O-GlcNAc Modification of tau Directly Inhibits Its Aggregation without Perturbing the Conformational Properties of tau Monomers

Journal of Molecular Biology

Volumn 426, Issue 8, 2014, Pages 1736-1752

  Yuzwa, Scott A ^a   Cheung, Adrienne H ^b   Okon, Mark ^b   McIntosh, Lawrence P ^b   Vocadlo, David J ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Alzheimer's disease; glycosylation; NMR spectroscopy; paired helical filaments; tauopathy

Indexed keywords

HEPARIN; MONOMER; N ACETYLGLUCOSAMINE; TAU PROTEIN;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CATALYSIS; CIS TRANS ISOMERISM; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MICROTUBULE ASSEMBLY; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MODIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SOLUBILITY; STOICHIOMETRY;

ALZHEIMER'S DISEASE; GLYCOSYLATION; NMR SPECTROSCOPY; PAIRED HELICAL FILAMENTS; TAUOPATHY;

ACETYLGLUCOSAMINE; ALZHEIMER DISEASE; ANIMALS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; MICE; MICROTUBULES; MUTAGENESIS, SITE-DIRECTED; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; TAU PROTEINS; TUBULIN;

EID: 84897117088     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.01.004     Document Type: Article

References (69)

1. F. Oosawa, and M. Kasai A theory of linear and helical aggregations of macromolecules J Mol Biol 4 1962 10 21
2. E.E. Congdon, S. Kim, J. Bonchak, T. Songrug, A. Matzavinos, and J. Kuret Nucleation-dependent tau filament formation: the importance of dimerization and an estimation of elementary rate constants J Biol Chem 283 2008 13806 13816
3. P. Friedhoff, M. von Bergen, E.M. Mandelkow, P. Davies, and E. Mandelkow A nucleated assembly mechanism of Alzheimer paired helical filaments Proc Natl Acad Sci U S A 95 1998 15712 15717
4. J.T. Jarrett, E.P. Berger, and P.T. Lansbury The carboxy terminus of the beta amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease Biochemistry 32 1993 4693 4697
5. S.J. Wood, J. Wypych, S. Steavenson, J.C. Louis, M. Citron, and A.L. Biere alpha-Synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease J Biol Chem 274 1999 19509 19512
6. S.R. Collins, A. Douglass, R.D. Vale, and J.S. Weissman Mechanism of prion propagation: amyloid growth occurs by monomer addition PLoS Biol 2 2004 e321
7. C.N. Chirita, E.E. Congdon, H. Yin, and J. Kuret Triggers of full-length tau aggregation: a role for partially folded intermediates Biochemistry 44 2005 5862 5872
8. C.L. Weaver, M. Espinoza, Y. Kress, and P. Davies Conformational change as one of the earliest alterations of tau in Alzheimer's disease Neurobiol Aging 21 2000 719 727
9. A. Alonso, T. Zaidi, M. Novak, I. Grundke-Iqbal, and K. Iqbal Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments Proc Natl Acad Sci U S A 98 2001 6923 6928
10. A. Abraha, N. Ghoshal, T.C. Gamblin, V. Cryns, R.W. Berry, and J. Kuret et al. C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease J Cell Sci 113 2000 3737 3745
11. Y.P. Wang, J. Biernat, M. Pickhardt, E. Mandelkow, and E.M. Mandelkow Stepwise proteolysis liberates tau fragments that nucleate the Alzheimer-like aggregation of full-length tau in a neuronal cell model Proc Natl Acad Sci U S A 104 2007 10252 10257
12. H. Yin, and J. Kuret C-terminal truncation modulates both nucleation and extension phases of tau fibrillization FEBS Lett 580 2006 211 215
13. T.J. Cohen, J.L. Guo, D.E. Hurtado, L.K. Kwong, I.P. Mills, and J.Q. Trojanowski et al. The acetylation of tau inhibits its function and promotes pathological tau aggregation Nat Commun 2 2011 252
