Can tau filaments be both physiologically beneficial and toxic?

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1739, Issue 2, 2005, Pages 260-267

  King, Michelle E ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Amyloid; Alzheimer's disease; Tau filament

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; HEAT SHOCK PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; TAU PROTEIN;

ALZHEIMER DISEASE; AMNESIA; AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; CORRELATION ANALYSIS; HUMAN; HUNTINGTON CHOREA; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; STATISTICAL SIGNIFICANCE;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; APOPTOSIS; HUMANS; NERVE DEGENERATION; NEUROFIBRILLARY TANGLES; OXIDATIVE STRESS; PHOSPHORYLATION; TAU PROTEINS;

EID: 10944224599     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2004.06.019     Document Type: Review

References (70)

1. D.J. Selkoe Alzheimer's disease: genes, proteins, and therapy Physiol. Rev. 81 2001 741 766
2. X. Cao, and T.C. Sudhof A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60 Science 293 2001 115 120
3. D. Edbauer, E. Winkler, J.T. Regula, B. Pesold, H. Steiner, and C. Haass Reconstitution of gamma-secretase activity Nat. Cell Biol. 5 2003 486 488
4. N. Takasugi, T. Tomita, I. Hayashi, M. Tsuruoka, M. Niimura, Y. Takahashi, G. Thinakaran, and T. Iwatsubo The role of presenilin cofactors in the gamma-secretase complex Nature 422 2003 438 441
5. D.W. Cleveland, S.Y. Hwo, and M.W. Kirschner Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin J. Mol. Biol. 116 1977 207 225
6. D.W. Cleveland, S.Y. Hwo, and M.W. Kirschner Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly J. Mol. Biol. 116 1977 227 247
7. S.C. Papasozomenos Tau protein immunoreactivity in dementia of the Alzheimer type: II. Electron microscopy and pathogenetic implications. Effects of fixation on the morphology of the Alzheimer's abnormal filaments Lab. Invest. 60 1989 375 389
8. S.C. Papasozomenos Tau protein immunoreactivity in dementia of the Alzheimer type. I. Morphology, evolution, distribution, and pathogenetic implications Lab. Invest. 60 1989 123 137
9. D.G. Drubin, D. Caput, and M.W. Kirschner Studies on the expression of the microtubule-associated protein, tau, during mouse brain development, with newly isolated complementary DNA probes J. Cell Biol. 98 1984 1090 1097
10. A. Ebneth, R. Godemann, K. Stamer, S. Illenberger, B. Trinczek, and E. Mandelkow Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease J. Cell Biol. 143 1998 777 794
11. K. Stamer, R. Vogel, E. Thies, E. Mandelkow, and E.M. Mandelkow Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress J. Cell Biol. 156 2002 1051 1063
12. M.G. Spillantini, J.R. Murrell, M. Goedert, M.R. Farlow, A. Klug, and B. Ghetti Mutation in the tau gene in familial multiple system tauopathy with presenile dementia Proc. Natl. Acad. Sci. U. S. A. 95 1998 7737 7741
13. P. Poorkaj, T.D. Bird, E. Wijsman, E. Nemens, R.M. Garruto, L. Anderson, A. Andreadis, W.C. Wiederholt, M. Raskind, and G.D. Schellenberg Tau is a candidate gene for chromosome 17 frontotemporal dementia Ann. Neurol. 43 1998 815 825
14. M. Hutton, C.L. Lendon, P. Rizzu, M. Baker, S. Froelich, H. Houlden, S. Pickering-Brown, S. Chakraverty, A. Isaacs, A. Grover, J. Hackett, J. Adamson, S. Lincoln, D. Dickson, P. Davies, R.C. Petersen, M. Stevens, E. de Graaff, E. Wauters, J. van Baren, M. Hillebrand, M. Joosse, J.M. Kwon, P. Nowotny, and P. Heutink Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17 Nature 393 1998 702 705
