Conformational changes and truncation of tau protein during tangle evolution in Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 5, Issue 2, 2003, Pages 65-77

  García Sierra, Francisco ^a   Ghoshal, Nupur ^a   Quinn, Bruce ^a   Berry, Robert W ^a   Bínder, Lester I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Neurofibrillary tangle; Pathology; Progression; Tau; Truncation

Indexed keywords

EPITOPE; PROTEIN ALZ 50; PROTEIN ANTIBODY; PROTEIN TAU 66; TAU PROTEIN; UNCLASSIFIED DRUG;

AGED; ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CLINICAL ARTICLE; CONFORMATIONAL TRANSITION; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; MALE; MOLECULAR RECOGNITION; NEUROFIBRILLARY TANGLE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

EID: 0038291981     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2003-5201     Document Type: Article

References (56)

1. 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.
2. 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.
3. M.J. Ball, S. Griffin-Brooks, J.A. MacGregor, B. Nagy, E. Ojalvo-Rose and P.H. Fewster, Neuropathological definition of Alzheimer disease: multivariate analyses in the morphometric distinction between Alzheimer dementia and normal aging, Alzheimer Dis Assoc Disord 2 (1988), 29-37.
4. C. Bancher, C. Brunner, H. Lassmann, H. Budka, K. Jellinger, G. Wiche, F. Seitelberger, I. Grundkebal, 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.
5. L. Berg, D.W. McKeel, Jr., J.P. Miller, J. Baty and J.C. Morris, Neuropathological indexes of Alzheimer's disease in demented and nondemented persons aged 80 years and older, Arch Neurol 50 (1993), 349-358.
6. J. Biernat, E.M. Mandelkow, C. Schroter, B. Lichtenberg-Kraag, B. Steiner, B. Berling, H. Meyer, M. Mercken, A. Vandermeeren, M. Goedert et al., The switch of tau protein to an Alzheimer-like state includes the phosphorylation of two serine-proline motifs upstream of the microtubule binding region, Embo J 11 (1992), 1593-1597.
7. W. Bondareff, C. Harrington, C.M. Wischik, D.L. Hauser and M. Roth, Immunohistochemical staging of neurofibrillary degeneration in Alzheimer's disease, J Neuropathol Exp Neurol 53 (1994), 158-164.
8. W. Bondareff, C.R. Harrington, C.M. Wischik, D.L. Hauser and M. Roth, Absence of abnormal hyperphosphorylation of tau in intracellular tangles in Alzheimer's disease, J Neuropathol Exp Neurol 54 (1995), 657-663.
9. W. Bondareff, C.M. Wischik, M. Novak, W.B. Amos, A. Klug and M. Roth, Molecular analysis of neurofibrillary degeneration in Alzheimer's disease. An immunohistochemical study, Am J Pathol 137 (1990), 711-723.
10. E. Braak, H. Braak and E.M. Mandelkow, A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads, Acta Neuropathol 87 (1994), 554-567.
11. H. Braak and E. Braak, Neuropathological stageing of Alzheimer-related changes, Acta Neuropathol 82 (1991), 239-259.
12. J.P. Brion, D.P. Hanger, A.M. Couck and B.H. Anderton, A68 proteins in Alzheimer's disease are composed of several tau isoforms in a phosphorylated state which affects their electrophoretic mobilities, Biochem J 279(Pt 3) (1991), 831-836.
13. V. Buee-Scherrer, O. Condamines, C. Mourton-Gilles, R. Jakes, M. Goedert, B. Pau and A. Delacourte, AD2, a phosphorylation-dependent monoclonal antibody directed against tau proteins found in Alzheimer's disease, Brain Res Mol Brain Res 39 (1996), 79-88.
14. G. Carmel, E.M. Mager, L.I. Binder and J. Kuret, The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology, J Biol Chem 271 (1996), 32789-32795.
15. D.W. Dickson, H. Ksiezak-Reding, W.K. Liu, P. Davies, A. Crowe and S.H. Yen, Immunocytochemistry of neurofibrillary tangles with antibodies to subregions of tau protein: identification of hidden and cleaved tau epitopes and a new phosphorylation site, Acta Neuropathol 84 (1992), 596-605.
16. F. Garcia-Sierra, C.M. Wischik, C.R. Harrington, J. Luna-Munoz and R. Mena, 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 (2001), 65-77.
