Nuclear magnetic resonance analysis of the acetylation pattern of the neuronal Tau protein

Biochemistry

Volumn 53, Issue 18, 2014, Pages 3020-3032

  Kamah, Amina ^a   Huvent, Isabelle ^a   Cantrelle, François Xavier ^a   Qi, Haoling ^a,b   Lippens, Guy ^a   Landrieu, Isabelle ^a,b   Smet Nocca, Caroline ^a  

^a UNIV LILLE   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYSACCHARIDES; PROTEINS;

ACETYL TRANSFERASE; AGGREGATION PROCESS; ALZHEIMER'S DISEASE; CREB BINDING PROTEINS; HEPARIN BINDING; HIGH RESOLUTION; NONENZYMATIC REACTION; POSTTRANSLATIONAL REGULATION;

ACETYLATION;

ACETYL COENZYME A; ACYLTRANSFERASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; HEPARIN; LYSINE; TAU PROTEIN;

ACETYLATION; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CATALYSIS; CONTROLLED STUDY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; IN VITRO STUDY; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN PROCESSING; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; WILD TYPE;

ACETYLATION; CYSTEINE; HEPARIN; HUMANS; KINETICS; NITROGEN ISOTOPES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; P300-CBP TRANSCRIPTION FACTORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TAU PROTEINS;

EID: 84900556648     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500006v     Document Type: Article

References (49)

1. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M. L., Rehman, M., Walther, T. C., Olsen, J. V., and Mann, M. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions Science 325, 834-840
2. Ito, A., Kawaguchi, Y., Lai, C. H., Kovacs, J. J., Higashimoto, Y., Appella, E., and Yao, T. P. (2002) MDM2-HDAC1-mediated deacetylation of p53 is required for its degradation EMBO J. 21, 6236-6245
3. Cripps, D., Thomas, S. N., Jeng, Y., Yang, F., Davies, P., and Yang, A. J. (2006) Alzheimer disease-specific conformation of hyperphosphorylated paired helical filament-Tau is polyubiquitinated through Lys-48, Lys-11, and Lys-6 ubiquitin conjugation J. Biol. Chem. 281, 10825-10838
4. Tai, H. C., Serrano-Pozo, A., Hashimoto, T., Frosch, M. P., Spires-Jones, T. L., and Hyman, B. T. (2012) The synaptic accumulation of hyperphosphorylated tau oligomers in Alzheimer disease is associated with dysfunction of the ubiquitin-proteasome system Am. J. Pathol. 181, 1426-1435
5. Mori, H., Kondo, J., and Ihara, Y. (1987) Ubiquitin is a component of paired helical filaments in Alzheimer's disease Science 235, 1641-1644
6. Min, S. W., Cho, S. H., Zhou, Y., Schroeder, S., Haroutunian, V., Seeley, W. W., Huang, E. J., Shen, Y., Masliah, E., Mukherjee, C., Meyers, D., Cole, P. A., Ott, M., and Gan, L. (2010) Acetylation of tau inhibits its degradation and contributes to tauopathy Neuron 67, 953-966
7. Petrucelli, L., Dickson, D., Kehoe, K., Taylor, J., Snyder, H., Grover, A., De Lucia, M., McGowan, E., Lewis, J., Prihar, G., Kim, J., Dillmann, W. H., Browne, S. E., Hall, A., Voellmy, R., Tsuboi, Y., Dawson, T. M., Wolozin, B., Hardy, J., and Hutton, M. (2004) CHIP and Hsp70 regulate tau ubiquitination, degradation and aggregation Hum. Mol. Genet. 13, 703-714
8. Tan, J. M., Wong, E. S., Kirkpatrick, D. S., Pletnikova, O., Ko, H. S., Tay, S. P., Ho, M. W., Troncoso, J., Gygi, S. P., Lee, M. K., Dawson, V. L., Dawson, T. M., and Lim, K. L. (2008) Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases Hum. Mol. Genet. 17, 431-439
9. Julien, C., Tremblay, C., Emond, V., Lebbadi, M., Salem, N., Jr., Bennett, D. A., and Calon, F. (2009) Sirtuin 1 reduction parallels the accumulation of tau in Alzheimer disease J. Neuropathol. Exp. Neurol. 68, 48-58
10. Cohen, T. J., Guo, J. L., Hurtado, D. E., Kwong, L. K., Mills, I. P., Trojanowski, J. Q., and Lee, V. M. (2011) The acetylation of tau inhibits its function and promotes pathological tau aggregation Nat. Commun. 2, 252
11. Goode, B. L. and Feinstein, S. C. (1994) Identification of a novel microtubule binding and assembly domain in the developmentally regulated inter-repeat region of tau J. Cell Biol. 124, 769-782
12. 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
13. Rizzu, P., Van Swieten, J. C., Joosse, M., Hasegawa, M., Stevens, M., Tibben, A., Niermeijer, M. F., Hillebrand, M., Ravid, R., Oostra, B. A., Goedert, M., van Duijn, C. M., and Heutink, P. (1999) High prevalence of mutations in the microtubule-associated protein tau in a population study of frontotemporal dementia in the Netherlands Am. J. Hum. Genet. 64, 414-421
14. 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
15. Hurtado, D. E., Molina-Porcel, L., Iba, M., Aboagye, A. K., Paul, S. M., Trojanowski, J. Q., and Lee, V. M. (2010) Aβ accelerates the spatiotemporal progression of tau pathology and augments tau amyloidosis in an Alzheimer mouse model Am. J. Pathol. 177, 1977-1988
16. Yoshiyama, Y., Higuchi, M., Zhang, B., Huang, S. M., Iwata, N., Saido, T. C., Maeda, J., Suhara, T., Trojanowski, J. Q., and Lee, V. M. (2007) Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model Neuron 53, 337-351
17. Irwin, D. J., Cohen, T. J., Grossman, M., Arnold, S. E., Xie, S. X., Lee, V. M., and Trojanowski, J. Q. (2012) Acetylated tau, a novel pathological signature in Alzheimer's disease and other tauopathies Brain 135, 807-818
18. Grinberg, L. T., Wang, X., Wang, C., Sohn, P. D., Theofilas, P., Sidhu, M., Arevalo, J. B., Heinsen, H., Huang, E. J., Rosen, H., Miller, B. L., Gan, L., and Seeley, W. W. (2013) Argyrophilic grain disease differs from other tauopathies by lacking tau acetylation Acta Neuropathol. 125, 581-593
19. Cook, C., Carlomagno, Y., Gendron, T. F., Dunmore, J., Scheffel, K., Stetler, C., Davis, M., Dickson, D., Jarpe, M., Deture, M., and Petrucelli, L. (2014) Acetylation of the KXGS motifs in tau is a critical determinant in modulation of tau aggregation and clearance Hum. Mol. Genet. 23, 104-116
20. Drewes, G., Trinczek, B., Illenberger, S., Biernat, J., Schmitt-Ulms, G., Meyer, H. E., Mandelkow, E. M., and Mandelkow, E. (1995) Microtubule-associated protein/microtubule affinity-regulating kinase (p110mark). A novel protein kinase that regulates tau-microtubule interactions and dynamic instability by phosphorylation at the Alzheimer-specific site serine 262 J. Biol. Chem. 270, 7679-7688
21. Schneider, A., Biernat, J., von Bergen, M., Mandelkow, E., and Mandelkow, E. M. (1999) Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments Biochemistry 38, 3549-3558
22. Smet-Nocca, C., Wieruszeski, J. M., Melnyk, O., and Benecke, A. (2010) NMR-based detection of acetylation sites in peptides J. Pept. Sci. 16, 414-423
23. Dose, A., Liokatis, S., Theillet, F. X., Selenko, P., and Schwarzer, D. (2011) NMR profiling of histone deacetylase and acetyl-transferase activities in real time ACS Chem. Biol. 6, 419-424
