, M. G., Murrell, J. R., Goedert, M., Farlow, M. R., Klug, A. and Ghetti, B. (1998) Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc. Natl. Acad. Sci. USA 95, 7737-7741.
37. Varani, L., Hasegawa, M., Spillantini, M. G., Smith, M. J., Murrell, J. R., Ghetti, B., Klug, A., Goedert, M. and Varani, G. (1999) Structure of tau exon 10 splicing regulatory element RNA and destabilization by mutations of frontotemporal dementia and parkinsonism linked to chromosome 17. Proc. Natl. Acad. Sci. USA 96, 8229-8234.
38. Heutink, P. (2000) Untangling tau-related dementia. Hum. Mol. Genet. 9, 979-986.
39. Rizzu, P., VanSwieten, J. C., Joosse, M., Hasegawa, M., Stevens, M., Tibben, A., Niermeijer, M. F., Hillebrand, M., Ravid, R., Oostra, B. A. et al. (1999) High prevalence of mutations in the microtubule-associated protein tau in a population study of frontotemporal dementia in the Netherlands. Am. J. Hum. Genet. 64, 414-421.
40. Lippa, C. F., Zhukareva, V., Kawarai, T., Uryu, K., Shafiq, M., Nee, L. E., Grafman, J., Liang, Y., St George-Hyslop, P. H., Trojanowski, J. Q. et al. (2000) Frontotemporal dementia with novel tau pathology and a Glu342Val tau mutation. Ann. Neurol. 48, 850-858.
41. Sergeant, N., David, J. P., Lefranc, D., Vermersch, P., Wattez, A. and Delacourte, A. (1997) Different distribution of phosphorylated tau protein isoforms in Alzheimer's and Pick's diseases. FEBS Lett. 412, 578-582.
42. Glatz, D. C., Rujescu, D., Tang, Y., Berendt, F. J., Hartmann, A. M., Faltraco, F., Rosenberg, C., Hulette, C., Jellinger, K., Hampel, H. et al. (2006) The alternative splicing of tau exon 10 and its regulatory proteins CLK2 and TRA2-BETA1 changes in sporadic Alzheimer's disease. J. Neurochem. 96, 635-644.
43. DSouza, I., Poorkaj, P., Hong, M., Nochlin, D., Lee, V. M. Y., Bird, T. D. and Schellenberg, G. D. (1999) Missense and silent tau gene mutations cause frontotemporal dementia with parkinsonism-chromosome 17 type, by affecting multiple alternative RNA splicing regulatory elements. Proc. Natl. Acad. Sci. USA 96, 5598-5603.
44. Hasegawa, M., Smith, M. J., Iijima, M., Tabira, T. and Goedert, M. (1999) FTDP-17 mutations N279K and S305N in tau produce increased splicing of exon 10. FEBS Lett. 443, 93-96.
45. Jiang, Z., Tang, H., Havlioglu, N., Zhang, X., Stamm, S., Yan, R. and Wu, J. Y. (2003) Mutations in tau gene exon 10 associated with FTDP-17 alter the activity of an exonic splicing enhancer to interact with Tra2 beta. J. Biol. Chem. 278, 18997-19007.
46. Hernandez, F., Perez, M., Lucas, J. J., Mata, A. M., Bhat, R. and Avila, J. (2004) Glycogen synthase kinase-3 plays a crucial role in tau exon 10 splicing and intranuclear distribution of SC35. Implications for Alzheimer's disease. J. Biol. Chem. 279, 3801-3806.
47. Baker, M., Litvan, I., Houlden, H., Adamson, J., Dickson, D., PerezTur, J., Hardy, J., Lynch, T., Bigio, E. and Hutton, M. (1999) Association of an extended haplotype in the tau gene with progressive supranuclear palsy. Hum. Mol. Genet. 8, 711-715.
48. Evans, W., Fung, H. C., Steele, J., Eerola, J., Tienari, P., Pittman, A., Silva, R., Myers, A., Vrieze, F. W., Singleton, A. et al. (2004) The tau H2 haplotype is almost exclusively Caucasian in origin. Neurosci. Lett. 369, 183-185.
49. Di Maria, E., Tabaton, M., Vigo, T., Abbruzzese, G., Bellone, E., Donati, C., Frasson, E., Marchese, R., Montagna, P., Munoz, D. G., Pramstaller, P. P., Zanusso, G. et al. (2000) Corticobasal degeneration shares a common genetic background with progressive supranuclear palsy. Ann. Neurol. 47, 374-377.
50. Houlden, H., Baker, M., Morris, H. R., MacDonald, N., Pickering-Brown, S., Adamson, J., Lees, A. J., Rossor, M. N., Quinn, N. P., Kertesz, A. et al. (2001) Corticobasal degeneration and progressive supranuclear palsy share a common tau haplotype. Neurology 56, 1702-1706.
51. Pastor, P., Ezquerra, M., Tolosa, E., Munoz, E., Marti, M. J., Valldeoriola, F., Molinuevo, J. L., Calopa, M. and Oliva, R. (2002) Further extension of the H1 haplotype associated with progressive supranuclear palsy. Mov. Disord. 17, 550-556.
52. Kwok, J. B., Teber, E. T., Loy, C., Hallupp, M., Nicholson, G., Mellick, G. D., Buchanan, D. D., Silburn, P. A. and Schofield, P. R. (2004) Tau haplotypes regulate transcription and are associated with Parkinson's disease. Ann. Neurol. 55, 329-334.
53. Dantuma, N. P. and Masucci, M. G. (2002) Stabilization signals: a novel regulatory mechanism in the ubiquitin/proteasome system. FEBS Lett. 529, 22-26.
54. David, D. C., Layfield, R., Serpell, L., Narain, Y., Goedert, M. and Spillantini, M. G. (2002) Proteasomal degradation of tau protein. J. Neurochem. 83, 176-185.