17. N. Ghoshal, F. Garcia-Sierra, Y. Fu, L.A. Beckett, E.J. Mufson, J. Kuret, R.W. Berry and L.I. Binder, Tau-66: Evidence for a novel tau conformation in Alzheimer's disease, J Neurochem 77 (2001), 1372-1385.
18. N. Ghoshal, F. Garcia-Sierra, J. Wuu, S. Leurgans, D.A. Bennett, R.W. Berry and L.I. Binder, Tau Conformational Changes Correspond to Impairments of Episodic Memory in Mild Cognitive Impairment and Alzheimer's Disease, Exp Neurol 177 (2002), 475-493.
19. M. Goedert, Tau protein and the neurofibrillary pathology of Alzheimer's disease, Trends Neurosci 16 (1993), 460-465.
20. M. Goedert, R. Jakes, R.A. Crowther, P. Cohen, E. Vanmechelen, M. Vandermeeren and P. Cras, Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer's disease: identification of phosphorylation sites in tau protein, Biochem J 301 (1994), 871-877.
21. M. Goedert, R. Jakes, R.A. Crowther, J. Six, U. Lubke, M. Vandermeeren, P. Cras, J.Q. Trojanowski and V.M. Lee, The abnormal phosphorylation of tau protein at Ser-202 in Alzheimer disease recapitulates phosphorylation during development, Proc Natl Acad Sci USA 90 (1993), 5066-5070.
22. M. Goedert, R. Jakes and E. Vanmechelen, Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205, Neurosci Lett 189 (1995), 167-169.
23. M. Goedert, M.G. Spillantini, N.J. Cairns and R.A. Crowther, Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms, Neuron 8 (1992), 159-168.
24. I. Grundke-Iqbal, K. Iqbal, Y.C. Tung, M. Quinlan, H.M. Wisniewski and L.I. Binder, Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology, Proc Natl Acad Sci USA 83 (1986), 4913-4917.
25. T. Hagestedt, B. Lichtenberg, H. Wille, E.M. Mandelkow and E. Mandelkow, Tau protein becomes long and stiff upon phosphorylation: correlation between paracrystalline structure and degree of phosphorylation, J Cell Biol 109 (1989), 1643-1651.
26. B.T. Hyman, G.W. Van Hoesen, B.L. Wolozin, P. Davies, L.J. Kromer and A.R. Damasio, Alz-50 antibody recognizes Alzheimer-related neuronal changes, Ann Neurol 23 (1988), 371-379.
27. G.A. Jicha, B. Berenfeld and P. Davies, Sequence requirements for formation of conformational variants of tau similar to those found in Alzheimer's disease, J Neurosci Res 55 (1999), 713-723.
28. G.A. Jicha, R. Bowser, I.G. Kazam and P. Davies, Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau, J Neurosci Res 48 (1997), 128-132.
29. M. Kidd, Paired helical filaments in electron microscopy of Alzheimer's disease, Nature 197 (1963), 192-193.
30. K.S. Kosik, C.L. Joachim and D.J. Selkoe, Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease, Proc Natl Acad Sci USA 83 (1986), 4044-4048.
31. K.S. Kosik, L.D. Orecchio, L. Binder, J.Q. Trojanowski, V.M. Lee and G. Lee, Epitopes that span the tau molecule are shared with paired helical filaments, Neuron 1 (1988), 817-825.
32. V.M. Lee, B.J. Balin, L. Otvos, Jr., and J.Q. Trojanowski, A68: a major subunit of paired helical filaments and derivatized forms of normal tau, Science 251 (1991), 675-678.
33. A.C. McKee, K.S. Kosik, N.W. Kowall, Neuritic pathology and dementia in Alzheimer's disease, Ann Neurol 30 (1991), 156-165.
34. R. Mena, P. Edwards, O. Perez-Olvera and C.M. Wischik, Monitoring pathological assembly of tau and beta-amyloid proteins in Alzheimer's disease, Acta Neuropathol 89 (1995), 50-56.
35. R. Mena, P.C. Edwards, C.R. Harrington, E.B. Mukaetova-Ladinska and C.M. Wischik, Staging the pathological assembly of truncated tau protein into paired helical filaments in Alzheimer's disease, Acta Neuropathol 91 (1996), 633-641.
36. R. Mena, C.M. Wischik, M. Novak, C. Milstein and A.C. Cuello, A progressive deposition of paired helical filaments (PHF) in the brain characterizes the evolution of dementia in Alzheimer's disease. An immunocytochemical study with a monoclonal antibody against the PHF core, J Neuropathol Exp Neurol 50 (1991), 474-490.
