Positional effects of phosphorylation on the stability and morphology of tau-related amyloid fibrils

Biochemistry

Volumn 51, Issue 7, 2012, Pages 1396-1406

  Inoue, Masafumi ^a   Konno, Takashi ^c   Tainaka, Kazuki ^a   Nakata, Eiji ^a   Yoshida, Hiro O ^a   Morii, Takashi ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF FUKUI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER'S DISEASE; AMINO ACID RESIDUES; AMINO GROUP; AMYLOID FIBRIL; CHARGED RESIDUES; CRITICAL CONCENTRATION; FIBRIL STABILITY; FOURIER TRANSFORM INFRARED; HYPERPHOSPHORYLATED; INTERSHEET INTERACTION; ISOFORMS; MAIN COMPONENT; MICROTUBULE-BINDING DOMAINS; N-TERMINALS; NET CHARGES; NEUROFIBRILLARY TANGLES; PAIRED HELICAL FILAMENTS; PHOSPHATE GROUP; PHOSPHORYLATED PEPTIDES; PROTOFILAMENTS; SERINE RESIDUES; STRAIGHT FIBERS; TAU PROTEINS; TYROSINE PHOSPHORYLATION; X RAY FIBER DIFFRACTION;

AMINO ACIDS; FIBERS; GLYCOPROTEINS; PHOSPHORYLATION; TRANSMISSION ELECTRON MICROSCOPY;

PEPTIDES;

AMYLOID; TAU PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; INFRARED SPECTROSCOPY; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY; X RAY DIFFRACTION;

AMYLOID; HUMANS; HYDROGEN-ION CONCENTRATION; LYSINE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROTUBULES; PEPTIDES; PHOSPHATES; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, SECONDARY; SERINE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TAU PROTEINS; X-RAY DIFFRACTION;

EID: 84857435692     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201451z     Document Type: Article

References (64)

