N-terminal fragments of tau inhibit full-length tau polymerization in vitro

Biochemistry

Volumn 45, Issue 42, 2006, Pages 12859-12866

  Horowitz, Peleg M ^a   LaPointe, Nichole ^a   Guillozet Bongaarts, Angela L ^a   Berry, Robert W ^a   Binder, Lester I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CONFORMATIONS; DISEASES; ENZYME INHIBITION; MONOMERS; POLYMERIZATION;

FILAMENTS; INHIBITORY EFFECTS; N-TERMINAL FRAGMENTS;

PROTEINS;

ARACHIDONIC ACID; MICROTUBULE ASSOCIATED PROTEIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY TAU 7; RECOMBINANT PROTEIN; TAU PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CENTRIFUGATION; CONFORMATIONAL TRANSITION; ELECTRON MICROSCOPY; EPITOPE MAPPING; FRONTOTEMPORAL DEMENTIA; IN VITRO STUDY; MICELLE; PRIORITY JOURNAL; PROTEIN POLYMERIZATION;

AMINO ACID SEQUENCE; ARACHIDONIC ACID; BINDING SITES; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; TAU PROTEINS;

EID: 33750380827     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061325g     Document Type: Article

References (52)

1. Johnson, G. V. W., and Jenkins, S. M. (1996) Tau protein in normal and Alzheimer's disease brain, Alzheimer's Dis. Rev. 1, 38-54.
2. Johnson, G. V. W., and Hartigan, J. A. (1998) Tau protein in normal and Alzheimer's disease brain: An update, Alzheimer's Dis. Rev. 3, 125-141.
3. Duyckaerts, C., Colle, M. A., Dessi, F., Piette, F., and Hauw, J. J. (1998) Progression of Alzheimer histopathological changes, Acta Neurol. Belg. 98, 180-185.
4. Binder, L. I., Guillozet-Bongaarts, A. L., Garcia-Sierra, F., and Berry, R. W. (2005) Tau, tangles, and Alzheimer's disease, Biochim. Biophys. Acta 1739, 216-223.
5. Lee, V. M., Goedert, M., and Trojanowski, J. Q. (2001) Neurodegenerative tauopathies, Annu. Rev. Neurosci. 24, 1121-1159.
6. Hutton, M. (2001) Missense and splice site mutations in tau associated with FTDP-17: Multiple pathogenic mechanisms, Neurology 56, S21-S25.
7. Poorkaj, P., Muma, N. A., Zhukareva, V., Cochran, E. J., Shannon, K. M., Hurtig, H., Koller, W. C., Bird, T. D., Trojanowski, J. Q., Lee, V. M., and Schellenberg, G. D. (2002) An R5L tau mutation in a subject with a progressive supranuclear palsy phenotype, Ann. Neurol. 52, 511-516.
8. Braak, H., and Braak, E. (1995) Staging of Alzheimer's disease-related neurofibrillary changes, Neurobiol. Aging 16, 271-284.
9. Mitchell, T. W., Mufson, E. J., Schneider, J. A., Cochran, E. J., Nissanov, J., Han, L. Y., Bienias, J. L., Lee, V. M., Trojanowski, J. Q., Bennett, D. A., and Arnold, S. E. (2002) Parahippocampal tau pathology in healthy aging, mild cognitive impairment, and early Alzheimer's disease, Ann. Neurol. 51, 182-189.
10. Ghoshal, N., Garcia-Sierra, F., Wuu, J., Leurgans, S., Bennett, D. A., Berry, R. W., and 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.
11. Schweers, O., Schonbrunn-Hanebeck, E., Marx, A., and Mandelkow, E. (1994) Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for β-structure, J. Biol. Chem. 269, 24290-24297.
12. 1H NMR spectroscopy, Biochem. Biophys. Res. Commun. 294, 210-214.
13. Berry, R. W., Abraha, A., Lagalwar, S., LaPointe, N., Gamblin, T. C., Cryns, V. L., and Binder, L. I. (2003) Inhibition of tau polymerization by its carboxy-terminal caspase cleavage fragment, Biochemistry 42, 8325-8331.
14. Esposito, G., Viglino, P., Novak, M., and Cattaneo, A. (2000) The solution structure of the C-terminal segment of tau protein, J. Pept. Sci. 6, 550-559.
15. Syme, C. D., Blanch, E. W., Holt, C., Jakes, R., Goedert, M., Hecht, L., and Barron, L. D. (2002) A Raman optical activity study of rheomorphism in caseins, synucleins and tau. New insight into the structure and behaviour of natively unfolded proteins, Eur. J. Biochem. 269, 148-156.
