TMAO promotes fibrillization and microtubule assembly activity in the C-terminal repeat region of tau

Biochemistry

Volumn 45, Issue 11, 2006, Pages 3684-3691

  Scaramozzino, Francesca ^a   Peterson, Dylan W ^a   Farmer, Patrick ^a   Gerig, J T ^a   Graves, Donald J ^a   Lew, John ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATES; AMINES; BIOCHEMISTRY; OXIDES; PATHOLOGY; PROTEINS;

DIRECT PATHOLOGIC; MICROTUBULE BINDING; NEUROFIBRILLARY TANGLES (NFT); PHYSICAL CHARACTERIZATION;

DISEASES;

ALANINE; TAU PROTEIN; TRIMETHYLAMINE OXIDE; TYROSINE;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CORRELATION ANALYSIS; MICROTUBULE ASSEMBLY; NEUROFIBRILLARY TANGLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID SUBSTITUTION; ENZYME ACTIVATION; HUMANS; METHYLAMINES; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULES; MODELS, BIOLOGICAL; MUTATION; NEUROFIBRILS; OXIDANTS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP; TAU PROTEINS; TIME FACTORS; TYROSINE;

EID: 33645241089     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052167g     Document Type: Article

References (53)

1. Lee, V. M., Goedert, M., and Trojanowski, J. Q. (2001) Neurodegenerative tauopathies, Annu. Rev. Neurosci. 24, 1121-1159.
2. Avila, J., Lucas, J. J., Perez, M., and Hernandez, F. (2004) Role of tau protein in both physiological and pathological conditions, Physiol. Rev. 84, 361-384.
3. 311) forming β structure, Proc. Natl. Acad. Sci. U.S.A. 97, 5129-5134.
4. 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.
5. 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.
6. Woody, R. W., Clark, D. C., Roberts, G. C., Martin, S. R., and Bayley, P. M. (1983) Molecular flexibility in microtubule proteins: Proton nuclear magnetic resonance characterization, Biochemistry 22, 2186-2192.
7. Wille, H., Drewes, G., Biernat, J., Mandelkow, E. M., and Mandelkow, E. (1992) Alzheimer-like paired helical filaments and antiparallel dimers formed from microtubule-associated protein tau in vitro, J. Cell Biol. 118, 573-584.
8. 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.
9. 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.
10. 1H NMR spectroscopy, Biochem. Biophys. Res. Commun. 294, 210-214.
11. 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.
12. Yanagawa, H., Chung, S. H., Ogawa, Y., Sato, K., Shibata-Seki, T., Masai, J., and Ishiguro, K. (1998) Protein anatomy: C-Tail region of human tau protein as a crucial structural element in Alzheimer's paired helical filament formation in vitro, Biochemistry 37, 1979-1988.
13. 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.
14. Gamblin, T. C., Berry, R. W., and Binder, L. I. (2003) Modeling Tau Polymerization in Vitro: A Review and Synthesis, Biochemistry 42, 15009-15017.
15. 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.
16. Kirschner, D. A., Abraham, C., and Selkoe, D. J. (1986) X-ray diffraction from intraneuronal paired helical filaments and extra-neuronal amyloid fibers in Alzheimer disease indicates cross-β conformation, Proc. Natl. Acad. Sci. U.S.A. 83, 503-507.
17. Giannetti, A. M., Lindwall, G., Chau, M. F., Radeke, M. J., Feinstein, S. C., and Kohlstaedt, L. A. (2000) Fibers of tau fragments, but not full length tau, exhibit a cross β-structure: Implications for the formation of paired helical filaments, Protein Sci. 9, 2427-2435.
18. 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.
19. 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.
20. Goux, W. J. (2002) The conformations of filamentous and soluble tau associated with Alzheimer paired helical filaments, Biochemistry 41, 13798-13806.
21. Sadqi, M., Hernandez, F., Pan, U., Perez, M., Schaeberle, M. D., Avila, J., and Munoz, V. (2002) α-Helix structure in Alzheimer's disease aggregates of tau-protein, Biochemistry 41, 7150-7155.
22. Kuret, J., Chirita, C. N., Congdon, E. E., Kannanayakal, T., Li, G. B., Necula, M., Yin, H. S., and Zhong, Q. (2005) Pathways of tau fibrillization, Biochim. Biophys. Acta 1739, 167-178.
23. Chirita, C. N., and Kuret, J. (2004) Evidence for an intermediate in tau filament formation, Biochemistry 43, 1704-1714.
24. Anfinsen, C. B. (1973) Principles that govern the folding of protein chains, Science 181, 223-230.
25. Yancey, P. H., Clark, M. E., Hand, S. C., Bowlus, R. D., and Somero, G. N. (1982) Living with water stress: Evolution of osmolyte systems, Science 217, 1214-1222.
26. Bolen, D. W., and Baskakov, I. V. (2001) The osmophobic effect: Natural selection of a thermodynamic force in protein folding, J. Mol. Biol. 310, 955-963.
27. Wang, A., and Bolen, D. W. (1996) Effect of proline on lactate dehydrogenase activity: Testing the generality and scope of the compatibility paradigm, Biophys. J. 71, 2117-2122.
28. Hochachka, P. W., and Somero, G. N. (1968) The adaptation of enzymes to temperature, Comp. Biochem. Physiol. 27, 659-668.