55. Shimura, H., Schwartz, D., Gygi, S. P. and Kosik, K. S. (2004) CHIP-Hsc70 complex ubiquitinates phosphorylated tau and enhances cell survival. J. Biol. Chem. 279, 4869-4876.
56. Petrucelli, L., Dickson, D., Kehoe, K., Taylor, J., Snyder, H., Grover, A., De Lucia, M., McGowan, E., Lewis, J., Prihar, G. et al. (2004) CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation. Hum. Mol. Genet. 13, 703-714.
57. Dickey, C. A., Yue, M., Lin, W. L., Dickson, D. W., Dunmore, J. H., Lee, W. C., Zehr, C., West, G., Cao, S., Clark, A. M. et al. (2006) Deletion of the ubiquitin ligase CHIP leads to the accumulation, but not the aggregation, of both endogenous phospho- and caspase-3-cleaved tau species. J. Neurosci. 26, 6985-6996.
58. Sherman, M. Y. and Goldberg, A. L. (2001) Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases. Neuron 29, 15-32.
59. Hernandez, F., Diaz-Hernandez, M., Avila, J. and Lucas, J. J. (2004) Testing the ubiquitin-proteasome hypothesis of neurodegeneration in vivo. Trends Neurosci. 27, 66-69.
60. Keller, J. N., Hanni, K. B. and Markesbery, W. R. (2000) Impaired proteasome function in Alzheimer's disease. J. Neurochem. 75, 436-439.
61. Morishima-Kawashima, M., Hasegawa, M., Takio, K., Suzuki, M., Titani, K. and Ihara, Y. (1993) Ubiquitin is conjugated with amino-terminally processed tau in paired helical filaments. Neuron 10, 1151-1160.
62. Cripps, D., Thomas, S. N., Jeng, Y., Yang, F., Davies, P. and Yang, A. J. (2006) Alzheimer disease-specific conformation of hyperphosphorylated paired helical filament-Tau is polyubiquitinated through Lys-48, Lys-11, and Lys-6 ubiquitin conjugation. J. Biol. Chem. 281, 10825-10838.
63. Keck, S., Nitsch, R., Grune, T. and Ullrich, O. (2003) Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J. Neurochem. 85, 115-122.
64. Rohn, T. T., Rissman, R. A., Davis, M. C., Kim, Y. E., Cotman, C. W. and Head, E. (2002) Caspase-9 activation and caspase cleavage of tau in the Alzheimer's disease brain. Neurobiol. Dis. 11, 341-354.
65. Gamblin, T. C., Chen, F., Zambrano, A., Abraha, A., Lagalwar, S., Guillozet, A. L., Lu, M., Fu, Y., Garcia-Sierra, F., LaPointe, N. et al. (2003) Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc. Natl. Acad. Sci. USA 100, 10032-10037.
66. Litersky, J. M. and Johnson, G. V. (1995) Phosphorylation of tau in situ: inhibition of calcium-dependent proteolysis. J. Neurochem. 65, 903-911.
67. Kenessey, A., Nacharaju, P., Ko, L. W. and Yen, S. H. (1997) Degradation of tau by lysosomal enzyme cathepsin D: implication for Alzheimer neurofibrillary degeneration. J. Neurochem. 69, 2026-2038.
68. Lim, F., Hernandez, F., Lucas, J. J., Gomez-Ramos, P., Moran, M. A. and Avila, J. (2001) FTDP-17 mutations in tau transgenic mice provoke lysosomal abnormalities and Tau filaments in forebrain. Mol. Cell. Neurosci. 18, 702-714.
69. Karsten, S. L., Sang, T. K., Gehman, L. T., Chatterjee, S., Liu, J., Lawless, G. M., Sengupta, S., Berry, R. W., Pomakian, J., Oh, H. S. et al. (2006) A genomic screen for modifiers of tauopathy identifies puromycin-sensitive aminopeptidase as an inhibitor of tau-induced neurodegeneration. Neuron 51, 549-560.
70. Kosik, K. S. and Shimura, H. (2005) Phosphorylated tau and the neurodegenerative foldopathies. Biochim. Biophys. Acta 1739, 298-310.
71. Baudier, J., Lee, S. H. and Cole, R. D. (1987) Separation of the different microtubule-associated tau protein species from bovine brain and their mode II phosphorylation by Ca2+/phospholipid-dependent protein kinase, C. J. Biol. Chem. 262, 17584-17590.
72. Imahori, K. and Uchida, T. (1997) Physiology and pathology of tau protein kinases in relation to Alzheimer's disease. J. Biochem. (Tokyo) 121, 179-188.
73. Goedert, M., Hasegawa, M., Jakes, R., Lawler, S., Cuenda, A. and Cohen, P. (1997) Phosphorylation of microtubule-associated protein tau by stress-activated protein kinases. FEBS Lett. 409, 57-62.
74. Correas, I., Diaz, N. J. and Avila, J. (1992) Microtubule-associated protein tau is phosphorylated by protein kinase C on its tubulin binding domain. J. Biol. Chem. 267, 15721-15728.
75. Drewes, G., Lichtenberg, K. B., Doring, F., Mandelkow, E. M., Biernat, J., Goris, J., Doree, M. and Mandelkow, E. (1992) Mitogen activated protein (MAP) kinase transforms tau protein into an Alzheimer-like state. EMBO J. 11, 2131-2138.
76. Baudier, J. and Cole, R. D. (1987) Phosphorylation of tau proteins to a state like that in Alzheimer's brain is catalyzed by a calcium/calmodulin- dependent kinase and modulated by phospholipids. J. Biol. Chem. 262, 17577-17583.
77. Scott, C. W., Spreen, R. C., Herman, J. L., Chow, F. P., Davison, M. D., Young, J. and Caputo, C. B. (1993) Phosphorylation of recombinant tau by cAMP-dependent protein kinase. Identification of phosphorylation sites and effect on microtubule assembly. J. Biol. Chem. 268, 1166-1173.
