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Research Article

Targeting Post-translational Modifications on Tau as a Therapeutic Strategy for Alzheimer's Disease

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Pages 127-133 | Received 29 Aug 2011, Accepted 20 Sep 2011, Published online: 17 Nov 2011

REFERENCES

  • Adams, S. J., Crook, R. J. P., DeTure, M., Randle, S. J., Innes, A.E., Yu, X. Z., Lin, W. L., Dugger, B. N., McBride, M., Hutton, M., Dickson, D.W., & McGowan, E. (2009). Overexpression of wild-type murine tau results in progressive tauopathy and neurodegeneration. Am J Pathol, 175, 1598–1609.
  • Adams, S. J., Deture, M. A., McBride, M., Dickson, D. W., & Petrucelli, L. (2010). Three repeat isoforms of tau inhibit assembly of four repeat tau filaments. PLoS One, 25, 5(5).
  • Arnold, C. S., Johnson, G. V. W., Cole, R. N., Dong, D. L. Y., Lee, M., & Hart, G. W. (1996). The microtubule-associated protein tau is extensively modified with O-linked N-acetylglucosamine. J Biol Chem, 271, 28741–28744.
  • Braak, H., & Braak, E. (1995). Staging of Alzheimers’ disease-related neurofibrillary changes. Neurobiol Aging, 16, 271–278.
  • Braak, H., & Braak, E. (1996). Evolution of the neuropathology of Alzheimer’s disease. Acta Neurol Scand, 93, 3–12.
  • Buee, L., Bussiere, T., Buee-Scherrer, V., Delacourte, A., & Hof, P. R. (2000). Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Rev, 33, 95–130.
  • Chen, L., Wei, Y., Wang, X. Q., & He, R. Q. (2009). d-Ribosylated Tau forms globular aggregates with high cytotoxicity. Cell Mol Life Sci, 66, 2559–2571.
  • Chow, V. W., Mattson, M. P., Wong, P. C., & Gleichmann, M. (2010). An overview of APP processing enzymes and products. Neuromol Med, 12, 1–12.
  • Cohen, T. J., Guo, J. L., Hurtado, D. E., Kwong, L. K., Mills, I. P., Trojanowski, J. Q., & Lee, V. M. Y. (2011). The acetylation of tau inhibits its function and promotes pathological tau aggregation. Nat Commun, 2, 252.
  • Dias, W. B., & Hart, G. W. (2007). O-GlcNAc modification in diabetes and Alzheimer’s disease. Mol Biosys, 3, 766–772.
  • Dodart, J. C., Mathis, C., Bales, K. R., & Paul, S. M. (2002). Does my mouse have Alzheimer’s disease? Genes Brain Behav, 1, 142–155.
  • Drewes, G., Trinczek, B., Illenberger, S., Biernat, J., Schmittulms, G., Meyer, H. E., Mandelkow, E. M., & Mandelkow, E. (1995). Microtubule-associated protein microtubule affinity-regulating kinase (P110(Mark))— 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.
  • Eckermann, K., Mocanu, M. M., Khlistunova, I., Biernat, J., Nissen, A., Hofmann, A., Schonig, K., Bujard, H., Haemisch, A., Mandelkow, E., Zhou, L., Rune, G., & Mandelkow, E. M. (2007). The beta-propensity of Tau determines aggregation and synaptic loss in inducible mouse models of tauopathy. J Biol Chem, 282, 31755–31765.
  • Flament, S., Delacourte, A., Hemon, B., & Defossez, A. (1989). Direct biochemical-evidence for an abnormal phosphorylation of tau proteins during Alzheimers’ disease. Comptes Rendus Acad Sci Serie III Sci Vie Life Sci, 308, 77–82.
  • Glabe, C. G., & Kayed, R. (2006). Common structure and toxic function of amyloid oligomers implies a common mechanism of pathogenesis. Neurology, 66, S74–S78.
  • Gravina, S. A., Ho, L. B., Eckman, C. B., Long, K. E., Otvos, L., Younkin, L. H., Suzuki, N., & Younkin, S. G. (1995). Amyloid-beta protein (A-beta) in Alzheimers’ disease brain — Biochemical and immunocytochemical analysis with antibodies specific for forms ending at A-beta-40 or A-beta-42(43). J Biol Chem, 270, 7013–7016.
  • Han, I., & Kudlow, J. E. (1997). Reduced O glycosylation of Sp1 is associated with increased proteasome susceptibility. Mol Cell Biol, 17, 2550–2558.
  • Hardy, J., & Allsop, D. (1991). Amyloid deposition as the central event in the etiology of Alzheimers’ disease. Trends Pharmacol Sci, 12, 383–388.
