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International Journal of Alzheimer’s Disease
Volume 2012 (2012), Article ID 578373, 7 pages
http://dx.doi.org/10.1155/2012/578373
Review Article

Tau Phosphorylation by GSK3 in Different Conditions

1Centro de Biologia Molecular “Severo Ochoa” (CSIC-UAM), Nicolás Cabrera 1, Campus Cantoblanco UAM, 28049 Madrid, Spain
2Centro de Investigación Biomédica en Red de Enfermedades neurodegenerativas (CIBERNED), 28031 Madrid, Spain
3Instituto Cajal, Consejo Superior de Investigaciones Científicas, 28002 Madrid, Spain
4Laboratorio Cajal de Circuitos Corticales, Centro de Tecnología Biomédica, Universidad Politécnica de Madrid, 28223 Madrid, Spain

Received 17 January 2012; Accepted 15 March 2012

Academic Editor: Hanna Rosenmann

Copyright © 2012 Jesús Avila et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. D. Weingarten, A. H. Lockwood, S. Y. Hwo, and M. W. Kirschner, “A protein factor essential for microtubule assembly,” Proceedings of the National Academy of Sciences of the United States of America, vol. 72, no. 5, pp. 1858–1862, 1975. View at Scopus
  2. A. Himmler, D. Drechsel, M. W. Kirschner, and D. W. Martin, “Tau consists of a set of proteins with repeated C-terminal microtubule-binding domains and variable N-terminal domains,” Molecular and Cellular Biology, vol. 9, no. 4, pp. 1381–1388, 1989. View at Scopus
  3. J. G. De Ancos, I. Correas, and J. Avila, “Differences in microtubule binding and self-association abilities of bovine brain tau isoforms,” Journal of Biological Chemistry, vol. 268, no. 11, pp. 7976–7982, 1993. View at Scopus
  4. M. Goedert, M. G. Spillantini, M. C. Potier, J. Ulrich, and R. A. Crowther, “Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain,” The EMBO Journal, vol. 8, no. 2, pp. 393–399, 1989. View at Scopus
  5. R. Brandt, J. Léger, and G. Lee, “Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain,” Journal of Cell Biology, vol. 131, no. 5, pp. 1327–1340, 1995. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Arrasate, M. Pérez, and J. Avila, “Tau dephosphorylation at Tau-1 site correlates with its association to cell membrane,” Neurochemical Research, vol. 25, no. 1, pp. 43–50, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. G. Lee, N. Cowan, and M. Kirschner, “The primary structure and heterogeneity of tau protein from mouse brain,” Science, vol. 239, no. 4837, pp. 285–288, 1988. View at Scopus
  8. X. Li, Y. Kumar, H. Zempel, E. M. Mandelkow, J. Biernat, and E. Mandelkow, “Novel diffusion barrier for axonal retention of Tau in neurons and its failure in neurodegeneration,” The EMBO Journal, vol. 30, pp. 4825–4837, 2011.
  9. L. M. Ittner, Y. D. Ke, F. Delerue et al., “Dendritic function of tau mediates amyloid-β toxicity in alzheimer's disease mouse models,” Cell, vol. 142, no. 3, pp. 387–397, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. M. W. Salter and L. V. Kalia, “SRC kinases: a hub for NMDA receptor regulation,” Nature Reviews Neuroscience, vol. 5, no. 4, pp. 317–328, 2004. View at Scopus
  11. J. Avila, J. J. Lucas, M. Perez, and F. Hernandez, “Role of tau protein in both physiological and pathological conditions,” Physiological Reviews, vol. 84, pp. 361–384, 2004.
  12. D. P. Hanger, B. H. Anderton, and W. Noble, “Tau phosphorylation: the therapeutic challenge for neurodegenerative disease,” Trends in Molecular Medicine, vol. 15, no. 3, pp. 112–119, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Frame and P. Cohen, “GSK3 takes centre stage more than 20 years after its discovery,” Biochemical Journal, vol. 359, no. 1, pp. 1–16, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. F. Hernandez, E. Gomez de Barreda, A. Fuster-Matanzo, J. J. Lucas, and J. Avila, “GSK3: a possible link between beta amyloid peptide and tau protein,” Experimental Neurology, vol. 223, pp. 322–325, 2010.
