Tau oligomers and aggregation in Alzheimer's disease

Journal of Neurochemistry

Volumn 112, Issue 6, 2010, Pages 1353-1367

  Meraz Ríos, Marco A ^a   Lira De León, Karla I ^a   Campos Peña, Victoria ^b   De Anda Hernández, Martha A ^a   Mena López, Raúl ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

Author keywords

Aggregates; Alzheimer's disease; Oligomers; Paired helical filament; Tau

Indexed keywords

2,3,4,2',4' PENTAHYDROXYPHENONE; ANILINE DERIVATIVE; ANTHRAQUINONE DERIVATIVE; AZURE A; AZURE B; DAUNORUBICIN; DOXORUBICIN; DYE; EMODIN; EPICATECHIN; FERRIC DEHYDROPORPHYRIN IX; GOSSYPETIN; METHYLENE BLUE; MYRICETIN; OLIGOMER; PHENOTHIAZINE DERIVATIVE; PHF 005; PHF 016; POLYPHENOL DERIVATIVE; PORPHYRIN DERIVATIVE; QUINANCRINE MUSTARD; RHODANINE; TAU PROTEIN; THIACARBOCYANINE DYE N 744; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; CORTICOBASAL DEGENERATION; DEMENTIA; DEMENTIA PUGILISTICA; FRONTOTEMPORAL DEMENTIA; GLUCOSE METABOLISM; GUAM PARKINSONISM DEMENTIA COMPLEX; HUMAN; NERVE CELL NECROSIS; NEUROPATHOLOGY; NEUROTOXICITY; NIEMANN PICK DISEASE; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROCESSING; REVIEW;

ALZHEIMER DISEASE; ANIMALS; HUMANS; NEUROFIBRILLARY TANGLES; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; TAU PROTEINS;

ANIMALIA;

EID: 77349118694     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06511.x     Document Type: Review

References (140)

1. Abraha A., Ghoshal N., Gamblin T. C., Cryns V., Berry R. W., Kuret J. Binder L. I. (2000) C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease. J. Cell Sci. 113, 3737 3745.
2. Adams C. W. M. Bruton C. J. (1989) The cerebral vasculature in dementia pugilistica. J. Neurol. Neurosurg. Psychiatry 52, 600 604.
3. Alonso A. D., Grundke-Iqbal I., Barra H. S. Iqbal K. (1997) Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: sequestration of microtubule-associated proteins 1 and 2 and the disassembly of microtubules by the abnormal tau. Proc. Natl Acad. Sci. USA 94, 298 303.
4. Alonso A. C., Zaidi T., Novak M., Grundke-Iqbal I. Iqbal K. (2001) Hyperphosphorylation induces self-assembly of t into tangles of paired helical filaments/straight filaments. Proc. Natl Acad. Sci. USA 98, 6923 6928.
5. Andronesi O. C., von Bergen M., Biernat J., Seidel K., Griesinger C., Mandelkow E. Baldus M. (2008) Characterization of Alzheimer's-like paired helical filaments from the core domain of tau protein using solid-state NMR spectroscopy. J. Am. Chem. Soc. 130, 5922 5928.
6. Arai T., Guao J. P. McGeer P. L. (2005) Proteolysis of non-phosphorylated and phosphorylated Tau by Thrombin. J. Cell Biol. 280, 5145 5153.
7. Ávila J., Lucas J. J., Pérez M. Hernández F. (2004) Role of tau protein in both physiological and pathological conditions. Physiol. Rev. 84, 361 384.
8. Bandyopadhyay B., Li G., Yin H. Kuret J. (2007) Tau aggregation and toxicity in a cell culture model of tauopathy. J. Biol. Chem. 282, 16454 16464.
9. Barghorn S. Mandelkow E. (2002) Toward a unified scheme for the aggregation of tau into Alzheimer paired helical filaments. Biochemistry 41, 14885 14896.
10. Basurto-Islas G., Luna-Muñoz J., Guillozet-Bongaart A., Binder L., Mena R. García-Sierra F. (2008) Accumulation of aspartic acid 421-and glutamic acid 391-cleaved Tau in neurofibrillary tangles correlates with progression in Alzheimer disease. J. Neuropathol. Exp. Neurol. 67, 1 14.
11. 311) forming β structure. Proc. Natl Acad. Sci. USA 97, 5129 5134.