16. Jeganathan, S., von Bergen, M., Brutlach, H., Steinhoff, H. J., and Mandelkow, E. (2006) Global hairpin folding of tau in solution, Biochemistry 45, 2283-2293.
17. Minoura, K., Yao, T. M., Tomoo, K., Sumida, M., Sasaki, M., Taniguchi, T., and Ishida, T. (2004) Different associational and conformational behaviors between the second and third repeat fragments in the tau microtubule-binding domain, Eur. J. Biochem. 271, 545-552.
18. Minoura, K., Mizushima, F., Tokimasa, M., Hiraoka, S., Tomoo, K., Sumida, M., Taniguchi, T., and Ishida, T. (2005) Structural evaluation of conformational transition state responsible for self-assembly of tau microtubule-binding domain, Biochem. Biophys. Res. Commun. 327, 1100-1104.
19. von Bergen, M., Friedhoff, P., Biernat, J., Heberle, J., and Mandelkow, E. (2000) Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif (306VQIVYK311) forming β structure, Proc. Natl. Acad. Sci. U.S.A. 97, 5129-5134.
20. Barghorn, S., Davies, P., and Mandelkow, E. (2004) Tau paired helical filaments from Alzheimer's disease brain and assembled in vitro are based on β-structure in the core domain, Biochemistry 43, 1694-1703.
21. Eliezer, D., Barre, P., Kobaslija, M., Chan, D., Li, X., and Heend, L. (2005) Residual structure in the repeat domain of tau: Echoes of microtubule binding and paired helical filament formation, Biochemistry 44, 1026-1036.
22. Tokimasa, M., Minoura, K., Hiraoka, S., Tomoo, K., Sumida, M., Taniguchi, T., and Ishida, T. (2005) Importance of local structures of second and third repeat fragments of microtubule-binding domain for tau filament formation, FEBS Lett. 579, 3481-3486.
23. Carmel, G., Mager, E. M., Binder, L. I., and Kuret, J. (1996) The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology, J. Biol. Chem. 271, 32789-32795.
24. Ghoshal, N., Garcia-Sierra, F., Fu, Y., Beckett, L. A., Mufson, E. J., Kuret, J., Berry, R. W., and Binder, L. I. (2001) Tau-66: Evidence for a novel tau conformation in Alzheimer's disease, J. Neurochem. 77, 1372-1385.
25. Jicha, G. A., Berenfeld, B., and Davies, P. (1999) Sequence requirements for formation of conformational variants of tau similar to those found in Alzheimer's disease, J. Neurosci. Res. 55, 713-723.
26. Hyman, B. T., Van Hoesen, G. W., Wolozin, B. L., Davies, P., Kromer, L. J., and Damasio, A. R. (1988) Alz-50 antibody recognizes Alzheimer-related neuronal changes, Ann. Neurol. 23, 371-379.
27. Garcia-Sierra, F., Ghoshal, N., Quinn, B., Berry, R. W., and Binder, L. I. (2003) Conformational changes and truncation of tau protein during tangle evolution in Alzheimer's disease, J. Alzheimer's Dis. 5, 65-77.
28. Gamblin, T. C., Berry, R. W., and Binder, L. I. (2003) Tau polymerization: Role of the amino terminus, Biochemistry 42, 2252-2257.
29. Gamblin, T. C., Berry, R. W., and Binder, L. I. (2003) Modeling tau polymerization in vitro: A review and synthesis, Biochemistry 42, 15009-15017.
30. Abraha, A., Ghoshal, N., Gamblin, T. C., Cryns, V., Berry, R. W., Kuret, J., and Binder, L. I. (2000) C-Terminal inhibition of tau assembly in vitro and in Alzheimer's disease, J. Cell Sci. 113, 3737-3745.
31. King, M. E., Ahuja, V., Binder, L. I., and Kuret, J. (1999) Ligand-dependent tau filament formation: Implications for Alzheimer's disease progression, Biochemistry 38, 14851-14859.
32. 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., and Binder, L. I. (2004) Early N-terminal changes and caspase-6 cleavage of tau in Alzheimer's disease, J. Neurosci. 24, 7895-7902.