24. Cohen, T. J., Friedmann, D., Hwang, A. W., Marmorstein, R., and Lee, V. M. (2013) The microtubule-associated tau protein has intrinsic acetyltransferase activity Nat. Struct. Mol. Biol. 20, 756-762
25. Tini, M., Benecke, A., Um, S. J., Torchia, J., Evans, R. M., and Chambon, P. (2002) Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription Mol. Cell 9, 265-277
26. Kuo, Y. M. and Andrews, A. J. (2013) Quantitating the specificity and selectivity of Gcn5-mediated acetylation of histone H3 PLoS One 8, e54896
27. Henry, R. A., Kuo, Y. M., and Andrews, A. J. (2013) Differences in Specificity and Selectivity Between CBP and p300 Acetylation of Histone H3 and H3/H4 Biochemistry 52, 5746-5759
28. Dormeyer, W., Ott, M., and Schnolzer, M. (2005) Probing lysine acetylation in proteins: Strategies, limitations, and pitfalls of in vitro acetyltransferase assays Mol. Cell. Proteomics 4, 1226-1239
29. Liokatis, S., Dose, A., Schwarzer, D., and Selenko, P. (2010) Simultaneous detection of protein phosphorylation and acetylation by high-resolution NMR spectroscopy J. Am. Chem. Soc. 132, 14704-14705
30. Theillet, F. X., Smet-Nocca, C., Liokatis, S., Thongwichian, R., Kosten, J., Yoon, M. K., Kriwacki, R. W., Landrieu, I., Lippens, G., and Selenko, P. (2012) Cell signaling, post-translational protein modifications and NMR spectroscopy J. Biomol. NMR 54, 217-236
31. Fauquant, C., Redeker, V., Landrieu, I., Wieruszeski, J. M., Verdegem, D., Laprevote, O., Lippens, G., Gigant, B., and Knossow, M. (2011) Systematic identification of tubulin-interacting fragments of the microtubule-associated protein Tau leads to a highly efficient promoter of microtubule assembly J. Biol. Chem. 286, 33358-33368
32. Verdegem, D., Dijkstra, K., Hanoulle, X., and Lippens, G. (2008) Graphical interpretation of Boolean operators for protein NMR assignments J. Biomol. NMR 42, 11-21
33. Sibille, N., Sillen, A., Leroy, A., Wieruszeski, J. M., Mulloy, B., Landrieu, I., and Lippens, G. (2006) Structural impact of heparin binding to full-length Tau as studied by NMR spectroscopy Biochemistry 45, 12560-12572
34. Schutz, A. K., Soragni, A., Hornemann, S., Aguzzi, A., Ernst, M., Bockmann, A., and Meier, B. H. (2011) The amyloid-Congo red interface at atomic resolution Angew. Chem., Int. Ed. 50, 5956-5960
35. Irwin, D. J., Cohen, T. J., Grossman, M., Arnold, S. E., McCarty-Wood, E., Van Deerlin, V. M., Lee, V. M., and Trojanowski, J. Q. (2013) Acetylated tau neuropathology in sporadic and hereditary tauopathies Am. J. Pathol. 183, 344-351
36. 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
37. Landrieu, I., Leroy, A., Smet-Nocca, C., Huvent, I., Amniai, L., Hamdane, M., Sibille, N., Buee, L., Wieruszeski, J. M., and Lippens, G. (2010) NMR spectroscopy of the neuronal tau protein: Normal function and implication in Alzheimer's disease Biochem. Soc. Trans. 38, 1006-1011
38. Smet-Nocca, C., Launay, H., Wieruszeski, J. M., Lippens, G., and Landrieu, I. (2013) Unraveling a phosphorylation event in a folded protein by NMR spectroscopy: Phosphorylation of the Pin1 WW domain by PKA J. Biomol. NMR 55, 323-337
39. Dormeyer, W., Dorr, A., Ott, M., and Schnolzer, M. (2003) Acetylation of the HIV-1 Tat protein: An in vitro study Anal. Bioanal. Chem. 376, 994-1005
40. von Bergen, M., Barghorn, S., Jeganathan, S., Mandelkow, E. M., and Mandelkow, E. (2006) Spectroscopic approaches to the conformation of tau protein in solution and in paired helical filaments Neurodegener. Dis. 3, 197-206
41. 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
42. Mukrasch, M. D., Bibow, S., Korukottu, J., Jeganathan, S., Biernat, J., Griesinger, C., Mandelkow, E., and Zweckstetter, M. (2009) Structural polymorphism of 441-residue tau at single residue resolution PLoS Biol. 7, e34
43. Schwalbe, M., Ozenne, V., Bibow, S., Jaremko, M., Jaremko, L., Gajda, M., Jensen, M. R., Biernat, J., Becker, S., Mandelkow, E., Zweckstetter, M., and Blackledge, M. (2014) Predictive atomic resolution descriptions of intrinsically disordered hTau40 and α-synuclein in solution from NMR and small angle scattering Structure 22, 238-249
44. Sinha, S., Lopes, D. H., and Bitan, G. (2012) A Key Role for Lysine Residues in Amyloid β-Protein Folding, Assembly, and Toxicity ACS Chem. Neurosci. 3, 473-481
45. Sinha, S., Lopes, D. H., Du, Z., Pang, E. S., Shanmugam, A., Lomakin, A., Talbiersky, P., Tennstaedt, A., McDaniel, K., Bakshi, R., Kuo, P. Y., Ehrmann, M., Benedek, G. B., Loo, J. A., Klarner, F. G., Schrader, T., Wang, C., and Bitan, G. (2011) Lysine-specific molecular tweezers are broad-spectrum inhibitors of assembly and toxicity of amyloid proteins J. Am. Chem. Soc. 133, 16958-16969
46. Marshall, K. E., Morris, K. L., Charlton, D., O'Reilly, N., Lewis, L., Walden, H., and Serpell, L. C. (2011) Hydrophobic, aromatic, and electrostatic interactions play a central role in amyloid fibril formation and stability Biochemistry 50, 2061-2071
47. Landau, M., Sawaya, M. R., Faull, K. F., Laganowsky, A., Jiang, L., Sievers, S. A., Liu, J., Barrio, J. R., and Eisenberg, D. (2011) Towards a pharmacophore for amyloid PLoS Biol. 9, e1001080
48. Holmes, B. B., DeVos, S. L., Kfoury, N., Li, M., Jacks, R., Yanamandra, K., Ouidja, M. O., Brodsky, F. M., Marasa, J., Bagchi, D. P., Kotzbauer, P. T., Miller, T. M., Papy-Garcia, D., and Diamond, M. I. (2013) Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds Proc. Natl. Acad. Sci. U.S.A. 110, E3138-E3147
49. Wolfe, M. S. (2009) Tau mutations in neurodegenerative diseases J. Biol. Chem. 284, 6021-6025