12. Berger Z., Roder H., Hanna A. et al. (2007) Accumulation of pathological tau species and memory loss in a conditional model of tauophaty. J. Neurosci. 27, 3650 3662.
13. Binder L. I., Guillozet-Bongaartsa A. L., Garcia-Sierra F. Berry R. W. (2005) Tau, tangles, and Alzheimer's disease. Biochim. Biophys. Acta 1739, 216 223.
14. Braak H. Braak E. (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol. 82, 239 259.
15. Braak H., Alafuzoff I., Arzberger T., Kretzshmar H. Del Tredici K. (2006) Staging of Alzheimer disease-associated neurofbrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol. 112, 389 404.
16. Brandt R., Hundetl M. Shahani N. (2005) Tau alteration and neuronal degeneration in Tauopathies: mechanisms and models. Biochim. Biophys. Acta 1739, 331 354.
17. Buée L., Bussière T., Buée-Scherrer V., Delacourte A. Hof P. R. (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res. Rev. 33, 95 130.
18. Bulic B., Pickhart M., Khlistunova I., Biernat J., Mandelkow E.-M., Mandelkow E. Waldmann H. (2007) Rhodanine-based tau aggregation inhibitors in cell models of tauopathy Angew. Chem. Int. Ed. 46, 1 6.
19. Bulic B., Pickhart M., Schmidt B., Mandelow E.-M., Waldmann H. Mandelkow E. (2009) Development of Tau aggregation inhibitors for Alzheimer Disease Angrew. Chem. Int. Ed. 48, 1740 1752.
20. Carlson S. W., Branden M., Voss K., Sun Q., Rankin C. A. Gamblin T. C. (2007) A complex mechanism for inducer mediated tau polymerization. Biochemistry. 46, 8838 8849.
21. Chirita C. N., Congdon E. E., Yin H. Kuret J. (2005) Triggers of full-length tau aggregation: a role for partially folded intermediates. Biochemistry. 44, 5862 5872.
22. Congdon E. E., Necula M., Blackstone R. D. Kuret J. (2007) Potency of a Tau fibrillization inhibitor is influenced by its aggregation state. Arch. Biochem. Biophys. 465, 127 135.
23. Congdon E. E., Kim S., Bonchak J., Songrug T., Matzavinos A. Kuret J. (2008) Nucleation-dependent tau filament formation, the importance of dimerization and an estimation of elementary rat constants. J. Biol. Chem. 283, 13806 13816.
24. Congdon E. E., Figueroa Y., Wang L., Toneva G., Chang E., Kuret J., Conrad C. Duff K. (2009) Inhibition of Tau polymerization with a cyanine dye in two distinct model systems. J. Biol. Chem. 284 (31 20830 20839.
25. Cripps D., Thomas S. N., Jeng Y., Yang F., Davies P. Yang A. J. (2005) Alzheimer disease-specific conformation of hyperphophorylated paired helical filament-tau is polyubiquitinated through Lys-48, Lys-11, and Lys-6 ubiquitin conjugation. J. Biol. Chem. 281, 10825 10838.
26. Cullen K. M. Halliday G. M. (1995a) Mechanisms of cell death in cholinergic basal forebrain neurons in chronic alcoholics. Metab. Brain Dis. 10, 81 91.
27. Cullen K. M. Halliday G. M. (1995b) Neurofibrillary tangles in chronic alcoholics. Neuropathol. Appl. Neurobiol. 21, 312 318.
28. Deshpande A., Win K. M. Buschiglio J. (2008) Tau isoform expression and regulation in human cortical neurons. FASEB J. 22, 2357 2367.
29. Dickey C. A., Yue M., Lin W. L. 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.
30. Dickson D. W., Rademarkers R. Hutton M. L. (2007) Progressive supranuclear palsy: pathology and genetics. Brain Pathol. 17, 74 82.
31. Ding H. Johnson V. W. (2008) The last tangle of tau. J. Alzheimers Dis. 14, 441 447.
32. Dubey M., Chaudhury P., Kabiru H. Shea T. B. (2008) Tau inhibits anterograde axonal transport and perturbs stability in growing axonal neurites in part by displacing kinesin cargo: neurofilaments attenuate tau-mediated neurite instability. Cell Motil. Cytoskeleton 65, 89 99.
33. Ebneth A., Godemann R., Stamer K., Illenberger S., Trinczek B., Mandelkow E. M. Mandelkow E. (1998) Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J. Cell Biol. 143, 777 794.
