Structural impact of heparin binding to full-length Tau as studied by NMR spectroscopy

Biochemistry

Volumn 45, Issue 41, 2006, Pages 12560-12572

  Sibille, Nathalie ^a   Sillen, Alain ^a   Leroy, Arnaud ^a,b   Wieruszeski, Jean Michel ^a   Mulloy, Barbara ^c   Landrieu, Isabelle ^a   Lippens, Guy ^a  

^a UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLOMERATION; BINDING ENERGY; DISEASE CONTROL; ENZYME INHIBITION; NEGATIVE IONS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

ALZHEIMER'S DISEASE (AD); HYPERPHOSPHORYLATION; MICROTUBULE BINDING REPEATS (MTBR); PAIRED HELICAL FILAMENTS (PHF);

POLYSACCHARIDES;

HEPARIN; HEPARIN BINDING PROTEIN; TAU PROTEIN;

ALPHA HELIX; ALZHEIMER DISEASE; ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; IN VITRO STUDY; MICROTUBULE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CATTLE; HEPARIN; HUMANS; MICROSCOPY, ELECTRON; MICROTUBULES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; RECOMBINANT PROTEINS; TAU PROTEINS;

EID: 33750045702     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060964o     Document Type: Article

References (62)

1. Buee, L., Bussiere, T., Buee-Scherrer, V., Delacourte, A., and Hof, P. R. (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders, Brain Res. Brain Res. Rev. 33, 95-130.
2. Delacourte, A., and Defossez, A. (1986) Alzheimer's disease: Tau proteins, the promoting factors of microtubule assembly, are major components of paired helical filaments, J. Neurol. Sci. 76, 173-186.
3. Grundke-Iqbal, I., Iqbal, K., Quinlan, M., Tung, Y. C., Zaidi, M. S., and Wisniewski, H. M. (1986) Microtubule-associated protein tau. A component of Alzheimer paired helical filaments, J. Biol. Chem. 261, 6084-6089.
4. Bennett, D. A., Schneider, J. A., Wilson, R. S., Bienias, J. L., and Arnold, S. E. (2004) Neurofibrillary tangles mediate the association of amyloid load with clinical Alzheimer disease and level of cognitive function, Arch. Neurol. 61, 378-384.
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. 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 beta-structure, J. Biol. Chem. 269, 24290-24297.
7. 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.
8. 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.
9. Mukrasch, M. D., Biernat, J., von Bergen, M., Griesinger, C., Mandelkow, E., and Zweckstetter, M. (2005) Sites of tau important for aggregation populate {beta}-structure and bind to microtubules and polyanions, J. Biol. Chem. 280, 24978-24986.
10. Lippens, G., Wieruszeski, J. M., Leroy, A., Smet, C, Sillen, A., Buee, L., and Landrieu, I. (2004) Proline-directed random-coil chemical shift values as a tool for the NMR assignment of the tau phosphorylation sites, ChemBioChem 5, 73-78.
11. Lippens, G., Sillen, A., Smet, C., Wieruszeski, J. M., Leroy, A., Buee, L., and Landrieu, I. (2006) Studying the natively unfolded neuronal Tau protein by solution NMR spectroscopy, Protein Pept. Lett. 13, 235-246.
12. Biernat, J., Gustke, N., Drewes, G., Mandelkow, E. M., and Mandelkow, E. (1993) Phosphorylation of Ser262 strongly reduces binding of tau to microtubules: distinction between PHF-like immunoreactivity and microtubule binding, Neuron 11, 153-163.
13. Hasegawa, M., Morishima-Kawashima, M., Takio, K., Suzuki, M., Titani, K., and Ihara, Y. (1992) Protein sequence and mass spectrometric analyses of tau in the Alzheimer's disease brain, J. Biol. Chem. 267, 17047-17054.
14. Goedert, M., Jakes, R., Spillantini, M. G., Hasegawa, M., Smith, M. J., and Crowther, R. A. (1996) Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans, Nature 383, 550-553.
15. Hasegawa, M., Crowther, R. A., Jakes, R., and Goedert, M. (1997) Alzheimer-like changes in microtubule-associated protein Tau induced by sulfated glycosaminoglycans. Inhibition of microtubule binding, stimulation of phosphorylation, and filament assembly depend on the degree of sulfation, J. Biol. Chem. 272, 33118-33124.
16. Kampers, T., Friedhoff, P., Biernat, J., Mandelkow, E. M., and Mandelkow, E. (1996) RNA stimulates aggregation of microtubule-associated protein tau into Alzheimer-like paired helical filaments, FEBS Lett. 399, 344-349.
