Tau post-translational modifications in wild-type and human amyloid precursor protein transgenic mice

Nature Neuroscience

Volumn 18, Issue 8, 2015, Pages 1183-1189

  Morris, Meaghan ^a,b   Knudsen, Giselle M ^c   Maeda, Sumihiro ^a,d   Trinidad, Jonathan C ^c,e   Ioanoviciu, Alexandra ^c   Burlingame, Alma L ^c   Mucke, Lennart ^a,d  

^a GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; LYSINE; N ACETYLGLUCOSAMINE; TAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN TISSUE; CONTROLLED STUDY; HIPPOCAMPUS; HUMAN; LIMIT OF DETECTION; MASS SPECTROMETRY; MOUSE; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; UBIQUITINATION; ACETYLATION; ANIMAL; C57BL MOUSE; METABOLISM; METHYLATION; PHYSIOLOGY; TRANSGENIC MOUSE;

ACETYLATION; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; MASS SPECTROMETRY; METHYLATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; TAU PROTEINS; UBIQUITINATION;

EID: 84938421302     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4067     Document Type: Article

References (67)

1. Morris, M., Maeda, S., Vossel, K. & Mucke, L. The many faces of tau. Neuron 70, 410-426 (2011).
2. Huang, Y. & Mucke, L. Alzheimer mechanisms and therapeutic strategies. Cell 148, 1204-1222 (2012).
3. Roberson, E.D. et al. Reducing endogenous tau ameliorates amyloid beta-induced defcits in an Alzheimer's disease mouse model. Science 316, 750-754 (2007).
4. Roberson, E.D. et al. Amyloid-β/Fyn-induced synaptic, network and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer's disease. J. Neurosci. 31, 700-711 (2011).
5. Ittner, L.M. et al. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 142, 387-397 (2010).
6. Seward, M.E. et al. Amyloid-β signals through tau to drive ectopic neuronal cell cycle re-entry in Alzheimer's disease. J. Cell Sci. 126, 1278-1286 (2013).
7. Suberbielle, E. et al. Physiologic brain activity causes DNA double-strand breaks in neurons, with exacerbation by amyloid-β. Nat. Neurosci. 16, 613-621 (2013).
8. DeVos, S.L. et al. Antisense reduction of tau in adult mice protects against seizures. J. Neurosci. 33, 12887-12897 (2013).
9. Gheyara, A.L. et al. Tau reduction prevents disease in a mouse model of Dravet syndrome. Ann. Neurol. 76, 443-456 (2014).
10. Holth, J.K. et al. Tau loss attenuates neuronal network hyperexcitability in mouse and Drosophila genetic models of epilepsy. J. Neurosci. 33, 1651-1659 (2013).
11. Li, Z., Hall, A.M., Kelinske, M. & Roberson, E.D. Seizure resistance without parkinsonism in aged mice after tau reduction. Neurobiol. Aging 35, 2617-2624 (2014).
12. Zempel, H. et al. Amyloid-β oligomers induce synaptic damage via Tau-dependent microtubule severing by TTLL6 and spastin. EMBO J. 32, 2920-2937 (2013).
13. 2+ elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation and destruction of microtubules and spines. J. Neurosci. 30, 11938-11950 (2010).
14. Funk, K.E. et al. Lysine methylation is an endogenous post-translational modifcation of tau protein in human brain and a modulator of aggregation propensity. Biochem. J. 462, 77-88 (2014).
15. Guo, A. et al. Immunoaffnity enrichment and mass spectrometry analysis of protein methylation. Mol. Cell. Proteomics 13, 372-387 (2014).
16. Thomas, S.N. et al. Dual modifcation of Alzheimer's disease PHF-tau protein by lysine methylation and ubiquitylation: a mass spectrometry approach. Acta Neuropathol. 123, 105-117 (2012).
17. Liu, F., Iqbal, K., Grundke-Iqbal, I., Hart, G.W. & Gong, C.-X. O-GlcNAcylation regulates phosphorylation of tau: a mechanism involved in Alzheimer's disease. Proc. Natl. Acad. Sci. USA 101, 10804-10809 (2004).
18. Yuzwa, S.A. et al. A potent mechanism-inspired O-GlcNAcase inhibitor that blocks phosphorylation of tau in vivo. Nat. Chem. Biol. 4, 483-490 (2008).
19. Arnold, C.S. et al. The microtubule-associated protein tau is extensively modifed with O-linked N-acetylglucosamine. J. Biol. Chem. 271, 28741-28744 (1996).
20. Wang, Z. et al. 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, 153-160 (2010).