34. El-faramawy Y. A., El-banouby M. H., Sergeev P., Mortagy A. K., Amer M. S. Abdel-tawab A. M. (2009) Changes in glutamate decarboxylase enzyme activity and tau-protein phosphorylation in the hippocampus of old rats exposed to chronic mild stress: reversal with the neuronal nitric oxide synthase inhibitor 7-nitroindazole. Pharmacol. Biochem. Behav. 91, 339 344.
35. Fasulo L., Ugolini G., Visitin M., Bradbury A., Brancolini C., Verzilo V., Novak M. Cattaneo A. (2000) The neuronal microtubule-associated protein Tau is a substrate for caspase-3 and effector of apoptosis. J. Neurochem. 75, 624 633.
36. Frost B., Jacks R. L. Diamond M. I. (2009) Propagation of tau misfolding from the outside to the inside of a cell. J. Biol. Chem. 284, 12845 12852.
37. Gamblin T. C., Berry R. W. Binder L. I. (2003) Tau polymerization: role of the amino terminus. Biochemistry 42, 2252 2257.
38. García-Sierra F., Wishick C. M., Harrington C. R., Luna-Muñoz J. Mena R. (2001) Accumulation of C-terminally truncated Tau protein associated with vulnerability of the perforant pathway in early stages of neurofibrillary pathology in Alzheimer's disease. J. Chem. Neuroanat. 22, 65 77.
39. Gendron T. F. Petrucelli L. (2009) The role of tau in neurodegeneration. Mol. Neurodegener. 4, 13 (1-19).
40. Ghoshal N., García-Sierra F., Wuu J., Leurgans S., Bennett D. A., Berry R. W. Binder L. I. (2002) Tau conformational changes correspond to impairments of episodic memory in mild cognitive impairment and Alzheimer's disease. Exp. Neurol. 177, 475 493.
41. Goedert M., Wischik C. M., Crowther R. A., Walker J. E. 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 (11 4051 4055.
42. Goedert M., Jakes R., Spillantini M. G., Hasegawa M., Smith M. J. Crowther R. A. (1996) Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature 383, 550 553.
43. Golde T. E. (2006) Disease modifying therapy for AD? J. Neurochem. 99, 689 707.
44. Gray E. G., Paula-Barbosa M. Roher A. (1987) Alzheimer's disease: paired helical filaments and cytomembranes. Neuropathol. Appl. Neurobiol. 13, 91 110.
45. Guillozet-Bongaarts A. L., Glajch K. E., Libson E. G., Cahill M. E., Bigio E., Berry R. W. Binder L. I. (2007) Phosphorylation and cleavage of tau in non-AD tauopathies. Acta Neuropathol. 113, 513 520.
46. Hamano T., Gendron T. F., Causevic E., Yen S.-H., Lin W.-L., Isidoro C., DeTure M. Ko L.-W. (2008) Autophagic-lysosomal perturbation enhances tau aggregation in transfectants with induced wild-type tau expression. Eur. J. Neuorsci. 27, 1119 1130.
47. Hanger D. P., Anderton B. H. Noble W. (2009) Tau phosphorylation: the therapeutic challenge for neurodegenerative disease. Trends Mol. Med. 15, 112 119.
48. Hernández F. Ávila J. (2007) Tauopathies. Cell. Mol. Life Sci. 64, 2219 2233.
49. Hernández F., Cuadros R. Ávila J. (2004) Zeta 14-3-3 favours the formation of human tau fibrillar polymers. Neurosci. Lett. 357, 143 146.
50. Hikosou R., Kurabayashi Y., Doumoto M., Hoshitoku K., Mizushima F., Minoura K., Tomoo K. Ishida T. (2007) Effect of DNA on filament formation of tau microtubule-binding domain: structural dependence of DNA. Chem. Pharm. Bull. 55, 1030 1033.
51. Holzter M., Gärtner U., Stöbe A., Härtig W., Gruschka H., Brucknër N. K. Arendt T. (2002) Inverse association of Pin1 and tau accumulation in Alzheimer's disease hippocampus. Acta Neuropathol. 104, 471 481.
52. Horowitz P. M., Patterson K. R., Guillozet-Bongaarts A. L., Reynolds M. R., Carroll C. A., Weintraub S. T., Bennett D. A., Cryns V. L., Berry R. W. Binder L. I. (2004) Early N-terminal changes and caspase-6 cleavage of Tau in Alzheimer's disease. J. Neurosci. 24, 7895 7902.