78. Hanger, D. P., Hughes, K., Woodgett, J. R., Brion, J. P. and Anderton, B. H. (1992) 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. 147, 58-62.
79. Lucas, J. J., Hernandez, F., Gomez-Ramos, P., Moran, M. A., Hen, R. and Avila, J. (2001) Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J. 20, 27-39.
80. Sato, S., Cerny, R. L., Buescher, J. L. and Ikezu, T. (2006) Tautubulin kinase 1 (TTBK1), a neuron-specific tau kinase candidate, is involved in tau phosphorylation and aggregation. J. Neurochem. 98, 1573-1584.
81. Yoshida, H. and Goedert, M. (2006) Sequential phosphorylation of tau protein by cAMP-dependent protein kinase and SAPK4/p38delta or JNK2 in the presence of heparin generates the AT100 epitope. J. Neurochem. 99, 154-164.
82. Li, T., Hawkes, C., Qureshi, H. Y., Kar, S. and Paudel, H. K. (2006) Cyclin-dependent protein kinase 5 primes microtubule-associated protein tau site-specifically for glycogen synthase kinase 3beta. Biochemistry 45, 3134-3145.
83. Plattner, F., Angelo, M. and Giese, K. P. (2006) The roles of cyclin-dependent kinase 5 and glycogen synthase kinase 3 in tau hyperphosphorylation. J. Biol. Chem. 281, 25457-25465.
84. Lee, G., Thangavel, R., Sharma, V. M., Litersky, J. M., Bhaskar, K., Fang, S. M., Do, L. H., Andreadis, A., Van Hoesen, G. and Ksiezak-Reding, H. (2004) Phosphorylation of tau by fyn: implications for Alzheimer's disease. J. Neurosci. 24, 2304-2312.
85. Bhaskar, K., Yen, S. H. and Lee, G. (2005) Disease-related modifications in tau affect the interaction between Fyn and Tau. J. Biol. Chem. 280, 35119-35125.
86. Williamson, R., Scales, T., Clark, B. R., Gibb, G., Reynolds, C. H., Kellie, S., Bird, I. N., Varndell, I. M., Sheppard, P. W., Everall, I. et al. (2002) Rapid tyrosine phosphorylation of neuronal proteins including tau and focal adhesion kinase in response to amyloid-beta peptide exposure: involvement of Src family protein kinases. J. Neurosci. 22, 10-20.
87. Derkinderen, P., Scales, T. M., Hanger, D. P., Leung, K. Y., Byers, H. L., Ward, M. A., Lenz, C., Price, C., Bird, I. N., Perera, T. et al. (2005) 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, 6584-6593.
88. Reynolds, M. R., Reyes, J. F., Fu, Y., Bigio, E. H., Guillozet-Bongaarts, A. L., Berry, R. W. and Binder, L. I. (2006) Tau nitration occurs at tyrosine 29 in the fibrillar lesions of Alzheimer's disease and other tauopathies. J. Neurosci. 26, 10636-10645.
89. Geddes, J. F., Hughes, A. J., Lees, A. J. and Daniel, S. E. (1993) Pathological overlap in cases of parkinsonism associated with neurofibrillary tangles. A study of recent cases of postencephalitic parkinsonism and comparison with progressive supranuclear palsy and Guamanian parkinsonism-dementia complex. Brain 116 (Pt 1), 281-302.
90. Goedert, M., Cohen, E. S., Jakes, R. and Cohen, P. (1992) p42 map kinase phosphorylation sites in microtubule-associated protein tau are dephosphorylated by protein phosphatase 2A1. Implications for Alzheimer's disease. FEBS Lett. 312, 95-99.
91. Iqbal, K., Alonso, A. D., Gong, C. X., Khatoon, S., Pei, J. J., Wang, J. Z. and GrundkeIqbal, I. (1997) Tauphosphatases. In: Brain Microtubule Associated Proteins, pp. 95-111, Avila, J., Brandt, R. and Kosik, K. S. (eds.), Harwood, Chur, Switzerland.
92. Szucs, K., Ledesma, M. D., Dombradi, V., Gergely, P., Avila, J. and Friendrich, P. (1994) Dephosphorylation of tau protein from Alzheimers disease patients. Neurosci. Lett. 165, 175-178.
93. Yamamoto, H., Hasegawa, M., Ono, T., Tashima, K., Ihara, Y. and Miyamoto, E. (1995) Dephosphorylation of fetal-tau and paired helical filaments-tau by protein phosphatases 1 and 2A and calcineurin. J Biochem (Tokyo) 118, 1224-1231.
94. Gong, C. X., Grundke-Iqbal, I. and Iqbal, K. (1994) Dephosphorylation of Alzheimer's disease abnormally phosphorylated tau by protein phosphatase-2A. Neuroscience 61, 765-772.
95. Gong, C. X., Singh, T. J., Grundkeiqbal, I. and Iqbal, K. (1994) Alzheimers disease abnormally phosphorylated tau is dephosphorylated by protein phosphatase-2B (Calcineurin). J. Neurochem. 62, 803-806.
96. Gong, C. X., Grundkeiqbal, I., Damuni, Z. and Iqbal, K. (1994) Dephosphorylation of microtubule-associated protein tau by protein phosphatase-1 and -2C and its implication in Alzheimer disease. FEBS Lett. 341, 94-98.
97. Goedert, M., Jakes, R., Qi, Z., Wang, J. H. and Cohen, P. (1995) Protein phosphatase 2A is the major enzyme in brain that dephosphorylates tau protein phosphorylated by proline-directed protein kinases or cyclic AMP-dependent protein kinase. J. Neurochem. 65, 2804-2807.