21. Hanger, D.P. et al. Novel phosphorylation sites in tau from Alzheimer brain support a role for casein kinase 1 in disease pathogenesis. J. Biol. Chem. 282, 23645-23654 (2007).
22. Cripps, D. et al. Alzheimer disease-specifc conformation of hyperphosphorylated paired helical flament-Tau is polyubiquitinated through Lys-48, Lys-11 and Lys-6 ubiquitin conjugation. J. Biol. Chem. 281, 10825-10838 (2006).
23. Morishima-Kawashima, M. et al. Ubiquitin is conjugated with amino-terminally processed tau in paired helical flaments. Neuron 10, 1151-1160 (1993).
24. Cohen, T.J. et al. The acetylation of tau inhibits its function and promotes pathological tau aggregation. Nat. Commun. 2, 252 (2011).
25. Cook, C. et al. Acetylation of the KXGS motifs in tau is a critical determinant in modulation of tau aggregation and clearance. Hum. Mol. Genet. 23, 104-116 (2014).
26. Min, S.-W. et al. Acetylation of tau inhibits its degradation and contributes to tauopathy. Neuron 67, 953-966 (2010).
27. Baker, P.R., Trinidad, J.C. & Chalkley, R.J. Modifcation site localization scoring integrated into a search engine. Mol. Cell Proteomics 10, M111.008078 (2011).
28. Beausoleil, S.A., Villén, J., Gerber, S.A., Rush, J. & Gygi, S.P. A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 24, 1285-1292 (2006).
29. Hornbeck, P.V. et al. PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifcations in man and mouse. Nucleic Acids Res. 40, D261-D270 (2012).
30. Bradshaw, R.A., Medzihradszky, K.F. & Chalkley, R.J. Protein PTMs: post-translational modifcations or pesky trouble makers? J. Mass Spectrom. 45, 1095-1097 (2010).
31. Biggar, K.K. & Li, S.S.-C. Non-histone protein methylation as a regulator of cellular signaling and function. Nat. Rev. Mol. Cell Biol. 16, 5-17 (2015).
32. Yuzwa, S.A. et al. Increasing O-GlcNAc slows neurodegeneration and stabilizes tau against aggregation. Nat. Chem. Biol. 8, 393-399 (2012).
33. Borghgraef, P. et al. Increasing brain protein O-GlcNAc-ylation mitigates breathing defects and mortality of Tau.P301L mice. PLoS ONE 8, e84442 (2013).
34. Liu, F. et al. Reduced O-GlcNAcylation links lower brain glucose metabolism and tau pathology in Alzheimer's disease. Brain 132, 1820-1832 (2009).
35. Yuzwa, S.A. et al. Mapping O-GlcNAc modifcation sites on tau and generation of a site-specifc O-GlcNAc tau antibody. Amino Acids 40, 857-868 (2011).
36. Hoover, B.R. et al. Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron 68, 1067-1081 (2010).
37. Goedert, M. & Jakes, R. Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J. 9, 4225-4230 (1990).
38. McMillan, P. et al. Tau isoform regulation is region-and cell-specifc in mouse brain. J. Comp. Neurol. 511, 788-803 (2008).
39. Yang, X.-J. & Seto, E. Lysine acetylation: codifed crosstalk with other post-translational modifcations. Mol. Cell 31, 449-461 (2008).
40. Biernat, J. & Mandelkow, E.M. The development of cell processes induced by tau protein requires phosphorylation of serine 262 and 356 in the repeat domain and is inhibited by phosphorylation in the proline-rich domains. Mol. Biol. Cell 10, 727-740 (1999).
41. Biernat, J., Gustke, N., Drewes, G., Mandelkow, E.M. & Mandelkow, E. Phosphorylation of Ser262 strongly reduces binding of tau to microtubules: distinction between PHF-like immunoreactivity and microtubule binding. Neuron 11, 153-163 (1993).
42. von Bergen, M. et al. Assembly of tau protein into Alzheimer paired helical flaments depends on a local sequence motif ((306)VQIVYK(311)) forming beta structure. Proc. Natl. Acad. Sci. USA 97, 5129-5134 (2000).
43. von Bergen, M. et al. Mutations of tau protein in frontotemporal dementia promote aggregation of paired helical flaments by enhancing local beta-structure. J. Biol. Chem. 276, 48165-48174 (2001).
44. Brandt, R., Léger, J. & Lee, G. Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J. Cell Biol. 131, 1327-1340 (1995).
