Earliest stages of tau conformational changes are related to the appearance of a sequence of specific phospho-dependent tau epitopes in Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 12, Issue 4, 2007, Pages 365-375

  Luna Muñoz, José ^a,c   Chávez Macías, Laura ^b   García Sierra, Francisco ^a   Mena, Raúl ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c DEPARTAMENTO DE SISTEMAS BIOLÓGICOS   (Mexico)

Author keywords

Alzheimer's disease; Conformational changes; Hyperphosphorylation; Paired helical filament formation; Tau protein

Indexed keywords

EPITOPE; TAU PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN TISSUE; CLINICAL ARTICLE; CONFOCAL MICROSCOPY; DEGENERATIVE DISEASE; ENTORHINAL CORTEX; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; NEUROFIBRILLARY TANGLE; NEUROLOGIC DISEASE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 38049030324     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2007-12410     Document Type: Article

References (46)

1. J.C. Augustinack, A. Schneider, E.M. Mandelkow and B.T. Hyman, Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease, Acta Neuropathol 103 (2002), 26-35.
2. 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.
3. A.A. Bielska and N.J. Zondlo, Hyperphosphorylation of tau induces local polyproline II helix, Biochemistry 45 (2006), 5527-5537.
4. J. Biernat, E.M. Mandelkow, C. Schroter, B. Lichtenberg-Kraag, B. Steiner, B. Berling, H. Meyer, M. Mercken, A. Vandermeeren, M. Goedert and E. Mandelkow, 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.
5. L.I. Binder, A.L. Guillozet-Bongaarts, F. Garcia-Sierra and R.W. Berry, Tau, tangles, and Alzheimer's disease, Biochim Biophys Acta 1739 (2005), 216-223.
6. 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.
7. H. Braak and E. Braak, Neuropathological stageing of Alzheimer-related changes, Acta Neuropathol 82 (1991), 239-259.
8. 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.
9. V. Búee-Scherrer, B. Pau, O. Condamines, C. Mourton-Guilles, 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 39 (1996), 79-88.
10. G. Carmel, E.M. Mager, L.I. Binder and J. Kuret, The structural basis of monoclonal antibody Alz50s selectivity for Alzheimer's Disease Pathology, J Biol Chem 271 (1996), 32789-32795.
11. W. Chun and G.V. Johnson, The role of tau phosphorylation and cleavage in neuronal cell death, Front Biosci 12 (2007), 733-756.
12. N.L. Daly, R. Hoffmann, Jr. L. Otvos and D.J. Craik, Role of phosphorylation in the conformation of tau peptides implicated in Alzheimer's disease, Biochem 39 (2000), 9039-9046.
13. L. Fasulo, G. Ugolini, M. Visintin, A. Bradbury, C. Brancolini, V. Verzillo, M. Novak and A. Cattaneo, The neuronal microtubule-associated protein tau is a substrate for caspase-3 and an effector of apoptosis, J Neurochem 75 (2000), 624-633.
14. M. Galv́an, J.P. David, A. Delacourte, J. Luna and R. Mena, Sequence of neurofibrillary changes in aging and Alzheimer's disease: A confocal study with phospho-tau antibody, AD2, J Alzheimers Dis 3 (2001), 417-425.
15. T.C. Gamblin, R.W. Berry and L.I. Binder, Modeling tau polymerization in vitro: a review and synthesis, Biochemistry 42 (2003), 15009-15017.
16. T.C. Gamblin, F. Chen, A. Zambrano, A. Abraha, S. Lagalwar, A.L. Guillozet, M. Lu, Y. Fu, F. García-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 USA 100 (2003), 10032-10037.
17. F. García-Sierra, N. Goshal, B. Quinn, W.R. Berry and I.L. Binder, Conformational changes and truncation of tau protein during tangle evolution in Alzheimer's disease, J Alzheimer's Dis 5 (2003), 65-77.
18. F. García-Sierra, J.J. Hauw, C. Duyckaerts, C.M. Wischik, J. Luna-MunTild;oz and R. Mena, The extent of neurofibrillary pathology in perforant pathway neurons is the key determinant of dementia in very old, Acta Neuropathol 100 (2000), 29-35.
19. F. Garcia-Sierra, C.M. Wischik, C.R. Harrington, J. Luna-Mũnoz 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.
20. M. Goedert, R. Jakes, R.A. Crowther, J. Six, U. Lubke, M. Vandermeeren, P. Cras, J.Q. Trojanowski and V.M-Y. 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.
21. 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.
22. M. Goedert, M.G. Spillantini, R. Jakes, D. Rutherford and R.A. Crowther, Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease, Neuron 3 (1989), 519-526.