98. Gong, C. X., Lidsky, T., Wegiel, J., Zuck, L., Grundke-Iqbal, I. and Iqbal, K. (2000) Phosphorylation ofmicrotubule-associated protein tau is regulated by protein phosphatase 2A in mammalian brain. Implications for neurofibrillary degeneration in Alzheimer's disease. J. Biol. Chem. 275, 5535-5544.
99. Sontag, E., NunbhakdiCraig, V., Lee, G., Brandt, R., Kamibayashi, C., Kuret, J., White, C. L., Mumby, M. C. and Bloom, G. S. (1999) Molecular interactions among protein phosphatase 2A, tau, and microtubules-implications for the regulation of tau phosphorylation and the development of tauopathies. J. Biol. Chem. 274, 25490-25498.
100. Goedert, M., Satumtira, S., Jakes, R., Smith, M. J., Kamibayashi, C., White, C. L., 3rd and Sontag, E. (2000) Reduced binding of protein phosphatase 2A to tau protein with frontotemporal dementia and parkinsonism linked to chromosome 17 mutations. J. Neurochem. 75, 2155-2162.
101. Planel, E., Miyasaka, T., Launey, T., Chui, D. H., Tanemura, K., Sato, S., Murayama, O., Ishiguro, K., Tatebayashi, Y. and Takashima, A. (2004) Alterations in glucose metabolism induce hypothermia leading to tau hyperphosphorylation through differential inhibition of kinase and phosphatase activities: implications for Alzheimer's disease. J. Neurosci. 24, 2401-2411.
102. Butterfield, D. A., Abdul, H. M., Opii, W., Newman, S. F., Joshi, G., Ansari, M. A. and Sultana, R. (2006) Pin1 in Alzheimer's disease. J. Neurochem. 98, 1697-1706.
103. Bhat, R. V., Budd Haeberlein, S. L. and Avila, J. (2004) Glycogen synthase kinase 3: a drug target for CNS therapies. J. Neurochem. 89, 1313-1317.
104. Klein, P. S. and Melton, D. A. (1996) A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. USA 93, 8455-8459.
105. Alvarez, G., MunozMontano, J. R., Satrustegui, J., Avila, J., Bogonez, E. and DiazNido, J. (1999) Lithium protects cultured neurons against beta-amyloid-induced neurodegeneration. FEBS Lett. 453, 260-264.
106. MunozMontano, J. R., Moreno, F. J., Avila, J. and DiazNido, J. (1997) Lithium inhibits Alzheimer's disease-like tau protein phosphorylation in neurons. FEBS Lett. 411, 183-188.
107. MunozMontano, J. R., Moreno, F. J., Avila, J. and DiazNido, J. (1999) Downregulation of glycogen synthase kinase-3 beta (GSK-3 beta) protein expression during neuroblastoma IMR-32 cell differentiation. J. Neurosci. Res. 55, 278-285.
108. Chen, R. W. and Chuang, D. M. (1999) Long term lithium treatment suppresses p53 and Bax expression but increases Bcl-2 expression. A prominent role in neuroprotection against excitotoxicity. J. Biol. Chem. 274, 6039-6042.
109. King, T. D., Bijur, G. N. and Jope, R. S. (2001) Caspase-3 activation induced by inhibition of mitochondrial complex I is facilitated by glycogen synthase kinase-3beta and attenuated by lithium. Brain Res. 919, 106-114.
110. Moore, G. J., Bebchuk, J. M., Wilds, I. B., Chen, G. and Manji, H. K. (2000) Lithium-induced increase in human brain grey matter. Lancet 356, 1241-1242.
111. Perez, M., Hernandez, F., Lim, F., Diaz-Nido, J. and Avila, J. (2003) Chronic lithium treatment decreases mutant tau protein aggregation in a transgenic mouse model. J. Alzheimers Dis. 5, 301-308.
112. Noble, W., Planel, E., Zehr, C., Olm, V., Meyerson, J., Suleman, F., Gaynor, K., Wang, L., LaFrancois, J., Feinstein, B. et al.. (2005) Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo. Proc. Natl. Acad. Sci. USA 102, 6990-6995.
113. Engel, T., Lucas, J. J., Gomez-Ramos, P., Moran, M. A., Avila, J. and Hernandez, F. (2006) Cooexpression of FTDP-17 tau and GSK-3beta in transgenic mice induce tau polymerization and neurodegeneration. Neurobiol. Aging 27, 1258-1268.
114. Nakashima, H., Ishihara, T., Suguimoto, P., Yokota, O., Oshima, E., Kugo, A., Terada, S., Hamamura, T., Trojanowski, J. Q., Lee, V. M. et al. (2005) Chronic lithium treatment decreases tau lesions by promoting ubiquitination in a mouse model of tauopathies. Acta Neuropathol. 110, 547-56.
115. Bhat, R., Xue, Y., Berg, S., Hellberg, S., Ormo, M., Nilsson, Y., Radesater, A. C., Jerning, E., Markgren, P. O., Borgegard, T. et al. (2003) Structural insights and biological effects of glycogen synthase kinase 3-specific inhibitor AR-A014418. J. Biol. Chem. 278, 45937-45945.
116. Le Corre, S., Klafki, H. W., Plesnila, N., Hubinger, G., Obermeier, A., Sahagun, H., Monse, B., Seneci, P., Lewis, J., Eriksen, J. et al. (2006) An inhibitor of tau hyperphosphorylation prevents severe motor impairments in tau transgenic mice. Proc. Natl. Acad. Sci. USA 103, 9673-9678.
117. Matsuoka, Y., Gray A. J., Li, H.-F., Hirata, C., Planel, E., Duff, K., Mattson, M. P., Gozes, I. and Aisen, P. S. (2006) NAP reduces phosphorylated tau in AD transgenic mice. Alzheimer Dementia 2, P4-P333.