15. M. Hutton Missense and splice site mutations in tau associated with FTDP-17: multiple pathogenic mechanisms Neurology 56 2001 S21 S25
16. P.V. Arriagada, J.H. Growdon, E.T. Hedley-Whyte, and B.T. Hyman Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease Neurology 42 1992 631 639
17. P. Nacharaju, L. Ko, and S.H. Yen Characterization of in vitro glycation sites of tau J. Neurochem. 69 1997 1709 1719
18. E.S. Matsuo, R.W. Shin, M.L. Billingsley, A. Van deVoorde, M. O'Connor, J.Q. Trojanowski, and V.M. Lee Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau Neuron 13 1994 989 1002
19. N. Shahani, and R. Brandt Functions and malfunctions of the tau proteins Cell. Mol. Life Sci. 59 2002 1668 1680
20. M. Goedert, R. Jakes, Z. Qi, J.H. Wang, and P. Cohen 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 1995 2804 2807
21. P.J. Lu, G. Wulf, X.Z. Zhou, P. Davies, and K.P. Lu The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein Nature 399 1999 784 788
22. M. Hamdane, C. Smet, A.V. Sambo, A. Leroy, J.M. Wieruszeski, P. Delobel, C.A. Maurage, A. Ghestem, R. Wintjens, S. Begard, N. Sergeant, A. Delacourte, D. Horvath, I. Landrieu, G. Lippens, and L. Buee Pin1: a therapeutic target in Alzheimer neurodegeneration J. Mol. Neurosci. 19 2002 275 287
23. D.H. Geschwind Tau phosphorylation, tangles, and neurodegeneration: the chicken or the egg? Neuron 40 2003 457 460
24. J.C. Cruz, H.C. Tseng, J.A. Goldman, H. Shih, and L.H. Tsai Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles Neuron 40 2003 471 483
25. A. Schneider, J. Biernat, M. von Bergen, E. Mandelkow, and E.M. Mandelkow Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments Biochemistry 38 1999 3549 3558
26. A. Abraha, N. Ghoshal, T.C. Gamblin, V. Cryns, R.W. Berry, J. Kuret, and L.I. Binder C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease J. Cell Sci. 113 2000 3737 3745
27. T.C. Gamblin, R.W. Berry, and L.I. Binder Modeling tau polymerization in vitro: a review and synthesis Biochemistry 42 2003 15009 15017
28. T. Arendt, J. Stieler, A.M. Strijkstra, R.A. Hut, J. Rudiger, E.A. Van der Zee, T. Harkany, M. Holzer, and W. Hartig Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals J. Neurosci. 23 2003 6972 6981
29. D. Panda, J.C. Samuel, M. Massie, S.C. Feinstein, and L. Wilson Differential regulation of microtubule dynamics by three- and four-repeat tau: implications for the onset of neurodegenerative disease Proc. Natl. Acad Sci. U. S. A. 100 2003 9548 9553
30. M.C. Gastard, J.C. Troncoso, and V.E. Koliatsos Caspase activation in the limbic cortex of subjects with early Alzheimer's disease Ann. Neurol. 54 2003 393 398
31. V. Galvan, S. Chen, D. Lu, A. Logvinova, P. Goldsmith, E.H. Koo, and D.E. Bredesen Caspase cleavage of members of the amyloid precursor family of proteins J. Neurochem. 82 2002 283 294
32. D.C. Lu, S. Rabizadeh, S. Chandra, R.F. Shayya, L.M. Ellerby, X. Ye, G.S. Salvesen, E.H. Koo, and D.E. Bredesen A second cytotoxic proteolytic peptide derived from amyloid beta-protein precursor Nat. Med. 6 2000 397 404
33. F.G. Gervais, D. Xu, G.S. Robertson, J.P. Vaillancourt, Y. Zhu, J. Huang, A. LeBlanc, D. Smith, M. Rigby, M.S. Shearman, E.E. Clarke, H. Zheng, L.H. Van Der Ploeg, S.C. Ruffolo, N.A. Thornberry, S. Xanthoudakis, R.J. Zamboni, S. Roy, and D.W. Nicholson Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-beta precursor protein and amyloidogenic A beta peptide formation Cell 97 1999 395 406