53. Horowitz P. M., LaPointe N., Guillozet-Bongaarts A., Berry R. Binder L. (2006) N-terminal fragments of tau inhibit full-length tau polymerization in vitro. Biochemistry 45, 12859 12866.
54. Hrnkova M., Zilka N., Minichova Z., Koson P. Novak M. (2007) Neurodegeneration caused by expression of human truncated Tau leads to progressive neurobehavioral impairment in transgenic rats. Brain Res. 1130, 206 213.
55. Hua Q. He R. Q. (2003) Tau could protect DNA double helix structure. Biochim. Biophys. Acta 1645, 205 211.
56. Iqbal K. Grundke-Iqbal I. (2008) Alzheimer neurofibrillary degeneration: significance, etiopathogenesis, therapeutics and prevention. J. Cell Mol. Med. 12, 38 55.
57. Ishii H., Ishikawa H., Meguro K., Tashiro M. Yamaguchi S. (2009) Decreased cortical glucose metabolism in converters from CDR 0.5 to Alzheimer's disease in a community: the Osaki-Tajiri project. Int. Psychogeriatr. 21, 148 156.
58. Jämsä A., Bäckström A., Gustafsson E., Dehvari N., Hiller G., Cowburn R. F. Vasänge M. (2006) Glutamate treatment and p25 transfection increase Cdk5 mediated tau phosphorylation in SH-SY5Y cells. Biochem. Biophys. Res. Commun. 345, 324 331.
59. Johnson G. V. W. Stoothoff W. H. (2004) Tau phosphorylation in neuronal cell function and dysfunction. J. Cell Sci. 117, 5721 5729.
60. Kampers T., Friedhoff P., Biernat J., Mandelkow E. M. Mandelkow E. (1996) RNA stimulates aggregation of microtubule-associated protein tau into Alzheimer-like paired helical filaments. FEBS Lett. 399, 344 349.
61. Kayed R. Jackon G. R. (2009) Prefilament tau species as potential targets for immunotherapy for Alzheimer disease and related disorders. Curr. Opin. Inmunol. 21, 359 363.
62. Khlistunova I., Biernat J., Wang Y., Pickhart M., von Berger M., Gazova Z., Mandelkow E. Mandelkow E.-M. (2005) 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.
63. King M. E., Ahuja V., Binder L. I. Kuret J. (1999) Ligand-dependent tau filament formation: implications for Alzheimer's disease progression. Biochemistry 38, 14851 14859.
64. Konno T., Oiki S., Hasegawa K. Naiki H. (2004) Anionic contribution for fibrous maturation of protofibrillar assemblies of the human tau repeat domain in a fluoroalcohol Solution. Biochemistry 43, 13613 13620.
65. Koson P., Zilka N., Kovac A., Kovacech B., Koreniva M., Filipcik P. Novak M. (2008) Truncated tau expression levels determine life span of a rat model of tauopathy without causing neuronal loss or correlating with terminal neurofibrillary tangle load. Eur. J. Neurosci. 28, 239 246.
66. Ksiezak-Reding H. Wall J. S. (2005) Characterization of paired helical filaments by scanning transmission electron microscopy. Microsc. Res. Tech. 67, 126 140.
67. Kuczynski B., Reed B., Mungas D., Weiner M., Chui H. C. Jagust W. (2008) Cognitive and Anatomic Contributions of Metabolic Decline in Alzheimer Disease and Cerebrovascular Disease. Arch. Neurol. 65, 650 655.
68. Kuhla B., Haase C., Flach K., Lüth H.-J., Arendt T. Münch G. (2007) Effect of pseudophosphorylation and cross-linking by lipid peroxidation and advanced glycation en d product precursors on tau aggregation and filament formation. J. Biol. Chem. 282, 6984 6991.
69. Kuret J., Congdon E. E., Li G., Yin H., Yu X. Zhong Q. I. (2005) Evaluating triggers and enhancers of tau fibrillization. Microsc. Res. Tech. 67, 141 155.
70. Lebouvier T., Scales T. M., Williamson R., Noble W., Duyckaerts C., Hanger D. P., Reynolds C. H., Anderton B. H. Derkinderen P. (2009) The microtubule-associated protein tau is also phosphorylated on tyrosine. J Alzheimers Dis. 18, 1 9.
71. Ledesma M. D., Bonay P., Colaço C. Avila J. (1994) Analysis of microtubule-associated protein glycation in paired helical filaments. J. Biol. Chem. 269, 21614 21619.