118. Noble, W., Hanger, D. P. and Anderton, B. H. (2006) Minocycline reduces tau phosphorylation and protects against Ab-induced neurotoxicity. Alzheimer's Dementia 2, S41-S42.
119. Farias, G. G., Godoy, J. A., Hernandez, F., Avila, J., Fisher, A. and Inestrosa, N. C. (2004) M1 muscarinic receptor activation protects neurons from beta-amyloid toxicity. A role for Wnt signaling pathway. Neurobiol. Dis. 17, 337-348.
120. d'Abramo, C., Ricciarelli, R., Pronzato, M. A. and Davies, P. (2006) Troglitazone, a peroxisome proliferator-activated receptor-gamma agonist, decreases tau phosphorylation in CHOtau4R cells. J. Neurochem. 98, 1068-1077.
121. Gopalakrishnan, M. (2006) Modulation of GSK3beta and MAP kinase pathway via alpha-7 neuronal nicotinic receptors: potential for disease modification in Alzheimer's disease. Alzheimer's Dementia 2, S615-S616.
122. Chen, S., Grundke-Iqbal, I. and Iqbal, K. (2006) I1PP2A and I2PP2A affect tau phosphorylation via association with the catalytic subunit of protein phosphatase 2A. Alzheimer's Dementia 2, S471.
123. Lindwall, G. and Cole, R. D. (1984) Phosphorylation affects the ability of tau protein to promote microtubule assembly. J. Biol. Chem. 259, 5301-5305.
124. Lu, Q. and Wood, J. G. (1993) Characterization of fluorescently derivatized bovine tau protein and its localization and functions in cultured Chinese hamster ovary cells. Cell Motil. Cytoskeleton 25, 190-200.
125. Lovestone, S., Hartley, C. L., Pearce, J. and Anderton, B. H. (1996) Phosphorylation of tau by glycogen synthase kinase-3 beta in intact mammalian cells: the effects on the organization and stability of microtubules. Neuroscience 73, 1145-1157.
126. Lucas, J. J., Hernandez, F. and Avila, J. (1999) Nuclear localization of beta-catenin in adult mouse thalamus correlates with low levels of GSK-3beta. Neuroreport 10, 2699-2703.
127. Engel, T., Hernandez, F., Avila, J. and Lucas, J. J. (2006) Full reversal of Alzheimer's disease-like phenotype in a mouse model with conditional overexpression of glycogen synthase kinase-3. J. Neurosci. 26, 5083-5090.
128. Vershinin, M., Carter, B. C., Razafsky, D. S., King, S. J. and Gross, S. P. (2007) Multiple-motor based transport and its regulation by Tau. Proc. Natl. Acad. Sci. USA 104, 87-92.
129. Fulga, T. A., Elson-Schwab, I., Khurana, V., Steinhilb, M. L., Spires, T. L., Hyman, B. T. and Feany, M. B. (2006) Abnormal bundling and accumulation of F-actin mediates tau-induced neuronal degeneration in vivo. Nat. Cell. Biol. 9, 139-148.
130. Correas, I., Padilla, R. and Avila, J. (1990) The tubulin-binding sequence of brain microtubule-associated proteins, tau and MAP-2, is also involved in actin binding. Biochem. J. 269, 61-64.
131. Price, D. L., Sisodia, S. S. and Borchelt, D. R. (1998) Genetic neurodegenerative diseases: the human illness and transgenic models. Science 282, 1079-1083.
132. Arrasate, M., Mitra, S., Schweitzer, E. S., Segal, M. R. and Finkbeiner, S. (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431, 805-810.
133. Hooper, C., Markevich, V., Plattner, F., Killick, R., Schofield, E., Engel, T., Hernandez, F., Anderton, B., Rosenblum, K., Bliss, T. et al. (2007) Glycogen synthase kinase-3 inhibition is integral to long-term potentiation. Eur. J. Neurosci. 25, 81-86.
134. Hernandez, F., Borrell, J., Guaza, C., Avila, J. and Lucas, J. J. (2002) Spatial learning deficit in transgenic mice that conditionally over-express GSK-3beta in the brain but do not form tau filaments. J. Neurochem. 83, 1529-1533.
135. Santacruz, K., Lewis, J., Spires, T., Paulson, J., Kotilinek, L., Ingelsson, M., Guimaraes, A., DeTure, M., Ramsden, M., McGowan, E. et al. (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science 309, 476-481.
136. Aoyama, K., Matsubara, K. and Kobayashi, S. (2006) Aging and oxidative stress in progressive supranuclear palsy. Eur. J. Neurol. 13, 89-92.
137. Odetti, P., Garibaldi, S., Norese, R., Angelini, G., Marinelli, L., Valentini, S., Menini, S., Traverso, N., Zaccheo, D., Siedlak, S. et al. (2000) Lipoperoxidation is selectively involved in progressive supranuclear palsy. J. Neuropathol. Exp. Neurol. 59, 393-397.
138. Schmechel, D. E., Saunders, A. M., Strittmatter, W. J., Crain, B. J., Hulette, C. M., Joo, S. H., Pericak-Vance, M. A., Goldgaber, D. and Roses, A. D. (1993) Increased amyloid betapeptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc. Natl. Acad. Sci. USA 90, 9649-9653.
139. Strittmatter, W. J., Saunders, A. M., Schmechel, D., Pericak-Vance, M., Enghild, J., Salvesen, G. S. and Roses, A. D. (1993) Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl. Acad. Sci. USA 90, 1977-1981.
140. Ohkubo, N., Lee, Y. D., Morishima, A., Terashima, T., Kikkawa, S., Tohyama, M., Sakanaka, M., Tanaka, J., Maeda, N., Vitek, M. P. et al. (2003) Apolipoprotein E and Reelin ligands modulate tau phosphorylation through an apolipoprotein E receptor/disabled-1/glycogen synthase kinase-3beta cascade. FASEB J. 17, 295-297.