  • Hutton, M., Lendon, C. L., Rizzu, P., Baker, M., Froelich, S., Houlden, H., Pickering-Brown, S., Chakraverty, S., Isaacs, A., Grover, A., Hackett, J., Adamson, J., Lincoln, S., Dickson, D., Davies, P., Petersen, R. C., Stevens, M., de Graaff, E., Wauters, E., van Baren, J., Hillebrand, M., Joosse, M., Kwon, J. M., Nowotny, P., Che, L. K., . (1998). Association of missense and 5’-splice-site mutations in tau with the inherited dementia FTDP-17. Nature, 393, 702–705.
  • Illenberger, S., Drewes, G., Trinczek, B., Biernat, J., Meyer, H. E., Olmsted, J. B., Mandelkow, E. M., & Mandelkow, E. (1996). Phosphorylation of microtubule-associated proteins MAP2 and MAP4 by the protein kinase p110(mark)— Phosphorylation sites and regulation of microtubule dynamics. J Biol Chem, 271, 10834–10843.
  • Ischiropoulos, H. (2003). Biological selectivity and functional aspects of protein tyrosine nitration. Biochem Biophys Res Commun, 305, 776–783.
  • Jin, M. J., Shepardson, N., Yang, T., Chen, G., Walsh, D., & Selkoe, D. J. (2011). Soluble amyloid beta-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc Natl Acad Sci U S A, 108, 5819–5824.
  • Kosik, K. S., Joachim, C. L., & Selkoe, D. J. (1986). Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc Natl Acad Sci U S A, 83, 4044–4048.
  • Lefebvre, T., Ferreira, S., Dupont-Wallois, L., Bussiere, T., Dupire, M. J., Delacourte, A., Michalski, J. C., & Caillet-Boudin, M. L. (2003). Evidence of a balance between phosphorylation and O-GlcNAc glycosylation of Tau proteins—A role in nuclear localization. Biochim Biophys Acta, 1619, 167–176.
  • Li, X., Lu, F., Wang, J. Z., & Gong, C. X. (2006). Concurrent alterations of O-GlcNAcylation and phosphorylation of tau in mouse brains during fasting. Eur J Neurosci, 23, 2078–2086.
  • Liu, F., Shi, J. H., Tanimukai, H., Gu, J. H., Gu, J. L., Grundke-Iqbal, I., Iqbal, K., & Gong, C. X. (2009). Reduced O-GlcNAcylation links lower brain glucose metabolism and tau pathology in Alzheimer’s disease. Brain, 132, 1820–1832.
  • Liu, Y., Liu, F., Grundke-Iqbal, I., Iqbal, K., & Gong, C. X. (2009). Brain glucose transporters, O-GlcNAcylation and phosphorylation of tau in diabetes and Alzheimer’s disease. J Neurochem, 111, 242–249.
  • Liu,. F, Iqbal, K., Grundke-Iqbal, I., Hart, G. W., & Gong, C. X. (2004). O-GlcNAcylation regulates phosphorylation of tau: A mechanism involved in Alzheimer’s disease. Proc Natl Acad Sci U S A, 101, 10804–10809.
  • Martin, L., Latypova, X., & Terro, F. (2011). Post-translational modifications of tau protein: Implications for Alzheimer’s disease. Neurochem Int, 58, 458–471.
  • Min, S. W., Cho, S. H., Zhou, Y.G., Schroeder, S., Haroutunian, V., Seeley, W. W., Huang, E. J., Shen, Y., Masliah, E., Mukherjee, C., Meyers, D., Cole, P. A., Ott, M., & Gan, L. (2010). Acetylation of tau inhibits its degradation and contributes to tauopathy (vol 67, pg 953, 2010). Neuron, 68, 801.
  • Mocanu, M. M., Nissen, A., Eckermann, K., Khlistunova, I., Biernat, J., Drexler, D., Petrova, O., Schonig, K., Bujard, H., Mandelkow, E., Zhou, L., Rune, G., & Mandelkow, E. M. (2008). The potential for beta-structure in the repeat domain of Tau protein determines aggregation, synaptic decay, neuronal loss, and coassembly with endogenous Tau in inducible mouse models of tauopathy. J Neurosci, 28, 737–748.
  • Qian, W., Iqbal, K., Grundke-Iqbal, I., Gong, C. X., & Liu, F. (2011). Splicing factor SC35 promotes tau expression through stabilization of its mRNA. FEBS Lett, 585, 875–880.
  • Ramsden, M., Kotilinek, L., Forster, C., Paulson, J., McGowan, E., SantaCruz, K., Guimaraes, A., Yue, M., Lewis, J., Carlson, G., Hutton, M., & Ashe, K. H. (2005). Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J Neurosci, 25, 10637–10647.