72. Lee G., Newman S. T., Gard D. L., Band H. Panchamoorthy G. (1998) Tau interacts with src-family non-receptor tyrosine kinases. J. Cell Sci. 111, 3167 3177.
73. Li D.-W., Mohanty S., Irbäck A. Huo S. (2008) Formation and growth of oligomers: a Monte Carlo study of an amyloid tau fragment. PLOS Comput. Biol. 4 (12 e1000238 (1-12).
74. Liang W. S., Dunckley T., Beach T. G. et al. (2007) Gene expression profiles in anatomically and functionally distinct regions of the normal aged human brain. Physiol. Genomics 28, 311 322.
75. Liang W. S., Reiman E. M., Valla J. et al. (2008) Alzheimer's disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proc. Natl Acad. Sci. USA 105, 4441 4446.
76. Lin Y.-T., Cheng J.-T., Liang L.-C., Ko C.-Y., Lo Y.-K. Lu P.-J. (2007) The binding and phosphorylation of Thr231 is critical for tau's hyperphosphorylation and functional regulation by glycogen synthase kinase 3β. J. Neurochem. 103, 802 813.
77. Lira-De León K. I., De Anda-Hernández M. A., Campos-Peña V. Meraz-Ríos M. A. (2009) Plasma membrane-associated PHF-core could be the trigger for tau aggregation, in Alzheimer's Disease Current Hypotheses and Research Milestones in Alzheimer's Disease (Maccioni R. B. Perry G., eds pp. 93 100. Springer, New York.
78. Liu F., Iqbal K., Grundke-iqbak I. Gong C.-X. (2002) Involvement of aberrant glycosylation in phosphorylation of tau by cdk5 and GSK3β. FEBS Lett. 530, 209 214.
79. Liu F., Li B., Tung E.-J., Grundke-Iqbal I., Iqbal K. Gong C.-X. (2007) Site-specific effects of tau phosphorylation on its microtubule assembly activity and self-aggregation. Eur. J. Neurosci. 26, 3429 3436.
80. Liu Y.-H., Wei W., Yin J., Lui G.-P., Wang Q., Cao F.-Y. Wang J.-Z. (2008a) Protesosome inhibition increases tau accumulation independent of phosphorylation. Neurobiol. Aging 30 (12 1949 1961.
81. Liu M., Choi S., Cuny G. D., Ding K., Dobson B. C., Glicksman M. A., Auserbach K. Stein R. L. (2008b) Kinetic studies of Cdk5/p25 kinase: phosphorylation of Tau and complex inhibition by two prototype inhibitors. Biochemistry 47, 8367 8377.
82. Liu F., Shi J., Tanimukai H., Gu J., Gu J., Grundke-Iqbal I., Iqbal K. Gong C. X. (2009) Reduced O-GlcNAcylation links lower brain glucose metabolism and tau pathology in Alzheimer's disease. Brain 132, 1820 1832.
83. Lovestone S. McLoughlin D. M. (2002) Protein aggregates and dementia: is there a common toxicity? J. Neurol. Neurosurg. Psychiatry 72, 152 161.
84. Lu P. J., Wulf G., Zhou X.-Z., Davies P. Lu K. P. (1999) The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 399, 784 788.
85. Ludolph A. C., Kassubek J., Landwehrmeyer B. G. et al. (2009) Tauopathies with parkinsonism: clinical spectrum, neuropathologic basis, biological markers, and treatment options. Eur J Neurol. 16, 297 309.
86. Luna-Muñoz J., Chávez-Macías L., García-Sierra F. Mena R. (2007) Earliest stages of tau conformational changes are related to the appearance of a sequence of specific phospho-dependent tau epitopes in Alzheimer's disease. J. Alzheimers Dis. 12, 365 375.
87. Maeda S., Sahara N., Saito Y., Muruyama S., Ikai A. Takashima A. (2006) Increased levels of granular tau oligomers: an early sign of brain aging and Alzheimer's disease. Neurosci. Res. 54, 197 201.
88. Maeda S., Sahara N., Saito Y., Murayama M., Yoshiike Y., Kim H., Miyasaka T., Murayama S., Ikai A. Takashima A. (2007) Granular Tau oligomers as intermediates of Tau filaments. Biochemistry 46, 3856 3861.