141. Beffert, U., Morfini, G., Bock, H. H., Reyna, H., Brady, S. T. and Herz, J. (2002) Reelin-mediated signaling locally regulates protein kinase B/Akt and glycogen synthase kinase 3beta. J. Biol. Chem. 277, 49958-49964.
142. Scheuner, D., Eckman, C., Jensen, M., Song, X., Citron, M., Suzuki, N., Bird, T. D., Hardy, J., Hutton, M., Kukull, W. et al. (1996) Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nat. Med. 2, 864-870.
143. Brunkan, A. L. and Goate, A. M. (2005) Presenilin function and gamma-secretase activity. J. Neurochem. 93, 769-792.
144. Busciglio, J., Lorenzo, A., Yeh, J. and Yankner, B. A. (1995) beta-Amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14, 879-888.
145. Takashima, A., Noguchi, K., Sato, K., Hoshino, T. and Imahori, K. (1993) Tau protein kinase I is essential for amyloid beta-protein-induced neurotoxicity. Proc. Natl. Acad. Sci. USA 90, 7789-7793.
146. Zhou, X. W., Tanila, H., Liu, R, Winblad, B., Pei, J. J. (2006) Ab mediates tau hyperphosphorylation via down-regulating PP2A in Alzheimer's disease. Alzheimer's Dementia 2, S463-S464.
147. Selkoe, D. J. (1996) Amyloid beta-protein and the genetics of Alzheimer's disease. J. Biol. Chem. 271, 18295-18298.
148. Hardy, J. and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356.
149. Murayama, O., Tomita, T., Nihonmatsu, N., Murayama, M., Sun, X. Y., Honda, T., Iwatsubo, T. and Takashima, A. (1999) Enhancement of amyloid beta 42 secretion by 28 different presenilin 1mutations of familial Alzheimer's disease. Neurosci. Lett. 265, 61-63.
150. Dermaut, B., Kumar-Singh, S., Engelborghs, S., Theuns, J., Rademakers, R., Saerens, J., Pickut, B. A., Peeters, K., van den Broeck, M., Vennekens, K. et al. (2004) A novel presenilin 1 mutation associated with Pick's disease but not beta-amyloid plaques. Ann. Neurol. 55, 617-626.
151. Weihl, C. C., Ghadge, G. D., Kennedy, S. G., Hay, N., Miller, R. J. and Roos, R. P. (1999) Mutant presenilin-1 induces apoptosis and downregulates Akt/PKB. J. Neurosci. 19, 5360-5369.
152. Baki, L., Shioi, J., Wen, P., Shao, Z., Schwarzman, A., Gama-Sosa, M., Neve, R. and Robakis, N. K. (2004) PS1 activates PI3K thus inhibiting GSK-3 activity and tau overphosphorylation: effects of FAD mutations. EMBO J. 23, 2586-2596.
153. Tu, H., Nelson, O., Bezprozvanny, A., Wang, Z., Lee, S. F., Hao, Y. H., Serneels, L., De Strooper, B., Yu, G. and Bezprozvanny, I. (2006) Presenilins form ER Ca2+ leak channels, a function disrupted by familial Alzheimer's disease-linked mutations. Cell 126, 981-993.
154. Amadoro, G., Ciotti, M. T., Costanzi, M., Cestari, V., Calissano, P. and Canu, N. (2006) NMDA receptor mediates tau-induced neurotoxicity by calpain and ERK/MAPK activation. Proc. Natl. Acad. Sci. USA 103, 2892-2897.
155. Li, L., Sengupta, A., Haque, N., Grundke-Iqbal, I. and Iqbal, K. (2004) Memantine inhibits and reverses the Alzheimer type abnormal hyperphosphorylation of tau and associated neurodegeneration. FEBS Lett. 566, 261-269.
156. Jope, R. S. and Johnson, G. V. (2004) The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 29, 95-102.
157. Yanagisawa, M., Planel, E., Ishiguro, K. and Fujita, S. C. (1999) Starvation induces tau hyperphosphorylation in mouse brain: implications for Alzheimer's disease. FEBS Lett. 461, 329-333.
158. Okawa, Y., Ishiguro, K. and Fujita, S. C. (2003) Stress-induced hyperphosphorylation of tau in the mouse brain. FEBS Lett. 535, 183-189.
159. Hanson, E. S., Levin, N. and Dallman, M. F. (1997) Elevated corticosterone is not required for the rapid induction of neuropeptide Y gene expression by an overnight fast. Endocrinology 138, 1041-1047.
160. Arendt, T., Stieler, J., Strijkstra, A. M., Hut, R. A., Rudiger, J., Van der Zee, E. A., Harkany, T., Holzer, M. and Hartig, W. (2003) Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J. Neurosci. 23, 6972-6981.
161. Billings, L. M., Green, K. N., McGaugh, J. L. and LaFerla, F. M. (2007) Learning decreases Aß*56 and tau pathology and ameliorates behavioral decline in 3xTg-AD mice., J. Neurosci. 27, 751-761.
162. Crowther, R. A., Olesen, O. F., Jakes, R. and Goedert, M. (1992) The microtubule binding repeats of tau protein assemble into filaments like those found in Alzheimer's disease. FEBS Lett. 309, 199-202.
163. Troncoso, J. C., Costello, A., Watson, A. L., Jr. and Johnson, G. V. (1993) In vitro polymerization of oxidized tau into filaments. Brain Res. 613, 313-316.
164. Wille, H., Drewes, G., Biernat, J., Mandelkow, E. M. and Mandelkow, E. (1992) Alzheimer-like paired helical filaments and antiparallel dimers formed from microtubule-associated protein tau in vitro. J. Cell. Biol. 118, 573-584.
