Folding of the Repeat Domain of Tau Upon Binding to Lipid Surfaces

Journal of Molecular Biology

Volumn 362, Issue 2, 2006, Pages 312-326

  Barré, Patrick ^a   Eliezer, David ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Alzheimer's; microtubule associated proteins; protein aggregation; protein folding; tau

Indexed keywords

LIPID; TAU PROTEIN;

ALZHEIMER DISEASE; ARTICLE; LIPID MEMBRANE; LIPID VESICLE; MICELLE; MICROTUBULE; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; STRUCTURE ANALYSIS;

EID: 33747790300     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.07.018     Document Type: Article

References (87)

1. Cleveland D.W., Hwo S.Y., and Kirschner M.W. Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J. Mol. Biol. 116 (1977) 207-225
2. Cleveland D.W., Hwo S.Y., and Kirschner M.W. Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J. Mol. Biol. 116 (1977) 227-247
3. Panda D., Miller H.P., and Wilson L. Rapid treadmilling of brain microtubules free of microtubule-associated proteins in vitro and its suppression by tau. Proc. Natl Acad. Sci. USA 96 (1999) 12459-12464
4. Goedert M., Spillantini M.G., Jakes R., Rutherford D., and Crowther R.A. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3 (1989) 519-526
5. Andreadis A., Brown W.M., and Kosik K.S. Structure and novel exons of the human tau gene. Biochemistry 31 (1992) 10626-10633
6. Goedert M., Spillantini M.G., and Crowther R.A. Cloning of a big tau microtubule-associated protein characteristic of the peripheral nervous system. Proc. Natl Acad. Sci. USA 89 (1992) 1983-1987
7. Couchie D., Mavilia C., Georgieff I.S., Liem R.K., Shelanski M.L., and Nunez J. Primary structure of high molecular weight tau present in the peripheral nervous system. Proc. Natl Acad. Sci. USA 89 (1992) 4378-4381
8. Wei M.L., and Andreadis A. Splicing of a regulated exon reveals additional complexity in the axonal microtubule-associated protein tau. J. Neurochem. 70 (1998) 1346-1356
9. Wang Y., Loomis P.A., Zinkowski R.P., and Binder L.I. A novel tau transcript in cultured human neuroblastoma cells expressing nuclear tau. J. Cell Biol. 121 (1993) 257-267
10. Hirokawa N., Shiomura Y., and Okabe S. Tau proteins: the molecular structure and mode of binding on microtubules. J. Cell Biol. 107 (1988) 1449-1459
11. Chen J., Kanai Y., Cowan N.J., and Hirokawa N. Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 360 (1992) 674-677
12. Kanai Y., Takemura R., Oshima T., Mori H., Ihara Y., Yanagisawa M., et al. Expression of multiple tau isoforms and microtubule bundle formation in fibroblasts transfected with a single tau cDNA. J. Cell Biol. 109 (1989) 1173-1184
13. Knops J., Kosik K.S., Lee G., Pardee J.D., Cohen-Gould L., and McConlogue L. Overexpression of tau in a nonneuronal cell induces long cellular processes. J. Cell Biol. 114 (1991) 725-733
14. Caceres A., and Kosik K.S. Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343 (1990) 461-463
15. Caceres A., Potrebic S., and Kosik K.S. The effect of tau antisense oligonucleotides on neurite formation of cultured cerebellar macroneurons. J. Neurosci. 11 (1991) 1515-1523
16. Dawson H.N., Ferreira A., Eyster M.V., Ghoshal N., Binder L.I., and Vitek M.P. Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J. Cell Sci. 114 (2001) 1179-1187
17. LoPresti P., Szuchet S., Papasozomenos S.C., Zinkowski R.P., and Binder L.I. Functional implications for the microtubule-associated protein tau: localization in oligodendrocytes. Proc. Natl Acad. Sci. USA 92 (1995) 10369-10373
18. Klein C., Kramer E.M., Cardine A.M., Schraven B., Brandt R., and Trotter J. Process outgrowth of oligodendrocytes is promoted by interaction of fyn kinase with the cytoskeletal protein tau. J. Neurosci. 22 (2002) 698-707
19. Ebneth A., Godemann R., Stamer K., Illenberger S., Trinczek B., and Mandelkow E. Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J. Cell Biol. 143 (1998) 777-794