  15. F. Hernández, E. G. D. Barreda, A. Fuster-Matanzo, P. Goñi-Oliver, J. J. Lucas, and J. Avila, “The role of GSK3 in Alzheimer disease,” Brain Research Bulletin, vol. 80, no. 4-5, pp. 248–250, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. M. H. Magdesian, M. M. V. F. Carvalho, F. A. Mendes et al., “Amyloid-β binds to the extracellular cysteine-rich domain of frizzled and inhibits Wnt/β-catenin signaling,” Journal of Biological Chemistry, vol. 283, no. 14, pp. 9359–9368, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Townsend, T. Mehta, and D. J. Selkoe, “Soluble Aβ inhibits specific signal transduction cascades common to the insulin receptor pathway,” Journal of Biological Chemistry, vol. 282, no. 46, pp. 33305–33312, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Baki, J. Shioi, P. Wen et al., “PS1 activates PI3K thus inhibiting GSK-3 activity and tau overphosphorylation: effects of FAD mutations,” The EMBO Journal, vol. 23, no. 13, pp. 2586–2596, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Cedazo-Mínguez, B. O. Popescu, J. M. Blanco-Millán et al., “Apolipoprotein E and β-amyloid (1-42) regulation of glycogen synthase kinase-3β,” Journal of Neurochemistry, vol. 87, no. 5, pp. 1152–1164, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. B. A. J. Schaffer, L. Bertram, B. L. Miller et al., “Association of GSK3B with Alzheimer disease and frontotemporal dementia,” Archives of Neurology, vol. 65, no. 10, pp. 1368–1374, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. J. J. Pei, E. Braak, H. Braak et al., “Distribution of active glycogen synthase kinase 3beta (GSK-3beta) in brains staged for Alzheimer disease neurofibrillary changes,” Journal of Neuropathology & Experimental Neurology, vol. 58, pp. 1010–1019, 1999.
  22. U. Wagner, M. Utton, J. M. Gallo, and C. C. J. Miller, “Cellular phosphorylation of tau by GSK-3β influences tau binding to microtubules and microtubule organisation,” Journal of Cell Science, vol. 109, no. 6, pp. 1537–1543, 1996. View at Scopus
  23. A. D. C. Alonso, I. Grundke-Iqbal, H. S. Barra, and K. Iqbal, “Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: sequestration of microtubule-associated proteins 1 and 2 and the disassembly of microtubules by the abnormal tau,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 1, pp. 298–303, 1997. View at Scopus
  24. P. J. Lu, G. Wulf, X. Z. Zhou, P. Davies, and K. P. Lu, “The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein,” Nature, vol. 399, no. 6738, pp. 784–788, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. S. L. Ma, L. Pastorino, X. Z. Zhou, and K. P. Lu, “Prolyl isomerase Pin1 promotes amyloid precursor protein (APP) turnover by inhibiting glycogen synthase kinase-3beta (GSK3beta) activity: novel mechanism for Pin1 to protect against alzheimer disease,” The Journal of Biological Chemistry, vol. 287, pp. 6969–6973, 2012.
  26. L. Pastorino, A. Sun, P. J. Lu et al., “The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-β production,” Nature, vol. 440, no. 7083, pp. 528–534, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. C. J. Phiel, C. A. Wilson, V. M. Y. Lee, and P. S. Klein, “GSK-3α regulates production of Alzheimer's disease amyloid-β peptides,” Nature, vol. 423, no. 6938, pp. 435–439, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. R. J. Castellani, A. Nunomura, H. G. Lee, G. Perry, and M. A. Smith, “Phosphorylated tau: toxic, protective, or none of the above,” Journal of Alzheimer's Disease, vol. 14, no. 4, pp. 377–383, 2008. View at Scopus
  29. S. Chatterjee, T. K. Sang, G. M. Lawless, and G. R. Jackson, “Dissociation of tau toxicity and phosphorylation: role of GSK-3β, MARK and Cdk5 in a Drosophila model,” Human Molecular Genetics, vol. 18, no. 1, pp. 164–177, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Talmat-Amar, Y. Arribat, C. Redt-Clouet et al., “Important neuronal toxicity of microtubule-bound Tau in vivo in Drosophila,” Human Molecular Genetics, vol. 20, pp. 3738–3745, 2011.