89. Makrides V., Shen T. E., Bhatia R., Smith B. L., Thimm J., Lal R. Feinstein S. C. (2003) Microtubule-dependent oligomerization of tau: implications for physiological tau function and tauopathies. J. Biol. Chem. 278, 33298 33304.
90. Mandelkow E., von Bergen M., Biernat J. Mandelkow E. M. (2007) Structural principles of tau and the paired helical filaments of Alzheimer's disease. Brain Pathol. 17, 83 90.
91. Manetto V., Perry G., Tabaton M., Mulvihill P., Fried V. A., Smith H. T., Gambetti P. Autilio-Gambetti L. (1988) Ubiquitin is associated with abnormal cytoplasmic filaments characteristic of neurodegenerative diseases. Proc. Natl Acad. Sci. USA 85, 4501 4505.
92. Mocanu M.-M., Niessen A., Eckermann K. et al. (2008) The potential for β-structure in the repeat domain of tau protein determines aggregation, synaptic decay, neuronal loss, and coassembly with endogenous tau in inducible mouse models of tauopathy. J. Neurosci. 28, 737 748.
93. Mondragón-Rodríguez S., Basurto-Islas G., Santa-Maria I., Mena R., Binder L. I., Avila J., Smith M. A., Perry G. García-Sierra F. (2008) Cleavage and conformational changes of tau protein follow phosphorylation during Alzheimer's disease. Int. J. Exp. Pathol. 89, 81 90.
94. Montejo de Garcini E., Carrascosa J. L., Correas I., Nieto A. Ávila J. (1988) Tau factor polymers are similar to paired helical filaments of Alzheimer's disease. FEBS Lett. 236, 150 154.
95. Murakami N. (1999) Parkinsonism-dementia complex on Guam - overview of clinical aspects. J. Neurol. 246 (Suppl. 2 II16 II18.
96. Nie C. L., Wang X. S., Liu Y., Perrett S. He R. Q. (2007a) Amyloid-like aggregates of neuronal tau induced by formaldehyde promote apoptosis of neuronal cells. BMC Neurosci. 8, 9.
97. Nie C. L., Wei Y., Chen X., Liu Y. Y., Dui W., Liu Y., Davies M. C., Tendler S. J. B. He R. G. (2007b) Formaldehyde at low concentration induces protein tau into globular amyloid-like aggregates in vitro and in vivo. PLoS ONE 2 (7 e629 (1-13).
98. Novak M., Kabat J. Wischik C. M. (1993) Molecular characterization of the minimal protease resistant Tau unit of the Alzheimer's disease paired helical filament. EMBO J. 12, 365 370.
99. Pacheco C. D. Lieberman A. P. (2008) The pathogenesis of Niemann-Pick type C disease: a role for autophagy? Expert Rev. Mol. Med. 10, e26 (1-17).
100. Pérez M., Arrasate M., Montejo de Garcini E., Muñoz V. Ávila J. (2001) In vitro assembly of tau protein: mapping the regions involved in filament formation. Biochemistry 40, 5983 5991.
101. Petterson D. W., Zhou H., Dahlquist F. W. Lew J. (2008) A soluble oligomer of tau associated with fiber formation analyzed by NMR. Biochemistry 47, 7393 7404.
102. Pickhart M., Gazova Z., von Bergen M., Khlistunova I., Wang Y., Hascher A., Mandelkow E.-M., Biernat J. Mandelkow E. (2005) Anthraquinones inhibit tau aggregation and dissolve Alzheimer's paired helical filaments in vitro and in cells. J. Biol. Chem. 280, 3628 3635.
103. Pickhart M., Larbig G., Khlistunova I., Coksezen A., Meyer B., Mandelkow E.-M., Schmidt B. Mandelkow E. (2007) Phenylthiazolyl-hydrazide and its derivates are potent inhibitors of Tau aggregation and toxicity in vitro and in cells. Biochemistry 46, 10016 10023.
104. Reyes J. F., Reynolds M. R., Horowitz P. M., Fu Y., Guillozet-Bongaarts A., Berry R. Binder L. (2008) A possible link between astrocyte activation and Tau nitration in Alzheimer's disease. Neurobiol. Dis. 31, 198 208.
105. Reynolds M. R., Berry R. Binder L. I. (2005) Site-specific nitration differentially influences assembly in vitro. Biochemistry 44, 13997 14009.