29. Yancey, P. H., Rhea, M. D., Kemp, K. M., and Bailey, D. M. (2004) Trimethylamine oxide, betaine and other osmolytes in deep-sea animals: Depth trends and effects on enzymes under hydrostatic pressure, Cell. Mol. Biol. (Paris, Fr., Print) 50, 371-376.
30. Bell, J. D., Lee, J. A., Lee, H. A., Sadler, P. J., Wilkie, D. R., and Woodham, R. H. (1991) Nuclear magnetic resonance studies of blood plasma and urine from subjects with chronic renal failure: Identification of trimethylamine-N-oxide, Biochim. Biophys. Acta 1096, 101-107.
31. Kumar, R., Lee, J. C., Bolen, D. W., and Thompson, E. B. (2001) The conformation of the glucocorticoid receptor af1/tau1 domain induced by osmolyte binds co-regulatory proteins, J. Biol. Chem. 276, 18146-18152.
32. Tatzelt, J., Prusiner, S. B., and Welch, W. J. (1996) Chemical chaperones interfere with the formation of scrapie prion protein, EMBO J. 15, 6363-6373.
33. Tamarappoo, B. K., and Verkman, A. S. (1998) Defective aquaporin-2 trafficking in nephrogenic diabetes insipidus and correction by chemical chaperones, J. Clin. Invest. 101, 2257-2267.
34. Brown, C. R., Hong-Brown, L. Q., Biwersi, J., Verkman, A. S., and Welch, W. J. (1996) Chemical chaperones correct the mutant phenotype of the delta F508 cystic fibrosis transmembrane conductance regulator protein, Cell Stress Chaperones 1, 117-125.
35. Baskakov, I., and Holen, D. W. (1998) Forcing thermodynamically unfolded proteins to fold, J. Biol. Chem. 273, 4831-4834.
36. Goode, B. L., Denis, P. E., Panda, D., Radeke, M. J., Miller, H. P., Wilson, L., and Feinstein, S. C. (1997) Functional interactions between the proline-rich and repeat regions of tau enhance microtubule binding and assembly, Mol. Biol. Cell 8, 353-365.
37. Tseng, H. C., Lu, Q., Henderson, E., and Graves, D. J. (1999) Phosphorylated tau can promote tubulin assembly, Proc. Natl. Acad. Sci. U.S.A. 96, 9503-9508.
38. Fulton, D. B., and Ni, F. (1997) ROESY with water nip back for high-field NMR of biomolecules, J. Magn. Reson. 129, 93-97.
39. Dalvit, C. (1998) Efficient multiple-solvent suppression for the study of the interactions of organic solvents with biomolecules, J. Biomol. NMR 11, 437-444.
40. Greenfield, N., and Fasman, G. D. (1969) Computed circular dichroism spectra for the evaluation of protein conformation, Biochemistry 8, 4108-4116.
41. Lendel, C., Dincbas-Renqvist, V., Flores, A., Wahlberg, E., Dogan, J., Nygren, P. A., and Hard, T. (2004) Biophysical characterization of Z(SPA-1): A phage-display selected binder to protein A, Protein Sci. 13, 2078-2088.
42. Tseng, H.-C., and Graves, D. J. (1998) Natural methylamine osmolytes, trimethylamine N-oxide and betaine, increase tau-induced polymerization of microtubules, Biochem. Biophys. Res. Commun. 250, 726-730.
43. Smith, M. J., Crowther, R. A., and Goedert, M. (2000) The natural osmolyte trimethylamine N-oxide (TMAO) restores the ability of mutant tau to promote microtubule assembly, FEBS Lett. 484, 265-270.
44. Eidenmuller, J., Fath, T., Hellwig, A., Reed, J., Sontag, E., and Brandt, R. (2000) Structural and functional implications of tau hyperphosphorylation: Information from phosphorylation-mimicking mutated tau proteins, Biochemistry 39, 13166-13175.
45. Goux, W. J., Kopplin, L., Nguyen, A. D., Leak, K., Rutkofsky, M., Shanmuganandam, V. D., Sharma, D., Inouye, H., and Kirschner, D. A. (2004) The formation of straight and twisted filaments from short tau peptides, J. Biol. Chem. 279, 26868-26875.
46. LeVine, H., III (1999) Quantification of β-sheet amyloid fibril structures with thioflavin T, Methods Enzymol. 309, 274-284.
47. Wisniewski, H. M., Merz, P. A., and Iqbal, K. (1984) Ultrastructure of paired helical filaments of Alzheimer's neurofibrillary tangle, J. Neuropathol. Exp. Neurol. 43, 643-656.
48. Chiti, F., Taddei, N., Baroni, F., Capanni, C., Stefani, M., Ramponi, G., and Dobson, C. M. (2002) Kinetic partitioning of protein folding and aggregation, Nat. Struct. Biol. 9, 137-143.
49. Kyte, J. (1995) Structure in Protein Chemistry, Garland Publishing, Inc., New York.
50. Uversky, V. N., Li, J., and Fink, A. L. (2001) Trimethylamine-N-oxide- induced folding of α-synuclein, FEBS Lett. 509, 31-35.
51. Yang, D. S., Yip, C. M., Huang, T. H., Chakrabartty, A., and Fraser, P. E. (1999) Manipulating the amyloid-β aggregation pathway with chemical chaperones, J. Biol. Chem. 274, 32970-32974.
52. Street, A. G., and Mayo, S. L. (1999) Intrinsic β-sheet propensities result from van der Waals interactions between side chains and the local backbone, Proc. Natl. Acad. Sci. U.S.A. 96, 9074-9076.
53. Chiti, F., Stefani, M., Taddei, N., Ramponi, G., and Dobson, C. M. (2003) Rationalization of the effects of mutations on peptide and protein aggregation rates, Nature 424, 805-808.