14. M.D. Ledesma, P. Bonay, C. Colaco, and J. Avila Analysis of microtubule-associated protein tau glycation in paired helical filaments J Biol Chem 269 1994 21614 21619
15. S.D. Yan, X. Chen, A.M. Schmidt, J. Brett, G. Godman, and Y.S. Zou et al. Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress Proc Natl Acad Sci U S A 91 1994 7787 7791
16. C.S. Arnold, G.V. Johnson, R.N. Cole, D.L. Dong, M. Lee, and G.W. Hart The microtubule-associated protein tau is extensively modified with O-linked N-acetylglucosamine J Biol Chem 271 1996 28741 28744
17. L.K. Kreppel, M.A. Blomberg, and G.W. Hart Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats J Biol Chem 272 1997 9308 9315
18. W.A. Lubas, D.W. Frank, M. Krause, and J.A. Hanover O-Linked GlcNAc transferase is a conserved nucleocytoplasmic protein containing tetratricopeptide repeats J Biol Chem 272 1997 9316 9324
19. D.L. Dong, and G.W. Hart Purification and characterization of an O-GlcNAc selective N-acetyl-beta-d-glucosaminidase from rat spleen cytosol J Biol Chem 269 1994 19321 19330
20. Y. Gao, L. Wells, F.I. Comer, G.J. Parker, and G.W. Hart Dynamic O-glycosylation of nuclear and cytosolic proteins: cloning and characterization of a neutral, cytosolic beta-N-acetylglucosaminidase from human brain J Biol Chem 276 2001 9838 9845
21. E.P. Roquemore, M.R. Chevrier, R.J. Cotter, and G.W. Hart Dynamic O-GlcNAcylation of the small heat shock protein alpha B-crystallin Biochemistry 35 1996 3578 3586
22. C. Haase, J.T. Stieler, T. Arendt, and M. Holzer Pseudophosphorylation of tau protein alters its ability for self-aggregation J Neurochem 88 2004 1509 1520
23. S. Jeganathan, A. Hascher, S. Chinnathambi, J. Biernat, E.M. Mandelkow, and E. Mandelkow Proline-directed pseudo-phosphorylation at AT8 and PHF1 epitopes induces a compaction of the paperclip folding of Tau and generates a pathological (MC-1) conformation J Biol Chem 283 2008 32066 32076
24. M. Necula, and J. Kuret Pseudophosphorylation and glycation of tau protein enhance but do not trigger fibrillization in vitro J Biol Chem 279 2004 49694 49703
25. M. Necula, and J. Kuret Site-specific pseudophosphorylation modulates the rate of tau filament dissociation FEBS Lett 579 2005 1453 1457
26. T. Lefebvre, S. Ferreira, L. Dupont-Wallois, T. Bussiere, M.J. Dupire, and A. Delacourte et al. Evidence of a balance between phosphorylation and O-GlcNAc glycosylation of Tau proteins - a role in nuclear localization Biochim Biophys Acta 1619 2003 167 176
27. F. Liu, K. Iqbal, I. Grundke-Iqbal, G.W. Hart, and C.X. Gong O-GlcNAcylation regulates phosphorylation of tau: a mechanism involved in Alzheimer's disease Proc Natl Acad Sci U S A 101 2004 10804 10809
28. L.A. Robertson, K.L. Moya, and K.C. Breen The potential role of tau protein O-glycosylation in Alzheimer's disease J Alzheimers Dis 6 2004 489 495
29. S. Marshall, V. Bacote, and R.R. Traxinger Discovery of a metabolic pathway mediating glucose-induced desensitization of the glucose transport system. Role of hexosamine biosynthesis in the induction of insulin resistance J Biol Chem 266 1991 4706 4712
30. R.P. Taylor, G.J. Parker, M.W. Hazel, Y. Soesanto, W. Fuller, and M.J. Yazzie et al. Glucose deprivation stimulates O-GlcNAc modification of proteins through up-regulation of O-linked N-acetylglucosaminyltransferase J Biol Chem 283 2008 6050 6057
31. W.D. Heiss, B. Szelies, J. Kessler, and K. Herholz Abnormalities of energy metabolism in Alzheimer's disease studied with PET Ann N Y Acad Sci 640 1991 65 71
