Spectroscopic approaches to the conformation of tau protein in solution and in paired helical filaments

Neurodegenerative Diseases

Volumn 3, Issue 4-5, 2006, Pages 197-206

  Von Bergen, M ^a   Barghorn, S ^a   Jeganathan, S ^a   Mandelkow, E M ^a   Mandelkow, E ^a  

^a MAX PLANCK UNIT FOR STRUCTURAL MOLECULAR BIOLOGY   (Germany)

Author keywords

Alzheimer's disease; Microtubule associated proteins; Paired helical filament; Tau protein

Indexed keywords

AMINO ACID; GADOLINIUM; ISOPROTEIN; MICROTUBULE ASSOCIATED PROTEIN; SOLVENT; TAU PROTEIN; TRYPTOPHAN;

AMINO ACID SEQUENCE; ASSAY; BETA SHEET; CIRCULAR DICHROISM; CONFERENCE PAPER; DISSOLUTION; FLUOROMETRY; HYDRODYNAMICS; HYDROPHOBICITY; INFRARED SPECTROSCOPY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PAIRED HELICAL FILAMENT; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN FOLDING; RADIATION SCATTERING; SITE DIRECTED MUTAGENESIS; SPECTROSCOPY;

ANIMALS; HUMANS; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; SPECTRUM ANALYSIS; TAU PROTEINS;

EID: 33750185145     PISSN: 16602854     EISSN: 16602862     Source Type: Journal    
DOI: 10.1159/000095257     Document Type: Conference Paper

References (64)