1. Dobson, C. M. (2003) Protein folding and misfolding Nature 426, 884-890
2. Chiti, F. and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75, 333-366
3. Selkoe, D. J. (1991) The molecular pathology of Alzheimer's disease Neuron 6, 487-498
4. Morishima-Kawashima, M., Hasegawa, M., Takio, K., Suzuki, M., Yoshida, H., Titani, K., and Ihara, Y. (1995) Proline-directed and non-proline-directed phosphorylation of PHF-tau J. Biol. Chem. 270, 823-829
5. Goedert, M., Spillantini, M. G., Cairns, N. J., and Crowther, R. A. (1992) Tau proteins of Alzheimer paired helical filaments: Aabnormal phosphorylation of all six brain isoforms Neuron 8, 159-168
6. Lee, V. M., Balin, B. J., Otvos, L., Jr., and Trojanowski, J. Q. (1991) A68: A major subunit of paired helical filaments and derivatized forms of normal Tau Science 251, 675-678
7. Hernandez, F. and Avila, J. (2007) Tauopathies Cell. Mol. Life Sci. 64, 2219-2233
8. Gong, C. X., Liu, F., Grundke-Iqbal, I., and Iqbal, K. (2005) Post-translational modifications of tau protein in Alzheimer's disease J. Neural Transm. 112, 813-838
9. Bielska, A. A. and Zondlo, N. J. (2006) Hyperphosphorylation of tau induces local polyproline II helix Biochemistry 45, 5527-5537
10. 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
11. Jicha, G. A., Lane, E., Vincent, I., Otvos, L., Jr., Hoffmann, R., and Davies, P. (1997) A conformation and phosphorylation-dependent antibody recognizing the paired helical filaments of Alzheimer's disease J. Neurochem. 69, 2087-2095
12. 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
13. Kidd, M. (1963) Paired helical filaments in electron microscopy of Alzheimer's disease Nature 197, 192-193
14. Perez, M., Valpuesta, J. M., de Garcini, E. M., Quintana, C., Arrasate, M., Lopez Carrascosa, J. L., Rabano, A., Garcia de Yebenes, J., and Avila, J. (1998) Ferritin is associated with the aberrant tau filaments present in progressive supranuclear palsy Am. J. Pathol. 152, 1531-1539
15. Wray, S., Saxton, M., Anderton, B. H., and Hanger, D. P. (2008) Direct analysis of tau from PSP brain identifies new phosphorylation sites and a major fragment of N-terminally cleaved tau containing four microtubule-binding repeats J. Neurochem. 105, 2343-2352
16. Santa-Maria, I., Hernandez, F., Martin, C. P., Avila, J., and Moreno, F. J. (2004) Quinones facilitate the self-assembly of the phosphorylated tubulin binding region of tau into fibrillar polymers Biochemistry 43, 2888-2897
17. Hanger, D. P., Anderton, B. H., and Noble, W. (2009) Tau phosphorylation: The therapeutic challenge for neurodegenerative disease Trends Mol. Med. 15, 112-119
18. Makin, O. S., Atkins, E., Sikorski, P., Johansson, J., and Serpell, L. C. (2005) Molecular basis for amyloid fibril formation and stability Proc. Natl. Acad. Sci. U.S.A. 102, 315-320
19. Tjernberg, L., Hosia, W., Bark, N., Thyberg, J., and Johansson, J. (2002) Charge attraction and β propensity are necessary for amyloid fibril formation from tetrapeptides J. Biol. Chem. 277, 43243-43246
20. Inoue, M., Hirata, A., Tainaka, K., Morii, T., and Konno, T. (2008) Charge-pairing mechanism of phosphorylation effect upon amyloid fibrillation of human tau core peptide Biochemistry 47, 11847-11857
21. Li, W. and Lee, V. M. (2006) Characterization of two VQIXXK motifs for tau fibrillization in vitro Biochemistry 45, 15692-15701
22. 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
23. Morishima-Kawashima, M., Hasegawa, M., Takio, K., Suzuki, M., Yoshida, H., Watanabe, A., Titani, K., and Ihara, Y. (1995) Hyperphosphorylation of tau in PHF Neurobiol. Aging 16, 365-371
24. Hanger, D. P., Betts, J. C., Loviny, T. L., Blackstock, W. P., and Anderton, B. H. (1998) New phosphorylation sites identified in hyperphosphorylated tau (paired helical filament-tau) from Alzheimer's disease brain using nanoelectrospray mass spectrometry J. Neurochem. 71, 2465-2476
25. Hanger, D. P., Byers, H. L., Wray, S., Leung, K. Y., Saxton, M. J., Seereeram, A., Reynolds, C. H., Ward, M. A., and Anderton, B. H. (2007) Novel phosphorylation sites in tau from Alzheimer brain support a role for casein kinase 1 in disease pathogenesis J. Biol. Chem. 282, 23645-23654
26. Wischik, C. M., Novak, M., Thogersen, 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
27. 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
28. Fernandez-Escamilla, A. M., Rousseau, F., Schymkowitz, J., and Serrano, L. (2004) Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins Nat. Biotechnol. 22, 1302-1306
29. Chiti, F., Calamai, M., Taddei, N., Stefani, M., Ramponi, G., and Dobson, C. M. (2002) Studies of the aggregation of mutant proteins in vitro provide insights into the genetics of amyloid diseases Proc. Natl. Acad. Sci. U.S.A. 99, 16419-16426
30. Yankner, B. A., Duffy, L. K., and Kirschner, D. A. (1990) Neurotrophic and neurotoxic effects of amyloid β protein: Reversal by tachykinin neuropeptides Science 250, 279-282
31. Azriel, R. and Gazit, E. (2001) Analysis of the minimal amyloid-forming fragment of the islet amyloid polypeptide. An experimental support for the key role of the phenylalanine residue in amyloid formation J. Biol. Chem. 276, 34156-34161
32. 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
33. Thompson, M. J., Sievers, S. A., Karanicolas, J., Ivanova, M. I., Baker, D., and Eisenberg, D. (2006) The 3D profile method for identifying fibril-forming segments of proteins Proc. Natl. Acad. Sci. U.S.A. 103, 4074-4078