33. King, M. E., Gamblin, T. C., Kuret, J., and Binder, L. I. (2000) Differential assembly of human tau isoforms in the presence of arachidonic acid, J. Neurochem. 74, 1749-1757.
34. Gamblin, T. C., Chen, F., Zambrano, A., Abraha, A., Lagalwar, S., Guillozet, A. L., Lu, M., Fu, Y., Garcia-Sierra, F., LaPointe, N., Miller, R., Berry, R. W., Binder, L. I., and Cryns, V. L. (2003) Caspase cleavage of tau: Linking amyloid and neurofibrillary tangles in Alzheimer's disease, Proc. Natl. Acad. Sci. U.S.A. 100, 10032-10037.
35. Reynolds, M. R., Berry, R. W., and Binder, L. I. (2005) Site-specific nitration and oxidative dityrosine bridging of the tau protein by peroxynitrite: Implications for Alzheimer's disease, Biochemistry 44, 1690-1700.
36. Gamblin, T. C., King, M. E., Dawson, H., Vitek, M. P., Kuret, J., Berry, R. W., and Binder, L. I. (2000) In vitro polymerization of tau protein monitored by laser light scattering: Method and application to the study of FTDP-17 mutants, Biochemistry 39, 6136-6144.
37. Brito, R. M., and Vaz, W. L. (1986) Determination of the critical micelle concentration of surfactants using the fluorescent probe N-phenyl-1- naphthylamine, Anal. Biochem. 152, 250-255.
38. Chirita, C. N., Necula, M., and Kuret, J. (2003) Anionic micelles and vesicles induce tau fibrillization in vitro, J. Biol. Chem. 278, 25644-25650.
39. Novak, M., Kabat, J., and 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.
40. Chirita, C. N., and Kuret, J. (2004) Evidence for an intermediate in tau filament formation, Biochemistry 43, 1704-1714.
41. Chirita, C., Necula, M., and Kuret, J. (2004) Ligand-dependent inhibition and reversal of tau filament formation, Biochemistry 43, 2879-2887.
42. Chirita, C. N., Congdon, E. E., Yin, H., and Kuret, J. (2005) Triggers of full-length tau aggregation: A role for partially folded intermediates, Biochemistry 44, 5862-5872.
43. Timasheff, S. N. (1981) The Self-Assembly of Long Rodlike Structures, in Protein/Protein Interactions (Frieden, C., and Nichol, L. W., Eds.) pp 315-336, John Wiley & Sons, New York.
44. Reynolds, M. R., Berry, R. W., and Binder, L. I. (2005) Site-specific nitration differentially influences tau assembly in vitro, Biochemistry 44, 13997-14009.
45. 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.
46. Otvos, L., Jr., Feiner, L., Lang, E., Szendrei, G. I., Goedert, M., and Lee, V. M. (1994) Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404, J. Neurosci. Res. 39, 669-673.
47. Wischik, C. M., Novak, M., Thogersen, H. C., Edwards, P. C., Runswick, M. J., Jakes, R., Walker, J. E., Milstein, C., Roth, M., and Klug, A. (1988) Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease, Proc. Natl. Acad. Sci. U.S.A. 85, 4506-4510.
48. 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. U.S.A. 85, 4884-4888.
49. Novak, M., Jakes, R., Edwards, P. C., Milstein, C., and Wischik, C. M. (1991) 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. U.S.A. 88, 5837-5841.
50. Wei, M. L., and Andreadis, A. (1998) Splicing of a regulated exon reveals additional complexity in the axonal microtubule-associated protein tau, J. Neurochem. 70, 1346-1356.
51. Wei, M. L., Memmott, J., Screaton, G., and Andreadis, A. (2000) The splicing determinants of a regulated exon in the axonal MAP tau reside within the exon and in its upstream intron, Brain Res. Mol. Brain Res. 80, 207-218.
52. Luo, M. H., Tse, S. W., Memmott, J., and Andreadis, A. (2004) Novel isoforms of tau that lack the microtubule-binding domain, J. Neurochem. 90, 340-351.