1. Drubin DG, Kirschner MW: Tau protein function in living cells. J Cell Biol 1986;103:2739-2746.
2. Garcia ML, Cleveland DW: Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr Opin Cell Biol 2001;13:41-48.
3. Goedert M, Spillantini MG: Tau mutations in frontotemporal dementia FTDP-17 and their relevance for Alzheimer's disease. Biochim Biophys Acta 2000;1502:110-121.
4. Andreadis A, Brown WM, Kosik KS: Structure and novel exons of the human tau gene. Biochemistry 1992;31:10626-10633.
5. Andreadis A: Tau gene alternative splicing: expression patterns, regulation and modulation of function in normal brain and neurodegenerative diseases. Biochim Biophys Acta 2005;1739:91-103.
6. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA: Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989;3:519-526.
7. Friedhoff P, Mandelkow E: Tau protein; in Kreis T, Vale R (eds): Guidebooks to the Cytoskeletal and Motor Proteins and to the Extracellular Matrix and Adhesion Proteins. Oxford, Oxford University Press, 1998.
8. Santarella RA, Skiniotis G, Goldie KN, Tittmann P, Gross H, Mandelkow EM, Mandelkow E, Hoenger A: Surface-decoration of microtubules by human tau. J Mol Biol 2004;339:539-553.
9. Mukrasch MD, Biernat J, von Bergen M, Griesinger C, Mandelkow E, Zweckstetter M: Sites of TAU important for aggregation populate beta-structure and bind to microtubules and polyanions. J Biol Chem 2005;280:24978-24986.
10. von Bergen M, Friedhoff P, Biernat J, Heberle J, Mandelkow EM, 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 2000;97:5129-5134.
11. Wischik CM, Novak M, Edwards PC, Klug A, Tichelaar W, Crowther RA: Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci USA 1988;85:4884-4888.
12. von Bergen M, Barghorn S, Müller SA, Pickhardt M, Biernat J, Mandelkow EM, Davies P, Aebi U, Mandelkow E: The core of Tau paired helical filaments studied by STEM and limited proteolysis. Biochemistry 2006;45:6446-6457.
13. Wright PE, Dyson HJ: Intrinsically unstructured proteins: re-assessing the protein structure- function paradigm. J Mol Biol 1999;293:321-331.
14. Tompa P: Intrinsically unstructured proteins. Trends Biochem Sci 2002;27:527-533.
15. Uversky VN, Gillespie JR, Fink AL: Why are 'natively unfolded' proteins unstructured under physiologic conditions? Proteins 2000;41:415-427.
16. Denning DP, Uversky V, Patel SS, Fink AL, Rexach M: The Saccharomyces cerevisiae nucleoporin Nup2p is a natively unfolded protein. J Biol Chem 2002;277:33447-33455.
17. +-dependent protease (calpain) and its high-molecular-weight endogenous inhibitor (calpastatin). Adv Enzyme Regul 1980;19:407-424.
18. Uemori T, Shimojo T, Asada K, Asano T, Kimizuka F, Kato I, Maki M, Hatanaka M, Murachi T, Hanzawa H, et al: Characterization of a functional domain of human calpastatin. Biochem Biophys Res Commun 1990;166:1485-1493.
19. Permyakov SE, Millett IS, Doniach S, Permyakov EA, Uversky VN: Natively unfolded C-terminal domain of caldesmon remains substantially unstructured after the effective binding to calmodulin. Proteins 2003;53:855-862.
20. Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW: A protein factor essential for microtubule assembly. Proc Natl Acad Sci USA 1975;72:1858-1862.
21. Cleveland DW, Hwo SY, Kirschner MW: Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J Mol Biol 1977;116:227-247.
22. Lee G, Cowan N, Kirschner M: The primary structure and heterogeneity of tau protein from mouse brain. Science 1988;239:285-288.
23. Goedert M, Wischik CM, Crowther RA, Walker JE, 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 1988;85:4051-4055.
24. Romero P, Obradovic Z, Li X, Garner EC, Brown CJ, Dunker AK: Sequence complexity of disordered protein. Proteins 2001;42:38-48.
25. Li X, Romero P, Rani M, Dunker AK, Obradovic Z: Predicting protein disorder for N-, C-, and internal regions. Genome Inform Ser Workshop Genome Inform 1999;10:30-40.
26. Uversky VN: Natively unfolded proteins: a point where biology waits for physics. Protein Sci 2002;11:739-756.
27. Prilusky J, Felder CE, Zeev-Ben-Mordehai T, Rydberg E, Man O, Beckmann JS, Silman I, Sussman JL: Foldlndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 2005;21:3435-3438.
28. Romero, Obradovic, Dunker K: Sequence data analysis for long disordered regions prediction in the calcineurin family. Genome Inform Ser Workshop Genome Inform 1997;8:110-124.
29. Schweers O, Schonbrunn-Hanebeck E, Marx A, Mandelkow E: Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for beta-structure. J Biol Chem 1994;269:24290-24297.
30. Barghorn S, Davies P, Mandelkow E: Tau paired helical filaments from Alzheimer's disease brain and assembled in vitro are based on beta-structure in the core domain. Biochemistry 2004;43:1694-1703.
31. Abraha A, Ghoshal N, Gamblin TC, Cryns V, Berry RW, Kuret J, Binder LI: C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease. J Cell Sci 2000;113:3737-3745.
32. Esposito G, Viglino P, Novak M, Cattaneo A: The solution structure of the C-terminal segment of tau protein. J Pept Sci 2000;6:550-559.