45. Reynolds, C.H. et al. Phosphorylation regulates tau interactions with Src homology 3 domains of phosphatidylinositol 3-kinase, phospholipase Cgamma1, Grb2 and Src family kinases. J. Biol. Chem. 283, 18177-18186 (2008).
46. Sultan, A. et al. Nuclear tau, a key player in neuronal DNA protection. J. Biol. Chem. 286, 4566-4575 (2011).
47. Mandelkow, E.M. et al. Tau domains, phosphorylation, and interactions with microtubules. Neurobiol. Aging 16, 355-362 (1995).
48. Sturchler-Pierrat, C. et al. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc. Natl. Acad. Sci. USA 94, 13287-13292 (1997).
49. Simón, A.-M. et al. Overexpression of wild-type human APP in mice causes cognitive defcits and pathological features unrelated to Abeta levels. Neurobiol. Dis. 33, 369-378 (2009).
50. Köpke, E. et al. Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical flament pool in Alzheimer disease. J. Biol. Chem. 268, 24374-24384 (1993).
51. 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J. Neurosci. 20, 4050-4058 (2000).
52. Dawson, H.N. et al. Inhibition of neuronal maturation in primary hippocampal neurons from tau defcient mice. J. Cell Sci. 114, 1179-1187 (2001).
53. Planel, E. et al. Anesthesia leads to tau hyperphosphorylation through inhibition of phosphatase activity by hypothermia. J. Neurosci. 27, 3090-3097 (2007).
54. Ivanovova, N., Handzusova, M., Hanes, J., Kontsekova, E. & Novak, M. High-yield purifcation of fetal tau preserving its structure and phosphorylation pattern. J. Immunol. Methods 339, 17-22 (2008).
55. Morris, M. et al. Age-appropriate cognition and subtle dopamine-independent motor defcits in aged tau knockout mice. Neurobiol. Aging 34, 1523-1529 (2013).
56. Trinidad, J.C., Thalhammer, A., Specht, C.G., Schoepfer, R. & Burlingame, A.L. Phosphorylation state of postsynaptic density proteins. J. Neurochem. 92, 1306-1316 (2005).
57. Trinidad, J.C., Specht, C.G., Thalhammer, A., Schoepfer, R. & Burlingame, A.L. Comprehensive identifcation of phosphorylation sites in postsynaptic density preparations. Mol. Cell. Proteomics 5, 914-922 (2006).
58. Vossel, K.A. et al. Tau reduction prevents Aβ-induced axonal transport defcits by blocking activation of GSK3β. J. Cell Biol. 209, 419-433 (2015).
59. Chalkley, R.J., Thalhammer, A., Schoepfer, R. & Burlingame, A.L. Identifcation of protein O-GlcNAcylation sites using electron transfer dissociation mass spectrometry on native peptides. Proc. Natl. Acad. Sci. USA 106, 8894-8899 (2009).
60. Trinidad, J.C. et al. Global identifcation and characterization of both O-GlcNAcylation and phosphorylation at the murine synapse. Mol. Cell. Proteomics 11, 215-229 (2012).
61. Vosseller, K. et al. O-linked N-acetylglucosamine proteomics of postsynaptic density preparations using lectin weak affnity chromatography and mass spectrometry. Mol. Cell. Proteomics 5, 923-934 (2006).
62. Olsen, J.V. et al. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol. Cell. Proteomics 4, 2010-2021 (2005).
63. Chalkley, R.J., Baker, P.R., Medzihradszky, K.F., Lynn, A.J. & Burlingame, A.L. In-depth analysis of tandem mass spectrometry data from disparate instrument types. Mol. Cell. Proteomics 7, 2386-2398 (2008).
64. Elias, J.E. & Gygi, S.P. Target-decoy search strategy for increased confdence in large-scale protein identifcations by mass spectrometry. Nat. Methods 4, 207-214 (2007).
65. Guan, S., Price, J.C., Prusiner, S.B., Ghaemmaghami, S. & Burlingame, A.L. A data processing pipeline for mammalian proteome dynamics studies using stable isotope metabolic labeling. Mol. Cell Proteomics 10, M111.010728 (2011).
66. Rudrabhatla, P., Jaffe, H. & Pant, H.C. Direct evidence of phosphorylated neuronal intermediate flament proteins in neurofbrillary tangles (NFTs): phosphoproteomics of Alzheimer's NFTs. FASEB J. 25, 3896-3905 (2011).
67. Tavares, I.A. et al. Prostate-derived sterile 20-like kinases (PSKs/TAOKs) phosphorylate tau protein and are activated in tangle-bearing neurons in Alzheimer disease. J. Biol. Chem. 288, 15418-15429 (2013).