34. T.C. Gamblin, F. Chen, A. Zambrano, A. Abraha, S. Lagalwar, A.L. Guillozet, M. Lu, Y. Fu, F. Garcia-Sierra, N. LaPointe, R. Miller, R.W. Berry, L.I. Binder, and V.L. Cryns Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease Proc. Natl. Acad. Sci. U. S. A. 100 2003 10032 10037
35. M.A. Smith, G. Casadesus, J.A. Joseph, and G. Perry Amyloid-beta and tau serve antioxidant functions in the aging and Alzheimer brain Free Radic. Biol. Med. 33 2002 1194 1199
36. R. Castellani, K. Hirai, G. Aliev, K.L. Drew, A. Nunomura, A. Takeda, A.D. Cash, M.E. Obrenovich, G. Perry, and M.A. Smith Role of mitochondrial dysfunction in Alzheimer's disease J. Neurosci. Res. 70 2002 357 360
37. A. Eckert, U. Keil, C.A. Marques, A. Bonert, C. Frey, K. Schussel, and W.E. Muller Mitochondrial dysfunction, apoptotic cell death, and Alzheimer's disease Biochem. Pharmacol. 66 2003 1627 1634
38. T.C. Gamblin, M.E. King, J. Kuret, R.W. Berry, and L.I. Binder Oxidative regulation of fatty acid-induced tau polymerization Biochemistry 39 2000 14203 14210
39. B.A. Bahr, and J. Bendiske The neuropathogenic contributions of lysosomal dysfunction J. Neurochem. 83 2002 481 489
40. M.Y. Sherman, and A.L. Goldberg Cellular defenses against unfolded proteins: a cell biologist thinks about neurodegenerative diseases Neuron 29 2001 15 32
41. A.L. Schwartz, and A. Ciechanover The ubiquitin-proteasome pathway and pathogenesis of human diseases Annu. Rev. Med. 50 1999 57 74
42. O. Goldbaum, M. Oppermann, M. Handschuh, D. Dabir, B. Zhang, M.S. Forman, J.Q. Trojanowski, V.M. Lee, and C. Richter-Landsberg Proteasome inhibition stabilizes tau inclusions in oligodendroglial cells that occur after treatment with okadaic acid J. Neurosci. 23 2003 8872 8880
43. M. Rapoport, H.N. Dawson, L.I. Binder, M.P. Vitek, and A. Ferreira Tau is essential to beta-amyloid-induced neurotoxicity Proc. Natl. Acad. Sci. U. S. A. 99 2002 6364 6369
44. R. Kayed, E. Head, J.L. Thompson, T.M. McIntire, S.C. Milton, C.W. Cotman, and C.G. Glabe Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300 2003 486 489
45. A.V. Savonenko, G.M. Xu, D.L. Price, D.R. Borchelt, and A.L. Markowska Normal cognitive behavior in two distinct congenic lines of transgenic mice hyperexpressing mutant APP SWE Neurobiol. Dis. 12 2003 194 211
46. C.W. Wittmann, M.F. Wszolek, J.M. Shulman, P.M. Salvaterra, J. Lewis, M. Hutton, and M.B. Feany Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles Science 293 2001 711 714
47. G.F. Hall, J. Yao, and G. Lee Human tau becomes phosphorylated and forms filamentous deposits when overexpressed in lamprey central neurons in situ Proc. Natl. Acad. Sci. U. S. A. 94 1997 4733 4738
48. G.F. Hall, V.M. Lee, G. Lee, and J. Yao Staging of neurofibrillary degeneration caused by human tau overexpression in a unique cellular model of human tauopathy Am. J. Pathol. 158 2001 235 246
49. R. de Silva, and M. Farrer Tau neurotoxicity without the lesions: a fly challenges a tangled web Trends Neurosci. 25 2002 327 329
50. G.F. Hall, S. Lee, and J. Yao Neurofibrillary degeneration can be arrested in an in vivo cellular model of human tauopathy by application of a compound which inhibits tau filament formation in vitro J. Mol. Neurosci. 19 2002 253 260
51. B. Trinczek, A. Ebneth, E.M. Mandelkow, and E. Mandelkow Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles J. Cell Sci. 112 1999 2355 2367
52. E.M. Mandelkow, K. Stamer, R. Vogel, E. Thies, and E. Mandelkow Clogging of axons by tau, inhibition of axonal traffic and starvation of synapses Neurobiol. Aging 24 2003 1079 1085