106. Reynolds M. R., Reyes J. F., Fu W., Bigio E. H., Guillozet-Bongaarts A., Berry R. Binder L. (2006) Tau nitration occurs at tyrosine 29 in the fibrillar lesions of Alzheimer's disease and other tauopathies. J. Neurosci. 26, 10636 10645.
107. Reynolds M. R., Berry R. Binder L. I. (2007) Nitration in neurodegeneration: deciphering the Hows 'nYs'. Biochemistry 46, 7325 7336.
108. Robert M. Mathuranath P. S. (2007) Tau and taupathies. Neurol. India 55, 11 16.
109. Rojo L., Sjöber M. K., Henández P., Zambrano C. Maccioni R. B. (2006) Roles of cholesterol and lipids in the etiopathogenesis of Alzheimer's disease. J. Biomed. Biotech. 2006, 1 17.
110. Rosenberg K. J., Ross J. L., Feinstein H. E., Feinstein S. C. Israelachvili J. (2008) Complementary dimerization of microtubule-associated tau protein: implications for microtubule bundling and tau-mediated pathogenesis. Proc. Natl Acad. Sci. USA 105, 7445 7450.
111. Rupsingh R., Borrie M., Smith M., Wells J. L. Bartha R. (2009) Reduced hippocampal glutamate in Alzheimer disease. Neurobiol. Aging (In press NBA-7333).
112. Sadik G., Tanaka T., Kato K., Yamamori H., Nessa B. N., Morihara T. Takeda M. (2009) Phosphorylation of tau at Ser214 mediates its interaction with 14-3-3 protein: implications for the mechanism of tau aggregation. J. Neurochem. 108, 33 43.
113. Sahara N., Maeda S., Murayama M., Suzuki T., Dohmae N., Yen S.-H. Takashima A. (2007a) Assembly of two distinct dimers and higher-order oligomers from full-length tau. Eur. J. Neurosci. 25, 3020 3029.
114. Sahara N., Maeda S., Yoshiike Y., Mizoroki T., Yamashita S., Murayama M., Park J.-M., Sito Y., Murayama S. Takashima A. (2007b) Molecular chaperone-mediated tau protein metabolism counteracts the formation of granular tau oligomers in human brain. J. Neurosci. Res. 85, 3098 3108.
115. Sánchez M. P., Álvarez-Tallada V. Ávila J. (2001) La proteína tau en enfermedades neurodegenerativas Taupatías. Rev. Neurol. 33, 169 177.
116. Santacruz K., Lewis J., Spires T. et al. (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science 309, 476 481.
117. Santa-María I., Hernández F., Smith M. A., Perry G., Ávila J. Moreno F. J. (2005) Neurotoxic dopamine quinone facilitates the assembly of tau into fibrillar polymers. Mol. Cell. Biochem. 278, 203 212.
118. Santa-María I., Hernández F., Moreno F. J. Ávila J. (2007) Taurine, an inducer for tau polymerization and a weak inhibitor for amyloid-β-peptide aggregation. Neurosc. Lett. 429, 91 94.
119. Sato Y., Naito Y., Grundke-Iqbal I., Iqbal K. Endo T. (2001) Analysis of N-glycans of pathological tau: possible occurrence of aberrant processing of tau in Alzheimer's disease. FEBS Lett. 496, 152 160.
120. Sato S., Cerny R. L., Buescher J. L. Ikezu T. (2006) Tau-tubulin kinase (TTBK1), a neuron-specific tau kinase candidate, is involved in tau phosphorylation and aggregation. J. Neurochem. 98, 1573 1584.
121. Sengupta S., Horowitz P. M., Karsten S. L., Jackson G. R., Geschwind D. H., Fu Y., Berry R. W. Binder L. I. (2006) Degradation of Tau protein by puromycin-sensitive aminopeptidase in vitro. Biochemistry 50, 15111 15119.
122. Sjöberg M. K., Shestakova E., Mansuroglu Z., Maccioni R. B. Bonnefoy E. (2006) Tau protein binds to pericentromeric DNA: a putative role for nuclear tau in nucleolar organization. J. Cell Sci. 119, 2025 2034.
123. Skrabana R., Kontsek P., Merderlyova A., Iqbal K. Novak M. (2004) Folding of Alzheimer's core PHF subunit revealed by monoclonal antibody 423. FEBS Lett. 568, 178 182.
124. Skrabana R., Sevcik J. Novak M. (2006) Intrinsically disordered proteins in the neurodegenerative process: formation of Tau protein paired helical filaments and their analysis. Cell.Mol. Neurobiol. 26 (7/8 1085 1097.