17. Wilson, D. M., and Binder, L. I. (1997) Free fatty acids stimulate the polymerization of tau and amyloid beta peptides. In vitro evidence for a common effector of pathogenesis in Alzheimer's disease, Am. J. Pathol. 150, 2181-2195.
18. von Bergen, M., Friedhoff, P., Biernat, J., Heberle, J., Mandelkow, E. M., and Mandelkow, E. (2000) Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif ((306)VQIVYK(311)) forming beta structure, Proc. Natl. Acad. Sci. U.S.A. 97, 5129-5134.
19. Capila, I., and Linhardt, R. J. (2002) Heparin-protein interactions, Angew. Chem., Int. Ed. Engl. 41, 391-412.
20. Sachchidanand, Lequin, O., Staunton, D., Mulloy, B., Forster, M. J., Yoshida, K., and Campbell, I. D. (2002) Mapping the heparin-binding site on the 13-14F3 fragment of fibronectin, J. Biol. Chem. 277, 50629-50635.
21. Mulloy, B., Forster, M. J., Jones, C., and Davies, D. B. (1993) N.m.r. and molecular-modelling studies of the solution conformation of heparin, Biochem. J. 293 (Part 3), 849-858.
22. Ruckert, M., and Otting, G. (2000) Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments, J. Am. Chem. Soc. 122, 7793-7797.
23. Mach, H., Middaugh, C. R., and Lewis, R. V. (1992) Statistical determination of the average values of the extinction coefficients of tryptophan and tyrosine in native proteins, Anal. Biochem 200, 74-80.
24. Palmer, A. G., Cavanagh, J., Wright, P. E., and Ranee, M. (1991) Sensitivity improvement in proton-detected 2-dimensional heteronuclear correlation NMR-spectroscopy, J. Magn. Reson. 93, 151-170.
25. Grzesiek, S., and Bax, A. (1993) Amino acid type determination in the sequential assignment procedure of uniformly 13C/15N-enriched proteins, J. Biomol. NMR 3, 185-204.
26. Grzesiek, S., and Bax, A. (1992) Improved 3d triple-resonance NMR techniques applied to a 31-kda protein, J. Magn. Reson. 96, 432-440.
27. Vuister, G. W., and Bax, A. (1993) Quantitative J correlation-A new approach for measuring homonuclear 3-bond J(H(N)H(alpha) coupling-constants in N-15-enriched proteins, J. Am. Chem. Soc. 115, 7772-7777.
28. 2O in protein NMR-Application to sensitivity enhancement and NOE measurements, J. Am. Chem. Soc. 115, 12593-12594.
29. Cordier, F., Dingley, A. J., and Grzesiek, S. (1999) A doublet-separated sensitivity-enhanced HSQC for the determination of scalar and dipolar one-bond J-couplings, J. Biomol. NMR 13, 175-180.
30. Wishart, D. S., and Sykes, B. D. (1994) The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data, J. Biomol. NMR 4, 171-180.
31. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1992) The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy, Biochemistry 31, 1647-1651.
32. Schwarzinger, S., Kroon, G. J., Foss, T. R., Chung, J., Wright, P. E., and Dyson, H. J. (2001) Sequence-dependent correction of random coil NMR chemical shifts, J. Am. Chem. Soc. 123, 2970-2978.
33. Kay, L. E., Torchia, D. A., and Bax, A. (1989) Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease, Biochemistry 28, 8972-8979.
34. Baleja, J. D., Mau, T., and Wagner, G. (1994) Recognition of DNA by GAL4 in solution: use of a monomeric protein-DNA complex for study by NMR, Biochemistry 33, 3071-3078.
35. Mulloy, B., Gray, E., and Barrowcliffe, T. W. (2000) Characterization of unfractionated heparin: comparison of materials from the last 50 years, Thromb. Haemostasis 84, 1052-1056.
36. Sillen, A., Leroy, A., Wieruszeski, J. M., Loyens, A., Beauvillain, J. C., Buee, L., Landrieu, I., and Lippens, G. (2005) Regions of tau implicated in the paired helical fragment core as defined by NMR, ChemBioChem 6, 1849-1856.
37. Friedhoff, P., Schneider, A., Mandelkow, E. M., and Mandelkow, E. (1998) Rapid assembly of Alzheimer-like paired helical filaments from microtubule-associated protein tau monitored by fluorescence in solution, Biochemistry 37, 10223-10230.
38. Suk, J. Y., Zhang, F., Balch, W. E., Linhardt, R. J., and Kelly, J. W. (2006) Heparin accelerates gelsolin amyloidogenesis, Biochemistry 45, 2234-2242.
39. Lopez De La Paz, M., Goldie, K., Zurdo, J., Lacroix, E., Dobson, C. M., Hoenger, A., and Serrano, L. (2002) De novo designed peptide-based amyloid fibrils, Proc. Natl. Acad. Sci. U.S.A. 99, 16052-16057.
40. Inouye, H., Sharma, D., Goux, W. J., and Kirschner, D. A. (2006) Structure of core domain of fibril-forming PHF/Tau fragments, Biophys. J. 90, 1774-1789.