32. S.A. Yuzwa, X. Shan, M.S. Macauley, T. Clark, Y. Skorobogatko, and K. Vosseller et al. Increasing O-GlcNAc slows neurodegeneration and stabilizes tau against aggregation Nat Chem Biol 8 2012 393 399
33. J. Lewis, E. McGowan, J. Rockwood, H. Melrose, P. Nacharaju, and M. Van Slegtenhorst et al. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein Nat Genet 25 2000 402 405
34. S.A. Yuzwa, A.K. Yadav, Y. Skorobogatko, T. Clark, K. Vosseller, and D.J. Vocadlo Mapping O-GlcNAc modification sites on tau and generation of a site-specific O-GlcNAc tau antibody Amino Acids 40 2011 857 868
35. C. Smet-Nocca, M. Broncel, J.M. Wieruszeski, C. Tokarski, X. Hanoulle, and A. Leroy et al. Identification of O-GlcNAc sites within peptides of the Tau protein and their impact on phosphorylation Mol Biosyst 7 2011 1420 1429
36. Z. Wang, N.D. Udeshi, M. O'Malley, J. Shabanowitz, D.F. Hunt, and G.W. Hart Enrichment and site mapping of O-linked N-acetylglucosamine by a combination of chemical/enzymatic tagging, photochemical cleavage, and electron transfer dissociation mass spectrometry Mol Cell Proteomics 9 2010 153 160
37. K.F. Geoghegan, H.B. Dixon, P.J. Rosner, L.R. Hoth, A.J. Lanzetti, and K.A. Borzilleri et al. Spontaneous alpha-N-6-phosphogluconoylation of a "His tag" in Escherichia coli: the cause of extra mass of 258 or 178 Da in fusion proteins Anal Biochem 267 1999 169 184
38. J.C. Aon, R.J. Caimi, A.H. Taylor, Q. Lu, F. Oluboyede, and J. Dally et al. Suppressing posttranslational gluconoylation of heterologous proteins by metabolic engineering of Escherichia coli Appl Environ Microbiol 74 2008 950 958
39. P. Du, P. Loulakis, C. Luo, A. Mistry, S.P. Simons, and P.K. LeMotte et al. Phosphorylation of serine residues in histidine-tag sequences attached to recombinant protein kinases: a cause of heterogeneity in mass and complications in function Protein Expression Purif 44 2005 121 129
40. K.M. Kim, E.C. Yi, D. Baker, and K.Y. Zhang Post-translational modification of the N-terminal His tag interferes with the crystallization of the wild-type and mutant SH3 domains from chicken src tyrosine kinase Acta Crystallogr Sect D Biol Crystallogr 57 2001 759 762
41. M.D. Weingarten, A.H. Lockwood, S.Y. Hwo, and M.W. Kirschner A protein factor essential for microtubule assembly Proc Natl Acad Sci U S A 72 1975 1858 1862
42. C.P. Winsor The Gompertz curve as a growth curve Proc Natl Acad Sci U S A 18 1932 1 8
43. P. Friedhoff, A. Schneider, E.M. Mandelkow, and E. Mandelkow Rapid assembly of Alzheimer-like paired helical filaments from microtubule-associated protein tau monitored by fluorescence in solution Biochemistry 37 1998 10223 10230
44. E. Chang, and J. Kuret Detection and quantification of tau aggregation using a membrane filter assay Anal Biochem 373 2008 330 336
45. G. Ramachandran, and J.B. Udgaonkar Evidence for the existence of a secondary pathway for fibril growth during the aggregation of Tau J Mol Biol 421 2012 296 314
46. S. Jeganathan, M. von Bergen, H. Brutlach, H.J. Steinhoff, and E. Mandelkow Global hairpin folding of tau in solution Biochemistry 45 2006 2283 2293
47. S.A. Yuzwa, M.S. Macauley, J.E. Heinonen, X. Shan, R.J. Dennis, and Y. He et al. A potent mechanism-inspired O-GlcNAcase inhibitor that blocks phosphorylation of tau in vivo Nat Chem Biol 4 2008 483 490
48. M.D. Mukrasch, S. Bibow, J. Korukottu, S. Jeganathan, J. Biernat, and C. Griesinger et al. Structural polymorphism of 441-residue tau at single residue resolution PLoS Biol 7 2009 e34
