Cross-seeding and conformational selection between three- and four-repeat human Tau proteins

Journal of Biological Chemistry

Volumn 287, Issue 18, 2012, Pages 14950-14959

  Yu, Xiang ^a   Luo, Yin ^a,b   Dinkel, Paul ^c   Zheng, Jie ^a   Wei, Guanghong ^b   Margittai, Martin ^c   Nussinov, Ruth ^d,e   Ma, Buyong ^d  

^a The University of Akron   (United States)

^b FUDAN UNIVERSITY   (China)

^c UNIVERSITY OF DENVER   (United States)

^d SAIC FREDERICK INC   (United States)

^e TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER'S DISEASE; ASYMMETRIC BARRIERS; CONFORMATIONAL SELECTION; CRITICAL STEPS; DIFFERENT STRUCTURE; ENERGY LANDSCAPE; FIBRIL FORMATION; FIBRIL GROWTH; FIBRILLIZATION; FRONTOTEMPORAL DEMENTIAS; HETEROGENEOUS STRUCTURES; L-SHAPED; MICROTUBULE ASSOCIATED PROTEIN; OCTAMERS; PAIRED HELICAL FILAMENTS; PROTEIN AGGREGATION; STRUCTURAL CORE; STRUCTURAL SIMILARITY; TAU PROTEINS; U-SHAPED;

BIOCHEMISTRY; BIOLOGY;

PROTEINS;

TAU PROTEIN;

ARTICLE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURAL HOMOLOGY;

MODELS, MOLECULAR; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; TAU PROTEINS;

EID: 84860380323     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.340794     Document Type: Article

References (42)