  31. C. Andorfer, C. M. Acker, Y. Kress, P. R. Hof, K. Duff, and P. Davies, “Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms,” Journal of Neuroscience, vol. 25, no. 22, pp. 5446–5454, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Reifert, D. Hartung-Cranston, and S. C. Feinstein, “Amyloid β-mediated cell death of cultured hippocampal neurons reveals extensive Tau fragmentation without increased full-length Tau phosphorylation,” Journal of Biological Chemistry, vol. 286, no. 23, pp. 20797–20811, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Aarden, S. R. Ruuls, and G. Wolbink, “Immunogenicity of anti-tumor necrosis factor antibodies-toward improved methods of anti-antibody measurement,” Current Opinion in Immunology, vol. 20, no. 4, pp. 431–435, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Hernández and J. Avila, “Tau aggregates and tau pathology,” Journal of Alzheimer's Disease, vol. 14, no. 4, pp. 449–452, 2008. View at Scopus
  35. C. A. Lasagna-Reeves, D. L. Castillo-Carranza, M. J. Guerrero-Muñoz, G. R. Jackson, and R. Kayed, “Preparation and characterization of neurotoxic tau oligomers,” Biochemistry, vol. 49, no. 47, pp. 10039–10041, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Perez, F. Hernandez, F. Lim, J. Diaz-Nido, and J. Avila, “Chronic lithium treatment decreases mutant tau protein aggregation in a transgenic mouse model,” Journal of Alzheimer's Disease, vol. 5, pp. 301–308, 2003.
  37. W. Noble, E. Planel, C. Zehr et al., “Inhibition of glycogen synthase kinase-3 by lithium correlates with reduced tauopathy and degeneration in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 19, pp. 6990–6995, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Oddo, V. Vasilevko, A. Caccamo, M. Kitazawa, D. H. Cribbs, and F. M. LaFerla, “Reduction of soluble Aβ and tau, but not soluble Aβ alone, ameliorates cognitive decline in transgenic mice with plaques and tangles,” Journal of Biological Chemistry, vol. 281, no. 51, pp. 39413–39423, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Santacruz, J. Lewis, T. Spires et al., “Medicine: Tau suppression in a neurodegenerative mouse model improves memory function,” Science, vol. 309, no. 5733, pp. 476–481, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Saman, W. Kim, M. Raya, et al., “Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid (CSF) in early Alzheimer's Disease,” The Journal of Biological Chemistry, vol. 287, no. 6, pp. 3842–3849, 2012.
  41. D. Simon, E. Garcia-Garcia, F. Royo, J. M. Falcon-Perez, and J. Avila, “Proteostasis of tau. Tau overexpression results in its secretion via membrane vesicles,” The FEBS Letter, vol. 586, pp. 47–54, 2012.
  42. G. V. W. Johnson, R. S. Jope, and L. I. Binder, “Proteolysis of tau by calpain,” Biochemical and Biophysical Research Communications, vol. 163, no. 3, pp. 1505–1511, 1989. View at Scopus
  43. F. Zhou, X. Zhu, R. J. Castellani et al., “Hibernation, a model of neuroprotection,” American Journal of Pathology, vol. 158, no. 6, pp. 2145–2151, 2001. View at Scopus
  44. Y. Tamura, M. Monden, M. Shintani, A. Kawai, and H. Shiomi, “Neuroprotective effects of hibernation-regulating substances against low-temperature-induced cell death in cultured hamster hippocampal neurons,” Brain Research, vol. 1108, no. 1, pp. 107–116, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Ittner, Y. D. Ke, J. Van Eersel, A. Gladbach, J. Götz, and L. M. Ittner, “Brief update on different roles of tau in neurodegeneration,” IUBMB Life, vol. 63, no. 7, pp. 495–502, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. H. Moreno, S. Choi, E. Yu et al., “Blocking effects of human Tau on squid giant synapse transmission and its prevention by T-817 MA,” Frontiers in Synaptic Neuroscience, vol. 3, article 3, 2011.