165. Wilson, D. M. and Binder, L. I. (1997) Free fatty acids stimulate the polymerization of tau and amyloid beta peptides. In vitro evidence for a common effector of pathogenesis in Alzheimer's disease. Am. J. Pathol. 150, 2181-2195.
166. Goedert, M., Jakes, R., Spillantini, M. G., Hasegawa, M., Smith, M. J. and Crowther, R. A. (1996) Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature 383, 550-553.
167. Perez, M., Valpuesta, J. M., Medina, M., Montejo de Garcini, E. and Avila, J. (1996) Polymerization of tau into filaments in the presence of heparin: the minimal sequence required for tau-tau interaction. J. Neurochem. 67, 1183-1190.
168. Perez, M., Cuadros, R., Smith, M. A., Perry, G. and Avila, J. (2000) Phosphorylated, but not native, tau protein assembles following reaction with the lipid peroxidation product, 4-hydroxy-2-nonenal. FEBS Lett. 486, 270-274.
169. Perez, M., Hernandez, F., Gomez-Ramos, A., Smith, M., Perry, G. and Avila, J. (2002) Formation of aberrant phosphotau fibrillar polymers in neural cultured cells. Eur. J. Biochem. 269, 1484-1489.
170. Santa-Maria, I., Hernandez, F., Martin, C. P., Avila, J. and Moreno, F. J. (2004) Quinones facilitate the self-assembly of the phosphorylated tubulin binding region of tau into fibrillar polymers. Biochemistry 43, 2888-2897.
171. Santa-Maria, I., Hernandez, F., Smith, M. A., Perry, G., Avila, J. and Moreno, F. J. (2005) Neurotoxic dopamine quinone facilitates the assembly of tau into fibrillar polymers. Mol. Cell. Biochem. 278, 203-212.
172. von Bergen, M., Friedhoff, P., Biernat, J., Heberle, J., Mandelkow, E. M. and Mandelkow, E. (2000) Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif [(306)VQIVYK(311)] forming beta structure. Proc. Natl. Acad. Sci. USA 97, 5129-5134.
173. Lee, V. M., Goedert, M. and Trojanowski, J. Q. (2001) Neurodegenerative tauopathies. Annu. Rev. Neurosci. 24, 1121-1159.
174. Bancher, C., Brunner, C., Lassmann, H., Budka, H., Jellinger, K., Wiche, G., Seitelberger, F., Grundke-Iqbal, I., Iqbal, K. and Wisniewski, H. M. (1989) Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease. Brain Res. 477, 90-99.
175. Gordon-Krajcer, W., Yang, L. and Ksiezak-Reding, H. (2000) Conformation of paired helical filaments blocks dephosphorylation of epitopes shared with fetal tau except Ser199/202 and Ser202/Thr205. Brain Res. 856, 163-175.
176. Eldar-Finkelman, H. (2002) Glycogen synthase kinase 3: an emerging therapeutic target. Trends Mol. Med. 8, 126-132.
177. Schneider, A., Biernat, J., vonBergen, M., Mandelkow, E. and Mandelkow, E. M. (1999) Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments. Biochemistry 38, 3549-3558.
178. Serpell, L. C., Sunde, M. and Blake, C. C. (1997) The molecular basis of amyloidosis. Cell. Mol. Life Sci. 53, 871-887.
179. Sadqi, M., Hernandez, F., Pan, U., Perez, M., Schaeberle, M. D., Avila, J. and Munoz, V. (2002) Alpha-helix structure in Alzheimer's disease aggregates of tau-protein. Biochemistry 41, 7150-7155.
180. Minoura, K., Tomoo, K., Ishida, T., Hasegawa, H., Sasaki, M. and Taniguchi, T. (2002) Amphipathic helical behavior of the third repeat fragment in the tau microtubule-binding domain, studied by (1)H NMR spectroscopy. Biochem. Biophys. Res. Commun. 294, 210-214.
181. Hiraoka, S., Yao, T. M., Minoura, K., Tomoo, K., Sumida, M., Taniguchi, T. and Ishida, T. (2004) Conformational transition state is responsible for assembly of microtubule-binding domain of tau protein. Biochem. Biophys. Res. Commun. 315, 659-663.
182. Mendieta, J., Fuertes, M. A., Kunjishapatham, R., Santa-Maria, I., Moreno, F. J., Alonso, C., Gago, F., Munoz, V., Avila, J. and Hernandez, F. (2005) Phosphorylation modulates the alpha-helical structure and polymerization of a peptide from the third tau microtubule-binding repeat. Biochim. Biophys. Acta 1721, 16-26.
183. Duff, K., Knight, H., Refolo, L. M., Sanders, S., Yu, X., Picciano, M., Malester, B., Hutton, M., Adamson, J., Goedert, M. et al. (2000) Characterization of pathology in transgenic mice over-expressing human genomic and cDNA tau transgenes. Neurobiol. Dis. 7, 87-98.
184. Andorfer, C., Acker, C. M., Kress, Y., Hof, P. R., Duff, K. and Davies, P. (2005) Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. J. Neurosci. 25, 5446-5454.
185. Sahara, N., Lewis, J., DeTure, M., McGowan, E., Dickson, D. W., Hutton, M. and Yen, S. H. (2002) Assembly of tau in transgenic animals expressing P301L tau: alteration of phosphorylation and solubility. J. Neurochem. 83, 1498-1508.
186. Allen, B., Ingram, E., Takao, M., Smith, M. J., Jakes, R., Virdee, K., Yoshida, H., Holzer, M., Craxton, M., Emson, P. C. et al.. (2002) Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J. Neurosci. 22, 9340-9351.
187. Bu, B., Klunemann, H., Suzuki, K., Li, J., Bird, T., Jin, L. W. and Vincent, I. (2002) Niemann-Pick disease type C yields possible clue for why cerebellar neurons do not form neurofibrillary tangles. Neurobiol. Dis. 11, 285-297.