20. Trinczek B., Biernat J., Baumann K., Mandelkow E.M., and Mandelkow E. Domains of tau protein, differential phosphorylation, and dynamic instability of microtubules. Mol. Biol. Cell 6 (1995) 1887-1902
21. Brandt R., Leger J., and Lee G. Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J. Cell Biol. 131 (1995) 1327-1340
22. Lee G., Newman S.T., Gard D.L., Band H., and Panchamoorthy G. Tau interacts with src-family non-receptor tyrosine kinases. J. Cell Sci. 111 (1998) 3167-3177
23. Jenkins S.M., and Johnson G.V. Tau complexes with phospholipase C-gamma in situ. Neuroreport 9 (1998) 67-71
24. Harada A., Oguchi K., Okabe S., Kuno J., Terada S., Ohshima T., et al. Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 369 (1994) 488-491
25. Grundke-Iqbal I., Iqbal K., Quinlan M., Tung Y.C., Zaidi M.S., and Wisniewski H.M. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J. Biol. Chem. 261 (1986) 6084-6089
26. Kosik K.S., Joachim C.L., and Selkoe D.J. Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc. Natl Acad. Sci. USA 83 (1986) 4044-4048
27. Goedert M., Wischik C.M., Crowther R.A., Walker J.E., and Klug A. Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: identification as the microtubule-associated protein tau. Proc. Natl Acad. Sci. USA 85 (1988) 4051-4055
28. Wischik C.M., Novak M., Edwards P.C., Klug A., Tichelaar W., and Crowther R.A. Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc. Natl Acad. Sci. USA 85 (1988) 4884-4888
29. Kondo J., Honda T., Mori H., Hamada Y., Miura R., Ogawara M., and Ihara Y. The carboxyl third of tau is tightly bound to paired helical filaments. Neuron 1 (1988) 827-834
30. Greenberg S.G., and Davies P. A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc. Natl Acad. Sci. USA 87 (1990) 5827-5831
31. Wood J.G., Mirra S.S., Pollock N.J., and Binder L.I. Neurofibrillary tangles of Alzheimer disease share antigenic determinants with the axonal microtubule-associated protein tau (tau). Proc. Natl Acad. Sci. USA 83 (1986) 4040-4043
32. Ingram E.M., and Spillantini M.G. Tau gene mutations: dissecting the pathogenesis of FTDP-17. Trends Mol. Med. 8 (2002) 555-562
33. Garcia M.L., and Cleveland D.W. Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr. Opin. Cell Biol. 13 (2001) 41-48
34. Murayama S., Mori H., Ihara Y., and Tomonaga M. Immunocytochemical and ultrastructural studies of Pick's disease. Ann. Neurol. 27 (1990) 394-405
35. Tabaton M., Whitehouse P.J., Perry G., Davies P., Autilio-Gambetti L., and Gambetti P. Alz 50 recognizes abnormal filaments in Alzheimer's disease and progressive supranuclear palsy. Ann. Neurol. 24 (1988) 407-413
36. Feany M.B., and Dickson D.W. Widespread cytoskeletal pathology characterizes corticobasal degeneration. Am. J. Pathol. 146 (1995) 1388-1396
37. Poorkaj P., Bird T.D., Wijsman E., Nemens E., Garruto R.M., Anderson L., et al. Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann. Neurol. 43 (1998) 815-825
38. Hutton M., Lendon C.L., Rizzu P., Baker M., Froelich S., Houlden H., et al. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393 (1998) 702-705
39. Spillantini M.G., Murrell J.R., Goedert M., Farlow M.R., Klug A., and Ghetti B. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc. Natl Acad. Sci. USA 95 (1998) 7737-7741
40. Butner K.A., and Kirschner M.W. Tau protein binds to microtubules through a flexible array of distributed weak sites. J. Cell Biol. 115 (1991) 717-730
41. Gustke N., Trinczek B., Biernat J., Mandelkow E.M., and Mandelkow E. Domains of tau protein and interactions with microtubules. Biochemistry 33 (1994) 9511-9522
42. Hayashi S., Toyoshima Y., Hasegawa M., Umeda Y., Wakabayashi K., Tokiguchi S., et al. Late-onset frontotemporal dementia with a novel exon 1 (Arg5His) tau gene mutation. Ann. Neurol. 51 (2002) 525-530
43. Gamblin T.C., Berry R.W., and Binder L.I. Tau polymerization: role of the amino terminus. Biochemistry 42 (2003) 2252-2257