  • Reyes, J. F., Reynolds, M. R., Horowitz, P. M., Fu, Y. F., Guillozet-Bongaarts, A. L., Berry, R., & Binder, L. I. (2008). A possible link between astrocyte activation and tau nitration in Alzheimer’s disease. Neurobiol Dis, 31, 198–208.
  • Reynolds, M. R., Berry, R. W., & Binder, L. I. (2005). Site-specific nitration differentially influences tau assembly in vitro. Biochemistry, 44, 13997–4009.
  • Reynolds, M. R., Berry, R. W., & Binder, L. I. (2007). Nitration in neurodegeneration: Deciphering the “hows” “nYs”. Biochemistry, 46, 7325–7336.
  • Reynolds, M. R., Lukas, T. J., Berry, R. W., & Binder, L. I. (2006). Peroxynitrite-mediated tau modifications stabilize preformed filaments and destabilize microtubules through distinct mechanisms. Biochemistry, 45, 4314–4326.
  • Reynolds, M. R., Reyes, J. F., Fu, Y. F., Bigio, E. H., Guillozet-Bongaarts, A. L., Berry, R. W., & Binder, L. I. (2006). Tau nitration occurs at tyrosine 29 in the fibrillar lesions of Alzheimer’s disease and other tauopathies. J Neurosci, 26, 10636–10645.
  • Robertson, L. A., Moya, K. L., & Breen, K. C. (2004). The potential role of tau protein O-glycosylation in Alzheimer’s disease. J Alzheimers Dis, 6, 489–695.
  • Sasaki, N., Fukatsu, R., Tsuzuki, K., Hayashi, Y., Yoshida, T., Fujii, N., Koike, T., Wakayama, I., Yanagihara, R., Garruto, R., Amano, N., & Makita, Z. (1998). Advanced glycation end products in Alzheimer’s disease and other neurodegenerative diseases. Am J Pathol, 153, 1149–1155.
  • Sengupta, A., Kabat, J., Novak, M., Wu, Q. L., Grundke-Iqbal, I., & Iqbal, K. (1998). Phosphorylation of tau at both Thr 231 and Ser 262 is required for maximal inhibition of its binding to microtubules. Arch Biochem Biophys, 357, 299–309.
  • Simanek, E. E., Huang, D. H., Pasternack, L., Machajewski, T. D., Seitz, O., Millar, D. S., Dyson, H.J., & Wong, C. H. (1998). Glycosylation of threonine of the repeating unit of RNA polymerase II with beta-linked N-acetylglucosame leads to a turnlike structure. J Am Chem Soc 1998, 120, 11567–11575.
  • Smet-Nocca, C., Broncel, M., Wieruszeski, J. M., Tokarski, C., Hanoulle, X., Leroy, A., Landrieu, I., Rolando, C., Lippens, G., & Hackenberger, C. P. R. (2011). Identification of O-GlcNAc sites within peptides of the Tau protein and their impact on phosphorylation. Mol Biosys, 7, 1420–1429.
  • Takahashi, M., Tsujioka, Y., Yamada, T., Tsuboi, Y., Okada, H., Yamamoto, T., & Liposits, Z. (1999). Glycosylation of microtubule-associated protein tau in Alzheimer’s disease brain. Acta Neuropathol, 97, 635–641.
  • Wang, J. Z., GrundkeIqbal, I., & Iqbal, K. (1996). Glycosylation of microtubule-associated protein tau: An abnormal posttranslational modification in Alzheimer’s disease. Nat Med, 2, 871–875.
  • Wang, Z. H., Udeshi, N. D., O’Malley, M., Shabanowitz, J., Hunt, D. F., & Hart, G. W. (2010). 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.
  • Wu, W. G., Pasternack, L., Huang, D. H., Koeller, K. M., Lin, C. C., Seitz, O., & Wong, C. H. (1999). 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, 2409–2417.
  • Yu, C. H., Si, T., Wu, W. H., Hu, J., Du, J. T., Zhao, Y. F., & Li, Y. M. (2008). O-GlcNAcylation modulates the self-aggregation ability of the fourth microtubule-binding repeat of tau. Biochem Biophys Res Commun, 375, 59–62.
  • Yuzwa, S. A., Macauley, M. S., Heinonen, J. E., Shan, X. Y., Dennis, R. J., He, Y. A., Whitworth, G. E., Stubbs, K. A., McEachern, E. J., Davies, G. J., & Vocadlo, D. J. (2008). A potent mechanism-inspired O-GlcNAcase inhibitor that blocks phosphorylation of tau in vivo. Nat Chem Biol, 4, 483–490.
  • Yuzwa, S. A., Yadav, A. K., Skorobogatko, Y., Clark, T., Vosseller, K., & Vocadlo, D. J. (2011). Mapping O-GlcNAc modification sites on tau and generation of a site-specific O-GlcNAc tau antibody. Amino Acids, 40, 857–868.

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