41. Mulloy, B., Crane, D. T., Drake, A. F., and Davies, D. B. (1996) The interaction between heparin and polylysine: a circular dichroism and molecular modelling study, Braz. J. Med. Biol. Res. 29, 721-729.
42. Tjandra, N., and Bax, A. (1997) Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium, Science 278, 1111-1114.
43. Shortle, D., and Ackerman, M. S. (2001) Persistence of native-like topology in a denatured protein in 8 M urea, Science 293, 487-489.
44. Louhivuori, M., Paakkonen, K., Fredriksson, K., Permi, P., Lounila, J., and Annila, A. (2003) On the origin of residual dipolar couplings from denatured proteins, J. Am. Chem. Soc. 125, 15647-15650.
45. Barghorn, S., Zheng-Fischhofer, Q., Ackmann, M., Biernat, J., von Bergen, M., Mandelkow, E. M., and Mandelkow, E. (2000) Structure, microtubule interactions, and paired helical filament aggregation by tau mutants of frontotemporal dementias, Biochemistry 39, 11714-11721.
46. Alonso, A., Mederlyova, A., Novak, M., Grundke-Iqbal, I., and Iqbal, K. (2004) Promotion of hyperphosphorylation by Frontotemporal dementia Tau mutations, J. Biol. Chem. 279, 34873-34881.
47. Barghorn, S., Davies, P., and Mandelkow, E. (2004) Tau paired helical filaments from Alzheimer's disease brain and assembled in vitro are based on beta-structure in the core domain, Biochemistry 43, 1694-1703.
48. 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-beta structure, Proc. Natl. Acad. Sci. U.S.A. 100, 9034-9038.
49. Landrieu, I., Lacosse, L., Leroy, A., Wieruszeski, J. M., Trivelli, X., Sillen, A., Sibille, N., Schwalbe, H., Saxena, K., Langer, T., and Lippens, G. (2006) NMR analysis of a Tau phosphorylation pattern, J. Am. Chem. Soc. 128, 3575-3583.
50. Perez, M., Valpuesta, J. M., Medina, M., Montejo de Garcini, E., and Avila, J. (1996) Polymerization of tau into filaments in the presence of heparin: the minimal sequence required for tau-tau interaction, J. Neurochem. 67, 1183-1190.
51. Perry, G., Siedlak, S. L., Richey, P., Kawai, M., Cras, P., Kalaria, R. N., Galloway, P. G., Scardina, J. M., Cordell, B., Greenberg, B. D., et al. (1991) Association of heparan sulfate proteoglycan with the neurofibrillary tangles of Alzheimer's disease, J. Neurosci. 11, 3679-3683.
52. Mulloy, B., Gee, C., Wheeler, S. F., Wait, R., Gray, E., and Barrowcliffe, T. W. (1997) Molecular weight measurements of low molecular weight heparins by gel permeation chromatography, Thromb. Haemostasis 77, 668-674.
53. Arrasate, M., Perez, M., Valpuesta, J. M., and Avila, J. (1997) Role of glycosaminoglycans in determining the helicity of paired helical filaments, Am. J. Pathol 151, 1115-1122.
54. Hoffmann, R., Lee, V. M., Leight, S., Varga, I., and Otvos, L., Jr. (1997) Unique Alzheimer's disease paired helical filament specific epitopes involve double phosphorylation at specific sites, Biochemistry 36, 8114-8124.
55. Ruben, G. C., Ciardelli, T. L., Grundke-Iqbal, I., and Iqbal, K. (1997) Alzheimer disease hyperphosphorylated tau aggregates hydrophobically, Synapse 27, 208-229.
56. Kunjithapatham, R., Oliva, F. Y., Doshi, U., Perez, M., Avila, J., and Munoz, V. (2005) Role for the alpha-helix in aberrant protein aggregation, Biochemistry 44, 149-156.
57. Sadqi, M., Hernandez, F., Pan, U., Perez, M., Schaeberle, M. D., Avila, J., and Munoz, V. (2002) Alpha-helix structure in Alzheimer's disease aggregates of tau-protein, Biochemistry 41, 7150-7155.
58. 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.
59. Nelson, R., Sawaya, M. R., Balbirnie M, Madsen, A. O., Riekel, C., Grothe, R., and Eisenberg, D. (2005) Structure of the cross-beta spine of amyloid-like fibrils, Nature 435, 773-778.
60. Ritter, C., Maddelein, M. L., Siemer, A. B., Luhrs, T., Ernst, M., Meier, B. H., Saupe, S. J., and Riek, R. (2005) Correlation of structural elements and infectivity of the HET-s prion, Nature 435, 844-848.
61. Tycko, R. (2004) Progress towards a molecular-level structural understanding of amyloid fibrils, Curr. Opin. Struct. Biol. 14, 96-103.
62. Goedert, M., Jakes, R., and Crowther, R. A. (1999) Effects of frontotemporal dementia FTDP-17 mutations on heparin-induced assembly of tau filaments, FEBS Lett. 450, 306-311.