23. A. Guillozet-Bongaarts, M.E. Cahill, V.L. Cryns, M.R. Reynolds, R.W. Berry and L.I. Binder, Pseudophosphorylation of tau at serine 422 inhibits caspase cleavage: in vitro evidence and implications for tangle formation in vivo, J Neurochem 97 (2006), 1005-1014.
24. A. Guillozet-Bongaarts. F. García-Sierra, M.R. Reynolds, P. Horowitz, Y. Fu, T. Wang, M. Cahill, H. Biogio, W. Berry and L.I. Binder, Tau truncation during neurofibrillary tangle evolution in Alzheimer's disease, Neurobiol Aging 26 (2005), 1015-1022.
25. B.T. Hyman, J.C. Augustinack and M. Ingelsson, Transcriptional and conformational change of tau molecule in Alzheimer's disease, Biochem Biophy Acta 1739 (2005), 150-157.
26. A.G. 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.
27. A.G. Jicha, R. Bowser, I.G. Kasam and D. Peter, Alz-50 and MC-1 a new monoclonal antibody raised to paired helical filaments, recognize conformational epítopes on recombinant tau, J Neurosc Res 48 (1997), 128-132.
28. A.G. Jicha, E. Lane, I. Vincent, Jr., L. Otvos, R. Hoffman and P. Davies, A conformational- and phosphorylation- dependent antibody recognizing the paired helical filaments of Alzheimer's disease, J Neurochem 69 (1997), 2087-2095.
29. M. Kidd, Paired helical filaments in electron microscopy of Alzheimer's disease, Nature 197 (1963), 192-193.
30. T. Kimura, T. Ono, J. Takamatsu, H. Yamamoto, K. Ikegami, A. Kondo, M. Hasegawa, Y. Ihara, E. Miyamoto and T. Miyakawa, Sequential changes of tau-site-specific phosphorylation during development of paired helical filaments, Dementia 7 (1966), 177-181.
31. J. Kondo, T. Honda and H. Mori, The carboxyl third of tau is tightly bound to paired helical filaments, Neuron 1 (1988), 827-834.
32. J. Luna-Munoz, F. García-Sierra, V. Falcon, I. Menendez, L. Chavez-Macias and R. Mena, Regional conformational change involving phosphorylation of tau protein at the Thr231, pre cedes the structural change detected by Alz-50 antibody in Alzheimer's disease, J Alzheimers Dis 8 (2005), 29-41.
33. G. McKhann, D. Drachman, M. Folstein, R. Katzman, D. Price and E.M. Stadlan, Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease, Neurology 34 (1984), 939-944.
34. 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.
35. R. Mena, P.C. Edwards, O. Pérez-Olvera and C.M. Wischik, Monitoring pathological assembly of tau and β-amyloid proteins in Alzheimer's disease, Acta Neuropathol 89 (1995), 50-56.
36. M. Novak, Truncated tau protein as a new marker for Alzheimer's disease, Acta Virol 38 (1994), 173-189.
37. R.A. Rissman, W.W. Poon, M. Blurton-Jones, S. Oddo, R. Torp, M.P. Vitek, F.M. LaFerla, T.T. Rohn and C.W. Cotman, Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology, J Clin Invest 114 (2004), 121-130.
38. P. Seubert, C. Vigo-Pelfrey, F. Esch, M. Lee, H. Dovey, D. Davis, S. Sinha, M. Schlossmacher, J. Whaley and C. Swindlehurst, Isolation and quantification of soluble Alzheimer's betapeptide from biological fluids, Nature 359 (1992), 325-327.
39. R. Skrabana, P. Kontsek, A. Mederlyova, K. Iqbal and M. Novak, Folding of Alzheimer's core PHF subunit revealed by monoclonal antibody 423, FEBS Lett 568 (2004), 178-182.
40. 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.
41. T. Uchihara, A. Nakamura, M. Yamazaki and O. Mori, Taupositive neurons in corticobasal degeneration and Alzheimer's disease - distinction by thiazin red and silver impregnations, Acta Neuropathol 100 (2000), 385-389.
42. T. Uchihara, A. Nakamura, M. Yamazaki and O. Mori, Evolution from pretangle neurons to neurofibrillary tangles monitored by thiazin red combined with Gallyas method and double immunofluorescence, Acta Neuropathol 101 (2001), 535-539.
43. C.L. Weaver, M. Espinoza, Y. Kress and P. Davies, Conformational change as one of the earliest alteration of tau in Alzheimer's disease, Neurobiol Aging 21 (2000), 719-727.
44. 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's disease, Proc Nat Acad Sci USA 85 (1988), 4884-4888.
45. B. Wolozin and P. Davies, Alzheimer-related neuronal protein A68: specificity and distribution, Ann Neurol 22 (1987), 521-526.
46. Zheng-Fichhofer, J. Biernat, E.-M. Mandelkow, S. Illenberger and R. Godemann, Sequential phosphorylation of tau by glycogen synthetase kinase-3β and protein kinase A at Thr212 and Ser 214 generates the Alzheimer-specific epitope of antibody AT100 and requires a paired-helical- filament-like conformation, Eur J Biochem 252 (1998), 542-552.