33. Chau MF, Radeke MJ, de Ines C, Barasoain I, Kohlstaedt LA, Feinstein SC: The microtubule-associated protein tau cross-links to two distinct sites on each alpha and beta tubulin monomer via separate domains. Biochemistry 1998;37:17692-17703.
34. Downing KH, Nogales E: Crystallographic structure of tubulin: implications for dynamics and drug binding. Cell Struct Funct 1999;24:269-275.
35. Kyte J, Doolittle RF: A simple method for displaying the hydropathic character of a protein. J Mol Biol 1982;157:105-132.
36. Linding R, Russell RB, Neduva V, Gibson TJ: GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res 2003;31:3701-3708.
37. Linding R, Jensen LJ, Diella F, Bork P, Gibson TJ, Russell RB: Protein disorder prediction: implications for structural proteomics. Structure 2003;11:1453-1459.
38. Fernandez-Escamilla AM, Rousseau F, Schymkowitz J, Serrano L: Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat Biotechnol 2004;22:1302-1306.
39. Nelson R, Sawaya MR, Balbirnie M, Madsen AO, Riekel C, Grothe R, Eisenberg D: Structure of the cross-beta spine of amyloid-like fibrils. Nature 2005;435:773-778.
40. Thompson MJ, Sievers SA, Karanicolas J, Ivanova MI, Baker D, Eisenberg D: The 3D profile method for identifying fibril-forming segments of proteins. Proc Natl Acad Sci USA 2006;103:4074-4078.
41. Jeganathan S, von Bergen M, Brutlach H, Steinhoff HJ, Mandelkow E: Global hairpin folding of tau in solution. Biochemistry 2006;45:2283-2293.
42. Hannemann F, Bera AK, Fischer B, Lisurek M, Teuchner K, Bernhardt R: Unfolding and conformational studies on bovine adrenodoxin probed by engineered intrinsic tryptophan fluorescence. Biochemistry 2002;41:11008-11016.
43. Li L, von Bergen M, Mandelkow EM, Mandelkow E: Structure, stability, and aggregation of paired helical filaments from tau protein and FTDP-17 mutants probed by tryptophan scanning mutagenesis. J Biol Chem 2002;277:41390-41400.
44. Eftink MR: Fluorescence techniques for studying protein structure. Methods Biochem Anal 1991;35:127-205.
45. Kohn JE, Millett IS, Jacob J, Zagrovic B, Dillon TM, Cingel N, Dothager RS, Seifert S, Thiyagarajan P, Sosnick TR, Hasan MZ, Pande VS, Ruczinski I, Doniach S, Plaxco KW: Random-coil behavior and the dimensions of chemically unfolded proteins. Proc Natl Acad Sci USA 2004;101:12491-12496.
46. Jicha GA, Bowser R, Kazam IG, Davies P: Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau. J Neurosci Res 1997;48:128-132.
47. Skrabana R, Kontsek P, Mederlyova A, Iqbal K, Novak M: Folding of Alzheimer's core PHF subunit revealed by monoclonal antibody 423. FEBS Lett 2004;568:178-182.
48. Ghoshal N, Garcia-Sierra F, Fu Y, Beckett LA, Mufson EJ, Kuret J, Berry RW, Binder LI: Tau-66: evidence for a novel tau conformation in Alzheimer's disease. J Neurochem 2001;77:1372-1385.
49. Jeganathan S, von Bergen M, Brutlach H, Steinhoff HJ, Mandelkow E: Global hairpin folding of tau in solution. Biochemistry 2006;45:2283-2293.
50. Dobson CM: Protein folding and misfolding. Nature 2003;426:884-890.
51. Selkoe DJ: Folding proteins in fatal ways. Nature 2003;426:900-904.
52. Caughey B, Lansbury PT Jr: Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu Rev Neurosci 2003;26:267-298.
53. Mandelkow E, Song YH, Schweers O, Marx A, Mandelkow EM: On the structure of microtubules, tau, and paired helical filaments. Neurobiol Aging 1995;16:347-354.
54. von Bergen M, Barghorn S, Biernat J, Mandelkow EM, Mandelkow E: Tau aggregation is driven by a transition from random coil to beta sheet structure. Biochim Biophys Acta 2005;1739:158-166.
55. Kirschner DA, Teplow DB, Damas AM: Twist and sheet: variations on the theme of amyloid. J Struct Biol 2000;130:87.
56. Sunde M, Serpell LC, Bartlam M, Fraser PE, Pepys MB, Blake CC: Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J Mol Biol 1997;273:729-739.
57. Makin OS, Serpell LC: Structures for amyloid fibrils. FEBS J 2005;272:5950-5961.
58. Sanchez SA, Brunet JE, Jameson DM, Lagos R, Monasterio O: Tubulin equilibrium unfolding followed by time-resolved fluorescence and fluorescence correlation spectroscopy. Protein Sci 2004;13:81-88.
59. Murali J, Jayakumar R: Spectroscopic studies on native and protofibrillar insulin. J Struct Biol 2005;150:180-189.
60. Pickhardt M, Gazova Z, von Bergen M, Khlistunova I, Wang Y, Hascher A, Mandelkow EM, Biernat J, Mandelkow E: Anthraquinones inhibit tau aggregation and dissolve Alzheimer's paired helical filaments in vitro and in cells. J Biol Chem 2005;280:3628-3635.
61. Necula M, Chirita CN, Kuret J: Cyanine dye N744 inhibits tau fibrillization by blocking filament extension: Implications for the treatment of tauopathic neurodegenerative diseases. Biochemistry 2005;44:10227-10237.
62. Taniguchi S, Suzuki N, Masuda M, Hisanaga S, Iwatsubo T, Goedert M, Hasegawa M: Inhibition of heparin-induced tau filament formation by phenothiazines, polyphenols, and porphyrins. J Biol Chem 2005;280:7614-7623.
63. Wischik CM, Edwards PC, Lai RY, Roth M, Harrington CR: Selective inhibition of Alzheimer disease-like tau aggregation by phenothiazines. Proc Natl Acad Sci USA 1996;93:11213-11218.
64. Romero P, Obradovic Z, Dunker AK: Natively disordered proteins: functions and predictions. Appl Bioinformatics 2004;3:105-113.