37. P.T. Nelson and C.B. Saper, Injections of okadaic acid, but not beta-amyloid peptide, induce Alz-50 immunoreactive dystrophic neurites in the cerebral cortex of sheep, Neurosci Lett 208 (1996), 77-80.
38. P.T. Nelson and C.B. Saper, Ultrastructure of neurofibrillary tangles in the cerebral cortex of sheep, Neurobiol Aging 16 (1995), 315-323.
39. M. Novak, R. Jakes, P.C. Edwards, C. Milstein and C.M. Wischik, Difference between the tau protein of Alzheimer paired helical filament core and normal tau revealed by epitope analysis of monoclonal antibodies 423 and 7.51, Proc Natl Acad Sci USA 88 (1991), 5837-5841.
40. M. Novak, J. Kabat and C.M. Wischik, Molecular characterization of the minimal protease resistant tau unit of the Alzheimer's disease paired helical filament, Embo J 12 (1993), 365-370.
41. D.B. Rye, J. Leverenz, S.G. Greenberg, P. Davies and C.B. Saper, The distribution of Alz-50 immunoreactivity in the normal human brain, Neuroscience 56 (1993), 109-127.
42. M.L. Schmidt, R.E. Gur, R.C. Gur and J.Q. Trojanowski, Intraneuronal and extracellular neurofibrillary tangles exhibit mutually exclusive cytoskeletal antigens, Ann Neurol 23 (1988), 184-189.
43. O. Schweers, E. Schonbrunn-Hanebeck, A. Marx and E. Mandelkow, Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for beta-structure, J Biol Chem 269 (1994), 24290-23297.
44. M. Tabaton, S. Cammarata, G. Mancardi, V. Manetto, L. Autilio-Gambetti, G. Perry and P. Gambetti, Ultrastructural localization of beta-amyloid, tau, and ubiquitin epitopes in extracellular neurofibrillary tangles, Proc Natl Acad Sci USA 88 (1991), 2098-2102.
45. M. Tabaton, P.J. Whitehouse, G. Perry, P. Davies, L. Autilio-Gambetti and P. Gambetti, Alz 50 recognizes abnormal filaments in Alzheimer's disease and progressive supranuclear palsy, Ann Neurol 24 (1988), 407-413.
46. R.D. Terry, N.K. Gonatas and M. Weiss, Ultrastructural studies in Alzheimer's disease presenile dementia, Am J Pathol 44 (1964), 669-697.
47. J.Q. Trojanowski and V.M. Lee, Phosphorylation of paired helical filament tau in Alzheimer's disease neurofibrillary le sions: focusing on phosphatases, Faseb J 9 (1995), 1570-1576.
48. N.V. Uboga and J.L. Price, Formation of diffuse and fibrillar tangles in aging and early Alzheimer's disease, Neurobiol Aging 21 (2000), 1-10.
49. G.W. Van Hoesen, B.T. Hyman and A.R. Damasio, Entorhinal cortex pathology in Alzheimer's disease, Hippocampus 1 (1991), 1-8.
50. C.L. Weaver, M. Espinoza, Y. Kress and P. Davies, Conformational change as one of the earliest alterations of tau in Alzheimer's disease, Neurobiol Aging 21 (2000), 719-727.
51. C.M. Wischik, P.C. Edwards, R.Y. Lai, H.N. Gertz, J.H. Xuereb, E.S. Paykel, C. Brayne, F.A. Huppert, E.B. Mukaetova-Ladinska, R. Mena et al., Quantitative analysis of tau protein in paired helical filament preparations: implications for the role of tau protein phosphorylation in PHF assembly in Alzheimer's disease, Neurobiol Aging 16 (1995), 409-417; discussion 418-431.
52. C.M. Wischik, P.C. Edwards, R.Y. Lai, M. Roth and C.R. Harrington, Selective inhibifion of Alzheimer disease-like tau aggregation by phenothiazines, Proc Natl Acad Sci USA 93 (1996), 11213-11218.
53. C.M. Wischik, M. Novak, P.C. Edwards, A. Klug, W. Tichelaar and R.A. Crowther, Structural characterization of the core of the paired helical filament of Alzheimer disease, Proc Natl Acad Sci USA 85 (1988), 4884-4888.
54. C.M. Wischik, M. Novak, H.C. Thogersen, P.C. Edwards, M.J. Runswick, R. Jakes, J.E. Walker, C. Milstein, M. Roth and A. Klug, Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease, Proc Natl Acad Sci USA 85 (1988), 4506-4510.
55. B.L. Wolozin, A. Pruchnicki, D.W. Dickson and P. Davies, A neuronal antigen in the brains of Alzheimer patients, Science 232 (1986), 648-650.
56. J.G. Wood, S.S. Mirra, N.J. Pollock and L.I. Binder, 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 (1986), 4040-4043.