53. M. von Bergen, P. Friedhoff, J. Biernat, J. Heberle, and E. Mandelkow Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif (306VQIVYK311) forming beta structure Proc. Natl. Acad. Sci. U. S. A. 97 2000 5129 5134
54. G. Perry, M. Kawai, M. Tabaton, M. Onorato, P. Mulvihill, P. Richey, A. Morandi, J.A. Connolly, and P. Gambetti Neuropil threads of Alzheimer's disease show a marked alteration of the normal cytoskeleton J. Neurosci. 11 1991 1748 1755
55. C. Bancher, C. Brunner, H. Lassmann, H. Budka, K. Jellinger, G. Wiche, F. Seitelberger, I. Grundke-Iqbal, K. Iqbal, and H.M. Wisniewski Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease Brain Res. 477 1989 90 99
56. J. Lauckner, P. Frey, and C. Geula Comparative distribution of tau phosphorylated at Ser262 in pre-tangles and tangles Neurobiol. Aging 24 2003 767 776
57. P. Friedhoff, A. Schneider, E.M. Mandelkow, and E. Mandelkow Rapid assembly of Alzheimer-like paired helical filaments from microtubule-associated protein tau monitored by fluorescence in solution Biochemistry 37 1998 10223 10230
58. T.C. Gamblin, M.E. King, H. Dawson, M.P. Vitek, J. Kuret, R.W. Berry, and L.I. Binder In vitro polymerization of tau protein monitored by laser light scattering: method and application to the study of FTDP-17 mutants Biochemistry 39 2000 6136 6144
59. M. Hasegawa, R.A. Crowther, R. Jakes, and M. Goedert Alzheimer-like changes in microtubule-associated protein Tau induced by sulfated glycosaminoglycans. Inhibition of microtubule binding, stimulation of phosphorylation, and filament assembly depend on the degree of sulfation J. Biol. Chem. 272 1997 33118 33124
60. P. Friedhoff, M. von Bergen, E. Mandelkow, and P. Davies A nucleated assembly mechanism of Alzheimer paired helical filaments Proc. Natl. Acad. Sci. U. S. A. 95 1998 15712 15717
61. M.E. King, V. Ahuja, L.I. Binder, and J. Kuret Ligand-dependent tau filament formation: implications for Alzheimer's disease progression Biochemistry 38 1999 14851 14859
62. D.M. Wilson, and L.I. Binder Polymerization of microtubule-associated protein tau under near-physiological conditions J. Biol. Chem. 270 1995 24306 24314
63. D.M. Wilson, and L.I. Binder 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 1997 2181 2195
64. M. Goedert, R. Jakes, M.G. Spillantini, M. Hasegawa, M.J. Smith, and R.A. Crowther Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans [see comments] Nature 383 1996 550 553
65. H. Wille, G. Drewes, J. Biernat, E.M. Mandelkow, and E. Mandelkow Alzheimer-like paired helical filaments and antiparallel dimers formed from microtubule-associated protein tau in vitro J. Cell Biol. 118 1992 573 584
66. T. Kampers, P. Friedhoff, J. Biernat, E.M. Mandelkow, and E. Mandelkow RNA stimulates aggregation of microtubule-associated protein tau into Alzheimer-like paired helical filaments FEBS Lett. 399 1996 344 349
67. M. Arrasate, M. Perez, R. Armas-Portela, and J. Avila Polymerization of tau peptides into fibrillar structures. The effect of FTDP-17 mutations FEBS Lett. 446 1999 199 202
68. M. DeTure, L.W. Ko, C. Easson, and S.H. Yen Tau assembly in inducible transfectants expressing wild-type or FTDP-17 tau Am. J. Pathol. 161 2002 1711 1722
69. M. Goedert, R. Jakes, and R.A. Crowther Effects of frontotemporal dementia FTDP-17 mutations on heparin-induced assembly of tau filaments FEBS Lett. 450 1999 306 311
70. P. Nacharaju, J. Lewis, C. Easson, S. Yen, J. Hackett, M. Hutton, and S.H. Yen Accelerated filament formation from tau protein with specific FTDP-17 missense mutations FEBS Lett. 447 1999 195 199