188. Tatebayashi, Y., Iqbal, K. and GrundkeIqbal, I. (1999) Dynamic regulation of expression and phosphorylation of tau by fibroblast growth factor-2 in neural progenitor cells from adult rat hippocampus. J. Neurosci. 19, 5245-5254.
189. Perez, M., Lim, F., Arrasate, M. and Avila, J. (2000) The FTDP-17-linked mutation R406W abolishes the interaction of phosphorylated tau with microtubules. J. Neurochem. 74, 2583-2589.
190. Tanemura, K., Murayama, M., Akagi, T., Hashikawa, T., Tominaga, T., Ichikawa, M., Yamaguchi, H. and Takashima, A. (2002) Neurodegeneration with tau accumulation in a transgenic mouse expressing V337M human tau. J. Neurosci. 22, 133-141.
191. Tanemura, K., Chui, D. H., Fukuda, T., Murayama, M., Park, J. M., Akagi, T., Tatebayashi, Y., Miyasaka, T., Kimura, T., Hashikawa, T. et al. (2006) Formation of tau inclusions in knock-in mice with familial Alzheimer disease (FAD) mutation of presenilin 1 (PS1). J. Biol. Chem. 281, 5037-5041.
192. Khlistunova, I., Biernat, J., Wang, Y., Pickhardt, M., von Bergen, M., Gazova, Z., Mandelkow, E. and Mandelkow, E. M. (2006) Inducible expression of Tau repeat domain in cell models of tauopathy: aggregation is toxic to cells but can be reversed by inhibitor drugs. J. Biol. Chem. 281, 1205-1214.
193. Ding, H., Matthews, T. A. and Johnson, G. V. (2006) Site-specific phosphorylation and caspase cleavage differentially impact tau-microtubule interactions and tau aggregation. J. Biol. Chem. 281, 19107-19114.
194. Shahani, N., Subramaniam, S., Wolf, T., Tackenberg, C. and Brandt, R. (2006) Tau aggregation and progressive neuronal degeneration in the absence of changes in spine density and morphology after targeted expression of Alzheimer's disease relevant tau constructs in organotypic hippocampal slices. J. Neurosci. 26, 6103-6114.
195. Braak, H. and Braak, E. (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82, 239-259.
196. Cras, P., Smith, M. A., Richey, P. L., Siedlak, S. L., Mulvihill, P. and Perry, G. (1995) Extracellular neurofibrillary tangles reflect neuronal loss and provide further evidence of extensive protein cross-linking in Alzheimer disease. Acta Neuropathologica 89, 291-295.
197. Fukutani, Y., Kobayashi, K., Nakamura, I., Watanabe, K., Isaki, K. and Cairns, N. J. (1995) Neurons, intracellular and extracellular neurofibrillary tangles in subdivisions of the hippocampal cortex in normal ageing and Alzheimer's disease. Neurosci. Lett. 200, 57-60.
198. Goedert, M. (1999) Filamentous nerve cell inclusions in neurodegenerative diseases: tauopathies and alpha-synucleinopathies. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354, 1101-1118.
199. Bondareff, W., Mountjoy, C. Q., Roth, M. and Hauser, D. L. (1989) Neurofibrillary degeneration and neuronal loss in Alzheimer's disease. Neurobiol. Aging 10, 709-715.
200. Caughey, B. and Lansbury, P. T. (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26, 267-298.
201. Morsch, R., Simon, W. and Coleman, P. D. (1999) Neurons may live for decades with neurofibrillary tangles. J. Neuropathol. Exp. Neurol. 58, 188-197.
202. Duff, K. and Planel, E. (2005) Untangling memory deficits. Nat. Med. 11, 826-827.
203. Bird, T. D., Nochlin, D., Poorkaj, P., Cherrier, M., Kaye, J., Payami, H., Peskind, E., Lampe, T. H., Nemens, E., Boyer, P. J. et al. (1999) A clinical pathological comparison of three families with frontotemporal dementia and identical mutations in the tau gene (P301L). Brain 122, 741-756.
204. Delacourte, A., David, J. P., Sergeant, N., Buee, L., Wattez, A., Vermersch, P., Ghozali, F., Fallet-Bianco, C., Pasquier, F., Lebert, F. et al. (1999) The biochemical pathway of neurofibrillary degeneration in aging and Alzheimer's disease. Neurology 52, 1158-1165.
205. Gomez-Isla, T., Hollister, R., West, H., Mui, S., Growdon, J. H., Petersen, R. C., Parisi, J. E. and Hyman, B. T. (1997) Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann. Neurol. 41, 17-24.
206. Prusiner, S. B. (2001) Shattuck lecture-neurodegenerative diseases and prions. N. Engl. J. Med. 344, 1516-1526.
207. Engel, T., Goni-Oliver, P., Lucas, J. J., Avila, J. and Hernandez, F. (2006) Chronic lithium administration to FTDP-17 tau and GSK-3beta overexpressing mice prevents tau hyperphosphorylation and neurofibrillary tangle formation, but pre-formed neurofibrillary tangles do not revert. J. Neurochem. 99, 1445-1455.
208. Oddo, S., Vasilevko, V., Caccamo, A., Kitazawa, M., Cribbs, D. H. and LaFerla, F. M. (2006) Reduction of soluble abeta and tau, but not soluble abeta alone, ameliorates cognitive decline in transgenic mice with plaques and tangles. J. Biol. Chem. 281, 39413-39423.
209. Morsch, R., Simon, W. and Coleman, P. D. (1999) Neurons may live for decades with neurofibrillary tangles. J. Neuropathol. Exp. Neurol. 58, 188-197.
210. Gomez-Ramos, A., Diaz-Hernandez, M., Cuadros, R., Hernandez, F. and Avila, J. (2006) Extracellular tau is toxic to neuronal cells. FEBS Lett. 580, 4842-4850.