44. Rizzini C., Goedert M., Hodges J.R., Smith M.J., Jakes R., Hills R., et al. Tau gene mutation K257T causes a tauopathy similar to Pick's disease. J. Neuropathol. Exp. Neurol. 59 (2000) 990-1001
45. Barghorn S., Zheng-Fischhofer Q., Ackmann M., Biernat J., von Bergen M., Mandelkow E.M., and Mandelkow E. Structure, microtubule interactions, and paired helical filament aggregation by tau mutants of frontotemporal dementias. Biochemistry 39 (2000) 11714-11721
46. Goedert M., Jakes R., and Crowther R.A. Effects of frontotemporal dementia FTDP-17 mutations on heparin-induced assembly of tau filaments. FEBS Letters 450 (1999) 306-311
47. Gamblin T.C., King M.E., Dawson H., Vitek M.P., Kuret J., Berry R.W., and Binder L.I. In vitro polymerization of tau protein monitored by laser light scattering: method and application to the study of FTDP-17 mutants. Biochemistry 39 (2000) 6136-6144
48. Nacharaju P., Lewis J., Easson C., Yen S., Hackett J., Hutton M., and Yen S.H. Accelerated filament formation from tau protein with specific FTDP-17 missense mutations. FEBS Letters 447 (1999) 195-199
49. Neumann M., Schulz-Schaeffer W., Crowther R.A., Smith M.J., Spillantini M.G., Goedert M., and Kretzschmar H.A. Pick's disease associated with the novel Tau gene mutation K369I. Ann. Neurol. 50 (2001) 503-513
50. Ksiezak-Reding H., and Yen S.H. Structural stability of paired helical filaments requires microtubule-binding domains of tau: a model for self-association. Neuron 6 (1991) 717-728
51. Goedert M., Spillantini M.G., Cairns N.J., and Crowther R.A. Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8 (1992) 159-168
52. Eliezer D., Barre P., Kobaslija M., Chan D., Li X., and Heend L. Residual structure in the repeat domain of tau: echoes of microtubule binding and paired helical filament formation. Biochemistry 44 (2005) 1026-1036
53. von Bergen M., Friedhoff P., Biernat J., Heberle J., Mandelkow E.M., and Mandelkow E. 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. USA 97 (2000) 5129-5134
54. Santarella R.A., Skiniotis G., Goldie K.N., Tittmann P., Gross H., Mandelkow E.M., et al. Surface-decoration of microtubules by human tau. J. Mol. Biol. 339 (2004) 539-553
55. Caron J.M., and Berlin R.D. Interaction of microtubule proteins with phospholipid vesicles. J. Cell Biol. 81 (1979) 665-671
56. Surridge C.D., and Burns R.G. The difference in the binding of phosphatidylinositol distinguishes MAP2 from MAP2C and Tau. Biochemistry 33 (1994) 8051-8057
57. Shea T.B. Phospholipids alter tau conformation, phosphorylation, proteolysis, and association with microtubules: implication for tau function under normal and degenerative conditions. J. Neurosci. Res. 50 (1997) 114-122
58. Wilson D.M., and Binder L.I. 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 (1997) 2181-2195
59. King M.E., Ahuja V., Binder L.I., and Kuret J. Ligand-dependent tau filament formation: implications for Alzheimer's disease progression. Biochemistry 38 (1999) 14851-14859
60. Chirita C.N., Necula M., and Kuret J. Anionic micelles and vesicles induce tau fibrillization in vitro. J. Biol. Chem. 278 (2003) 25644-25650
61. Luo P., and Baldwin R.L. Mechanism of helix induction by trifluoroethanol: a framework for extrapolating the helix-forming properties of peptides from trifluoroethanol/water mixtures back to water. Biochemistry 36 (1997) 8413-8421
62. Rohl C.A., and Baldwin R.L. Comparison of NH exchange and circular dichroism as techniques for measuring the parameters of the helix-coil transition in peptides. Biochemistry 36 (1997) 8435-8442
63. Bussell Jr. R., and Eliezer D. Effects of Parkinson's disease-linked mutations on the structure of lipid-associated alpha-synuclein. Biochemistry 43 (2004) 4810-4818
64. Rhoades E., Ramlall T.F., Webb W.W., and Eliezer D. Quantification of alpha-synuclein binding to lipid vesicles using fluorescence correlation spectroscopy. Biophys. J. 90 (2006) 4692-4700