125. Sugino E., Nishiura C., Minoura K., In Y., Sumida M., Taniguchi T., Tomoo K. Ishida T. (2009) Three-/four-repeat-dependent aggregation profile of tau microtubule-binding domain clarified by dynamic light scattering analysis. Biochem. Biophys. Res. Commun. 385, 236 240.
126. Takahashi K., Uchida C., Shin R. W., Shimazaki K. Uchida T. (2008) Prolyl isomerase, Pin1: new findings of post-translational modifications and physiological substrates in cancer, asthma and Alzheimer's disease. Cell. Mol. Life Sci. 65, 359 375.
127. Taniguchi S., Suzuki N., Masuda M., Hisanaga S.-I., Iwatsubo T., Goedert M. Hasegawa M. (2005) Inhibition of heparin-induced tau filaments formation by phenothiazines, polyphenols and porphyrins. J. Biol. Chem. 280, 7614 7623.
128. Wang J. Z. Liu F. (2008) Microtubule-associated protein tau in development, degeneration and protection of neurons. Prog. Neurobiol. 85, 148 175.
129. Wang Y. P., Biernat J., Pickhardt M., Mandelkow E. Mandelkow E. M. (2007) Stepwise proteolysis liberates tau fragments that nucleate the Alzheimer-like aggregation of full-length tau in a neuronal cell model. Proc. Natl Acad. Sci. USA 104, 10252 10257.
130. Wei Y., Qu M. H., Wang X. S., Chen L., Wang D. L., Liu Y., Qian H. He R. Q. (2008) Binding to the minor groove of the double-strand, tau protein prevents DNA from damage by peroxidation. PLoS ONE 3 (7 e2600 (1-10).
131. Weingarten M. D., Lockwood A. H., Hwo S. Y. Kirschner M. W. (1975) A protein factor essential for microtubule assembly. Proc. Natl Acad. Sci. USA 72, 1858 1862.
132. Williams D. R. Lees A. J. (2009) Progressive supranuclear palsy: clinicopathological concepts and diagnostic challenges. Lancet Neurol. 8, 270 279.
133. Winton M. J., Joyce S., Zhukareva V., Practico D., Perl D. P., Galasko D., Craig U., Trojanowski J. Q. Lee V. M. Y. (2006) Characterization of tau pathologies in gray and white matter of Guam parkinsonism-dementia complex. Acta Neuropathol. 111, 401 412.
134. Wischik C. M., Novak M., Thøgersen H. C., Edwards P. C., Runswick M. J., Jakes R., Walker J. E., Milstein C., Rotht M. Klug A. (1988a) Isolation of a fragment of Tau derived from the core of the paired helical filament of Alzheimer disease. Proc. Natl Acad. Sci. USA 85, 4506 4510.
135. Wischik C. M., Novak M., Edwards P. C., Klug A., Tichelaar W. Crowther R. A. (1988b) Structural characterization of the core of paired helical filament of Alzheimer disease. Proc. Natl Acad. Sci. USA 85, 4884 4888.
136. Wischik C. M., Edwards P. C., Lai R. Y. K., Roth M. Harrington C. R. (1996) Selective inhibition of Alzheimer disease-like tau aggregation by phenothiazines. Proc. Natl Acad. Sci. USA 93, 11213 11218.
137. Yang L.-S. Ksiezak-Reding H. (1995) Calpain-induced proteolysis of normal human Tau and Tau associated with paired helical filaments. Eur. J. Biochem. 233, 9 17.
138. Yu C.-H., Si T., Wu W.-H., Hu J., Du J.-T., Zhao Y.-F. Li Y.-M. (2008) O-GlcNacylation modulates the self-aggregation ability of the fourth microtubule-binding repeat of tau. Biochem. Biophys. Res. Commun. 375, 59 62.
139. Zhang Y. J., Xu Y. F., Chen X. Q., Wang X. C. Wang J. Z. (2005) Nitration and oligomerization of Tau induced by peroxynitrite inhibit its microtubule-binding activity. FEBS Lett. 579, 2421 2427.
140. Zilka N., Filipcik P., Koson P., Fialova L., Skrabana R., Zilkova M., Rolkova G., Kontsekova E. Novak M. (2006) Truncated Tau from sporadic Alzheimer's disease suffices to drive neurofibrillary degeneration in vivo. FEBS Lett. 580, 3582 3588.