49. S. Bibow, M.D. Mukrasch, S. Chinnathambi, J. Biernat, C. Griesinger, and E. Mandelkow et al. The dynamic structure of filamentous Tau Angew Chem Int Ed 50 2011 11520 11524
50. C. Camilloni, A. De Simone, W.F. Vranken, and M. Vendruscolo Determination of secondary structure populations in disordered states of proteins using nuclear magnetic resonance chemical shifts Biochemistry 51 2012 2224 2231
51. 15N NMR spectroscopy J Biomol NMR 17 2000 239 255
52. 1H}-NOE experiment J Biomol NMR 23 2002 23 33
53. 13C chemical shift statistics J Biomol NMR 24 2002 149 154
54. E.E. Simanek, D.H. Huang, L. Pasternack, T.D. Machajewski, O. Seitz, and D.S. Millar et al. Glycosylation of threonine of the repeating unit of RNA polymerase II with β-linked N-acetylglucosame leads to a turnlike structure J Am Chem Soc 120 1998 11567 11575
55. W.G. Wu, L. Pasternack, D.H. Huang, K.M. Koeller, C.C. Lin, and O. Seitz et al. Structural study on O-glycopeptides: glycosylation-induced conformational changes of O-GlcNAc, O-LacNAc, O-sialyl-LacNAc, and O-sialyl-lewis-X peptides of the mucin domain of MAdCAM-1 J Am Chem Soc 121 1999 2409 2417
56. Y.X. Chen, J.T. Du, L.X. Zhou, X.H. Liu, Y.F. Zhao, and H. Nakanishi et al. Alternative O-GlcNAcylation/O-phosphorylation of Ser(16) induce different conformational disturbances to the N terminus of murine estrogen receptor beta Chem Biol 13 2006 937 944
57. F.C. Liang, R.P.Y. Chen, C.C. Lin, K.T. Huang, and S.I. Chan Tuning the conformation properties of a peptide by glycosylation and phosphorylation Biochem Biophys Res Commun 342 2006 482 488
58. A. Fernandez-Tejada, F. Corzana, J.H. Busto, G. Jimenez-Oses, J. Jimenez-Barbero, and A. Avenoza et al. Insights into the geometrical features underlying β-O-GlcNAc glycosylation: water pockets drastically modulate the interactions between the carbohydrate and the peptide backbone Chem Eur J 15 2009 7297 7301
59. S.S. Mallajosyula, and A.D. MacKerell Influence of solvent and intramolecular hydrogen bonding on the conformational properties of O-linked glycopeptides J Phys Chem B 115 2011 11215 11229
60. Y. Narimatsu, T. Kubota, S. Furukawa, H. Morii, H. Narimatsu, and K. Yamasaki Effect of glycosylation on cis/trans isomerization of prolines in IgA1-hinge peptide J Am Chem Soc 132 2010 5548 5549
61. B. Srikanth, M.M. Vaidya, and R.D. Kalraiya O-GlcNAcylation determines the solubility, filament organization, and stability of keratins 8 and 18 J Biol Chem 285 2010 34062 34071
62. E. Chang, S. Kim, K.N. Schafer, and J. Kuret Pseudophosphorylation of tau protein directly modulates its aggregation kinetics Biochim Biophys Acta 1814 2011 388 395
63. Q. Sun, and T.C. Gamblin Pseudohyperphosphorylation causing AD-like changes in tau has significant effects on its polymerization Biochemistry 48 2009 6002 6011
64. F. Delaglio, S. Grzesiek, G.W. Vuister, G. Zhu, J. Pfeifer, and A. Bax NMRPipe: a multidimensional spectral processing system based on Unix pipes J Biomol NMR 6 1995 277 293
65. T.D. Goddard, and D.G. Kneeler Sparky 3rd ed. 1999
66. M. Sattler, J. Schleucher, and C. Griesinger Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients Prog Nucl Magn Reson Spectrosc 34 1999 93 158
67. 15N) labeled proteins: Application to unfolded proteins J Biomol NMR 20 2001 135 147
68. 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium J Biomol NMR 4 1994 727 734
69. H. Kuboniwa, S. Grzesiek, F. Delaglio, and A. Bax Measurement of H-N-H-alpha J-couplings in calcium-free calmodulin using new 2D and 3D water-flip-back methods J Biomol NMR 4 1994 871 878