65. Spera S., and Bax A. Empirical correlation between protein backbone conformation and C-alpha and C-beta C-13 nuclear magnetic resonance chemical shifts. J. Am. Chem. Soc. 113 (1991) 5490-5492
66. Wishart D.S., Sykes B.D., and Richards F.M. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222 (1991) 311-333
67. Lee G., Neve R.L., and Kosik K.S. The microtubule binding domain of tau protein. Neuron 2 (1989) 1615-1624
68. 13C chemical-shift data. J. Biomol. NMR 4 (1994) 171-180
69. Bussell Jr. R., Ramlall T.F., and Eliezer D. Helix periodicity, topology, and dynamics of membrane-associated alpha-synuclein. Protein Sci. 14 (2005) 862-872
70. Mukrasch M.D., Biernat J., von Bergen M., Griesinger C., Mandelkow E., and Zweckstetter M. Sites of tau important for aggregation populate {beta}-structure and bind to microtubules and polyanions. J. Biol. Chem. 280 (2005) 24978-24986
71. Arbuzova A., Murray D., and McLaughlin S. MARCKS, membranes, and calmodulin: kinetics of their interaction. Biochim. Biophys. Acta 1376 (1998) 369-379
72. Murray D., Hermida-Matsumoto L., Buser C.A., Tsang J., Sigal C.T., Ben-Tal N., et al. Electrostatics and the membrane association of Src: theory and experiment. Biochemistry 37 (1998) 2145-2159
73. Krueger-Koplin R.D., Sorgen P.L., Krueger-Koplin S.T., Rivera-Torres I.O., Cahill S.M., Hicks D.B., et al. An evaluation of detergents for NMR structural studies of membrane proteins. J. Biomol. NMR 28 (2004) 43-57
74. Littauer U.Z., Giveon D., Thierauf M., Ginzburg I., and Ponstingl H. Common and distinct tubulin binding sites for microtubule-associated proteins. Proc. Natl Acad. Sci. USA 83 (1986) 7162-7166
75. Chau M.F., Radeke M.J., de Ines C., Barasoain I., Kohlstaedt L.A., and Feinstein S.C. The microtubule-associated protein tau cross-links to two distinct sites on each alpha and beta tubulin monomer via separate domains. Biochemistry 37 (1998) 17692-17703
76. Eliezer D. Characterizing residual structure in disordered protein states using NMR. Methods Mol. Biol. 350 (2006) 49-67
77. Mohana-Borges R., Goto N.K., Kroon G.J., Dyson H.J., and Wright P.E. Structural characterization of unfolded states of apomyoglobin using residual dipolar couplings. J. Mol. Biol. 340 (2004) 1131-1142
78. Minoura K., Tomoo K., Ishida T., Hasegawa H., Sasaki M., and Taniguchi T. Amphipathic helical behavior of the third repeat fragment in the tau microtubule-binding domain, studied by (1)H NMR spectroscopy. Biochem. Biophys. Res. Commun. 294 (2002) 210-214
79. Minoura K., Yao T.M., Tomoo K., Sumida M., Sasaki M., Taniguchi T., and Ishida T. Different associational and conformational behaviors between the second and third repeat fragments in the tau microtubule-binding domain. Eur. J. Biochem. 271 (2004) 545-552
80. Abraha A., Ghoshal N., Gamblin T.C., Cryns V., Berry R.W., Kuret J., and Binder L.I. C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease. J. Cell Sci. 113 (2000) 3737-3745
81. Gamblin T.C., Berry R.W., and Binder L.I. Modeling tau polymerization in vitro: a review and synthesis. Biochemistry 42 (2003) 15009-15017
82. von Bergen M., Barghorn S., Li L., Marx A., Biernat J., Mandelkow E.M., and Mandelkow E. Mutations of tau protein in frontotemporal dementia promote aggregation of paired helical filaments by enhancing local beta-structure. J. Biol. Chem. 276 (2001) 48165-48174
83. Kar S., Fan J., Smith M.J., Goedert M., and Amos L.A. Repeat motifs of tau bind to the insides of microtubules in the absence of taxol. EMBO J. 22 (2003) 70-77
84. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes [see comments]. J. Biomol. NMR 6 (1995) 277-293
85. Johnson B.A., and Blevins R.A. NMRView: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4 (1994) 603-614
86. 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR 5 (1995) 67-81
87. Eliezer D., Kutluay E., Bussell Jr. R., and Browne G. Conformational properties of alpha-synuclein in its free and lipid- associated states. J. Mol. Biol. 307 (2001) 1061-1073