1. Hardy, J., and Allsop, D. (1991) Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol. Sci. 12, 383-388
2. Hardy, J. A., and Higgins, G. A. (1992) Alzheimer's disease. The amyloid cascade hypothesis. Science 256, 184-185
3. Drubin, D. G., and Kirschner, M. W. (1986) Tau protein function in living cells. J. Cell Biol. 103, 2739-2746
4. Dinkel, P. D., Siddiqua, A., Huynh, H., Shah, M., and Margittai, M. (2011) Variations in filament conformation dictate seeding barrier between three- and four-repeat Tau. Biochemistry 50, 4330-4336
5. Goedert, M., Spillantini, M. G., Jakes, R., Rutherford, D., and Crowther, R. A. (1989) Multiple isoforms of human microtubule-associated protein Tau. Sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3, 519-526
6. Goedert, M., Spillantini, M. G., Cairns, N. J., and Crowther, R. A. (1992) Tau proteins of Alzheimer paired helical filaments. Abnormal phosphorylation of all six brain isoforms. Neuron 8, 159-168
7. Schweers, O., Schönbrunn-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
8. Cleveland, D. W., Hwo, S. Y., and Kirschner, M. W. (1977) Physical and chemical properties of purified Tau factor and the role of Tau in microtubule assembly. J. Mol. Biol. 116, 227-247
9. Berriman, J., Serpell, L. C., Oberg, K. A., Fink, A. L., Goedert, M., and Crowther, R. A. (2003) Tau filaments from human brain and from in vitro assembly of recombinant protein show cross-β structure. Proc. Natl. Acad. Sci. U.S.A. 100, 9034-9038
10. von Bergen, M., Barghorn, S., Li, L., Marx, A., Biernat, J., Mandelkow, E. M., and Mandelkow, E. (2001) Mutations of Tau protein in frontotemporal dementia promote aggregation of paired helical filaments by enhancing local β-structure. J. Biol. Chem. 276, 48165-48174
11. Congdon, E. E., Kim, S., Bonchak, J., Songrug, T., Matzavinos, A., and Kuret, J. (2008) Nucleation-dependent Tau filament formation. The importance of dimerization and an estimation of elementary rate constants. J. Biol. Chem. 283, 13806-13816
12. Xu, S. H., Brunden, K. R., Trojanowski, J. Q., and Lee, V. M., (2010) Characterization of Tau fibrillization in vitro. Alzheimers Dement. 6, 110-117
13. Wischik, C. M., Novak, M., Thøgersen, 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
14. von Bergen, M., Barghorn, S., Müller, S. A., Pickhardt, M., Biernat, J., Mandelkow, E. M., Davies, P., Aebi, U., and Mandelkow, E. (2006) The core of Tau-paired helical filaments studied by scanning transmission electron microscopy and limited proteolysis. Biochemistry 45, 6446-6457
15. Wegmann, S., Jung, Y. J., Chinnathambi, S., Mandelkow, E. M., Mandelkow, E., and Muller, D. J. (2010) Human Tau isoforms assemble into ribbon-like fibrils that display polymorphic structure and stability. J. Biol. Chem. 285, 27302-27313
16. Li, L., von Bergen, M., Mandelkow, E. M., and Mandelkow, E. (2002) Structure, stability, and aggregation of paired helical filaments from Tau protein and FTDP-17 mutants probed by tryptophan scanning mutagenesis. J. Biol. Chem. 277, 41390-41400
17. Mukrasch, M. D., von Bergen, M., Biernat, J., Fischer, D., Griesinger, C., Mandelkow, E., and Zweckstetter, M. (2007) The "jaws" of the Tau-micro- tubule interaction. J. Biol. Chem. 282, 12230-12239
18. Margittai, M., and Langen, R. (2004) Template-assisted filament growth by parallel stacking of Tau. Proc. Natl. Acad. Sci. U.S.A. 101, 10278-10283
19. Mukrasch, M. D., Biernat, J., von Bergen, M., Griesinger, C., Mandelkow, E., and Zweckstetter, M. (2005) Sites of Tau important for aggregation populate β-structure and bind to microtubules and polyanions. J. Biol. Chem. 280, 24978-24986
20. Siddiqua, A., and Margittai, M. (2010) Three- and four-repeat Tau coassemble into heterogeneous filaments. An implication for Alzheimer disease. J. Biol. Chem. 285, 37920-37926
21. Csermely, P., Palotai, R., and Nussinov, R. (2010) Induced fit, conformational selection and independent dynamic segments. An extended view of binding events. Trends Biochem. Sci. 35, 539-546
22. Ma, B., Kumar, S., Tsai, C. J., and Nussinov, R. (1999) Folding funnels and binding mechanisms. Protein Eng. 12, 713-720
23. Ma, B., and Nussinov, R. (2010) Enzyme dynamics point to stepwise conformational selection in catalysis. Curr. Opin. Chem. Biol. 14, 652-659
24. Ma, B., and Nussinov, R. (2012) Selective molecular recognition in amyloid growth and transmission and cross-species barriers. J. Mol. Biol., in press
25. Frost, B., and Diamond, M. I. (2010) Prion-like mechanisms in neurodegenerative diseases. Nat. Rev. Neurosci. 11, 155-159
26. Frost, B., Jacks, R. L., and Diamond, M. I. (2009) Propagation of Tau misfolding from the outside to the inside of a cell. J. Biol. Chem. 284, 12845-12852
27. Clavaguera, F., Bolmont, T., Crowther, R. A., Abramowski, D., Frank, S., Probst, A., Fraser, G., Stalder, A. K., Beibel, M., Staufenbiel, M., Jucker, M., Goedert, M., and Tolnay, M. (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat. Cell Biol. 11, 909-913
28. Miller, Y., Ma, B., and Nussinov, R. (2011) Synergistic interactions between repeats in Tau protein and Aβ amyloids may be responsible for accelerated aggregation via polymorphic states. Biochemistry 50, 5172-5181
29. Ma, B., and Nussinov, R. (2002) Stabilities and conformations of Alzheimer's β-amyloid peptide oligomers (Aβ 16-22, Aβ 16-35, and Aβ10-35). Sequence effects. Proc. Natl. Acad. Sci. U.S.A. 99, 14126-14131
30. Zheng, J., Ma, B., and Nussinov, R. (2006) Consensus features in amyloid fibrils. Sheet-sheet recognition via a (polar or nonpolar) zipper structure. Phys. Biol. 3, P1-4
31. Miller, Y., Ma, B., and Nussinov, R. (2010) Polymorphism in Alzheimer Aßamyloid organization reflects conformational selection in a rugged energy landscape. Chem. Rev. 110, 4820-4838
32. Ma, B., and Nussinov, R. (2011) Polymorphic triple β-sheet structures contribute to amide hydrogen/deuterium (H/D) exchange protection in the Alzheimer amyloid β42 peptide. J. Biol. Chem. 286, 34244-34253
33. Ma, B., and Nussinov, R. (2010) Polymorphic C-terminal β-sheet interactions determine the formation of fibril or amyloid beta-derived diffusible ligand-like globulomer for the Alzheimer Aβ42 dodecamer. J. Biol. Chem. 285, 37102-37110
34. Kale, L., Skeel, R., Bhandarkar, M., Brunner, R., Gursoy, A., Krawetz, N., Phillips, J., Shinozaki, A., Varadarajan, K., and Schulten, K. (1999) NAMD2: greater scalability for parallel molecular dynamics. J. Comput. Phys. 151, 283-312
35. Mackerell, A. D., Jr., Feig, M., and Brooks, C. L., 3rd (2004) Extending the treatment of backbone energetics in protein force fields. Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25, 1400-1415
36. Lee, M. S., Salsbury, F. R., and Brooks, C. L. (2002) Novel generalized Born methods. J. Chem. Phys. 116, 10606-10614
37. Zheng, J., Ma, B., Chang, Y., and Nussinov, R. (2008) Molecular dynamics simulations of Alzheimer Aβ40 elongation and lateral association. Front. Biosci. 13, 3919-3930
38. Sibille, N., Sillen, A., Leroy, A., Wieruszeski, J. M., Mulloy, B., Landrieu, I., and Lippens, G. (2006) Structural impact of heparin binding to full-length Tau as studied by NMR spectroscopy. Biochemistry 45, 12560-12572
39. Frishman, D., and Argos, P. (1995) Knowledge-based protein secondary structure assignment. Proteins 23, 566-579
40. Cerf, E., Sarroukh, R., Tamamizu-Kato, S., Breydo, L., Derclaye, S., Dufrêne, Y. F., Narayanaswami, V., Goormaghtigh, E., Ruysschaert, J. M., and Raussens, V. (2009) Antiparallel β-sheet. A signature structure of the oligomeric amyloid β-peptide. Biochem. J. 421, 415-423
41. Matsumura, S., Shinoda, K., Yamada, M., Yokojima, S., Inoue, M., Ohnishi, T., Shimada, T., Kikuchi, K., Masui, D., Hashimoto, S., Sato, M., Ito, A., Akioka, M., Takagi, S., Nakamura, Y., Nemoto, K., Hasegawa, Y., Takamoto, H., Inoue, H., Nakamura, S., Nabeshima, Y., Teplow, D. B., Kinjo, M., and Hoshi, M. (2011) Two distinct amyloid β-protein (Aβ) assembly pathways leading to oligomers and fibrils identified by combined fluorescence correlation spectroscopy, morphology, and toxicity analyses. J. Biol. Chem. 286, 11555-11562
42. Nonaka, T., Watanabe, S. T., Iwatsubo, T., and Hasegawa, M. (2010) Seeded aggregation and toxicity of α-synuclein and Tau. Cellular models of neurodegenerative diseases. J. Biol. Chem. 285, 34885-34898