34. Nelson, R., Sawaya, M. R., Balbirnie, M., Madsen, A. O., Riekel, C., Grothe, R., and Eisenberg, D. (2005) Structure of the cross-β spine of amyloid-like fibrils Nature 435, 773-778
35. Sawaya, M. R., Sambashivan, S., Nelson, R., Ivanova, M. I., Sievers, S. A., Apostol, M. I., Thompson, M. J., Balbirnie, M., Wiltzius, J. J., McFarlane, H. T., Madsen, A. O., Riekel, C., and Eisenberg, D. (2007) Atomic structures of amyloid cross-β spines reveal varied steric zippers Nature 447, 453-457
36. 311) forming β structure Proc. Natl. Acad. Sci. U.S.A. 97, 5129-5134
37. 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
38. Rojas Quijano, F. A., Morrow, D., Wise, B. M., Brancia, F. L., and Goux, W. J. (2006) Prediction of nucleating sequences from amyloidogenic propensities of tau-related peptides Biochemistry 45, 4638-4652
39. Hirata, A., Sugimoto, K., Konno, T., and Morii, T. (2007) Amyloid-forming propensity of the hydrophobic non-natural amino acid on the fibril-forming core peptide of human tau Bioorg. Med. Chem. Lett. 17, 2971-2974
40. Hensley, K., Floyd, R. A., Zheng, N. Y., Nael, R., Robinson, K. A., Nguyen, X., Pye, Q. N., Stewart, C. A., Geddes, J., Markesbery, W. R., Patel, E., Johnson, G. V., and Bing, G. (1999) p38 kinase is activated in the Alzheimer's disease brain J. Neurochem. 72, 2053-2058
41. Drewes, G., Ebneth, A., Preuss, U., Mandelkow, E. M., and Mandelkow, E. (1997) MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption Cell 89, 297-308
42. Lee, V. M., Goedert, M., and Trojanowski, J. Q. (2001) Neurodegenerative tauopathies Annu. Rev. Neurosci. 24, 1121-1159
43. Lomakin, A., Chung, D. S., Benedek, G. B., Kirschner, D. A., and Teplow, D. B. (1996) On the nucleation and growth of amyloid β-protein fibrils: Detection of nuclei and quantitation of rate constants Proc. Natl. Acad. Sci. U.S.A. 93, 1125-1129
44. O'Nuallain, B., Shivaprasad, S., Kheterpal, I., and Wetzel, R. (2005) Thermodynamics of Aβ(1-40) amyloid fibril elongation Biochemistry 44, 12709-12718
45. Harper, J. D. and Lansbury, P. T., Jr. (1997) Models of amyloid seeding in Alzheimer's disease and scrapie: Mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins Annu. Rev. Biochem. 66, 385-407
46. Jarrett, J. T. and Lansbury, P. T., Jr. (1993) Seeding "one-dimensional crystallization" of amyloid: A pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73, 1055-1058
47. Krimm, S. and Bandekar, J. (1986) Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins Adv. Protein Chem. 38, 181-364
48. Kirschner, D. A., Inouye, H., Duffy, L. K., Sinclair, A., Lind, M., and Selkoe, D. J. (1987) Synthetic peptide homologous to β protein from Alzheimer disease forms amyloid-like fibrils in vitro Proc. Natl. Acad. Sci. U.S.A. 84, 6953-6957
49. Kirschner, D. A., Abraham, C., and Selkoe, D. J. (1986) X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-β conformation Proc. Natl. Acad. Sci. U.S.A. 83, 503-507
50. Sunde, M., Serpell, L. C., Bartlam, M., Fraser, P. E., Pepys, M. B., and Blake, C. C. (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction J. Mol. Biol. 273, 729-739
51. Ivanova, M. I., Sievers, S. A., Sawaya, M. R., Wall, J. S., and Eisenberg, D. (2009) Common core structure of amyloid fibrils by synchrotron X-ray diffraction Proc. Natl. Acad. Sci. U.S.A. 106, 18990-18995
52. Jahn, T. R., Makin, O. S., Morris, K. L., Marshall, K. E., Tian, P., Sikorski, P., and Serpell, L. C. (2009) The common architecture of cross-β amyloid J. Mol. Biol. 395, 717-727
53. Balbirnie, M., Grothe, R., and Eisenberg, D. S. (2001) An amyloid-forming peptide from the yeast prion Sup35 reveals a dehydrated β-sheet structure for amyloid Proc. Natl. Acad. Sci. U.S.A. 98, 2375-2380
54. Serpell, L. C., Fraser, P. E., and Sunde, M. (1999) X-ray fiber diffraction of amyloid fibrils Methods Enzymol. 309, 526-536
55. Lim, A., Makhov, A. M., Bond, J., Inouye, H., Connors, L. H., Griffith, J. D., Erickson, B. W., Kirschner, D. A., and Costello, C. E. (2000) Betabellins 15D and 16D, de novo designed β-sandwich proteins that have amyloidogenic properties J. Struct. Biol. 130, 363-370
56. Blake, C. and Serpell, L. (1996) Synchrotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous β-sheet helix Structure 4, 989-998
57. Malinchik, S. B., Inouye, H., Szumowski, K. E., and Kirschner, D. A. (1998) Structural analysis of Alzheimer's β(1-40) amyloid: Protofilament assembly of tubular fibrils Biophys. J. 74, 537-545
58. 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
59. Rousseau, F., Serrano, L., and Schymkowitz, J. W. H. (2006) How evolutionary pressure against protein aggregation shaped chaperone specificity J. Mol. Biol. 355, 1037-1047
60. Rousseau, F., Schymkowitz, J., and Serrano, L. (2006) Protein aggregation and amyloidosis: Confusion of the kinds? Curr. Opin. Struct. Biol. 16, 118-126
61. Pedersen, J. S., Christensen, G., and Otzen, D. E. (2004) Modulation of S6 fibrillation by unfolding rates and gatekeeper residues J. Mol. Biol. 341, 575-588
62. Konno, T. (2001) Amyloid-induced aggregation and precipitation of soluble proteins: An electrostatic contribution of the Alzheimer's β(25-35) amyloid fibril Biochemistry 40, 2148-2154
63. Konno, T., Oiki, S., Hasegawa, K., and Naiki, H. (2004) Anionic contribution for fibrous maturation of protofibrillar assemblies of the human tau repeat domain in a fluoroalcohol solution Biochemistry 43, 13613-13620
64. Avila, J. (2009) The tau code Front. Aging Neurosci. 1, 1-5