  47. B. R. Hoover, M. N. Reed, J. Su et al., “Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration,” Neuron, vol. 68, no. 6, pp. 1067–1081, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Avila, E. Gómez De Barreda, T. Engel, J. J. Lucas, and F. Hernández, “Tau phosphorylation in hippocampus results in toxic gain-of-function,” Biochemical Society Transactions, vol. 38, no. 4, pp. 977–980, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. E. G. de Barreda, M. Pérez, P. G. Ramos et al., “Tau-knockout mice show reduced GSK3-induced hippocampal degeneration and learning deficits,” Neurobiology of Disease, vol. 37, no. 3, pp. 622–629, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. A. M. Pooler and D. P. Hanger, “Functional implications of the association of tau with the plasma membrane,” Biochemical Society Transactions, vol. 38, no. 4, pp. 1012–1015, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. A. M. Pooler, A. Usardi, C. J. Evans, K. L. Philpott, W. Noble, and D. P. Hanger, “Dynamic association of tau with neuronal membranes is regulated by phosphorylation,” Neurobiology of Aging, vol. 33, no. 2, pp. 431.e27–431.e38, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Fath, J. Eidenmüller, and R. Brandt, “Tau-mediated cytotoxicity in a pseudohyperphosphorylation model of Alzheimer's disease,” Journal of Neuroscience, vol. 22, no. 22, pp. 9733–9741, 2002. View at Scopus
  53. A. D. Alonso, J. Di Clerico, B. Li et al., “Phosphorylation of Tau at Thr212, Thr231, and Ser262 combined causes neurodegeneration,” Journal of Biological Chemistry, vol. 285, no. 40, pp. 30851–30860, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Del, I. Grundke-Iqbal, and K. Iqbal, “Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules,” Nature Medicine, vol. 2, no. 7, pp. 783–787, 1996. View at Publisher · View at Google Scholar · View at Scopus
  55. L. Glodzik, Santi S. de, W. H. Tsui, et al., “Phosphorylated tau 231, memory decline and medial temporal atrophy in normal elders,” Neurobiology of Aging, vol. 32, pp. 2131–2141, 2011.
  56. S. Jeganathan, M. Von Bergen, H. Brutlach, H. J. Steinhoff, and E. Mandelkow, “Global hairpin folding of tau in solution,” Biochemistry, vol. 45, no. 7, pp. 2283–2293, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. 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,” Journal of Biological Chemistry, vol. 283, no. 46, pp. 32066–32076, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. E. Braak, H. Braaak, and E. M. Mandelkow, “A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads,” Acta Neuropathologica, vol. 87, no. 6, pp. 554–567, 1994. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Mercken, M. Vandermeeren, U. Lubke et al., “Monoclonal antibodies with selective specificity for Alzheimer Tau are directed against phosphatase-sensitive epitopes,” Acta Neuropathologica, vol. 84, no. 3, pp. 265–272, 1992. View at Scopus
  60. L. Otvos Jr., L. Feiner, E. Lang, G. I. Szendrei, M. Goedert, and V. M. Y. Lee, “Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404,” Journal of Neuroscience Research, vol. 39, no. 6, pp. 669–673, 1994. View at Publisher · View at Google Scholar · View at Scopus
  61. F. Hernández, J. J. Lucas, R. Cuadros, and J. Avila, “GSK-3 dependent phosphoepitopes recognized by PHF-1 and AT-8 antibodies are present in different tau isoforms,” Neurobiology of Aging, vol. 24, no. 8, pp. 1087–1094, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Delacourte, J. P. David, N. Sergeant et al., “The biochemical pathway of neurofibrillary degeneration in aging and Alzheimer's disease,” Neurology, vol. 52, no. 6, pp. 1158–1165, 1999. View at Scopus
  63. L. Blazquez-Llorca, V. Garcia-Marin, P. Merino-Serrais, J. Avila, and J. Defelipe, “Abnormal Tau phosphorylation in the thorny excrescences of CA3 hippocampal neurons in patients with Alzheimer's disease,” Journal of Alzheimer's Disease, vol. 26, pp. 683–698, 2011.
  64. N. Spruston, “Pyramidal neurons: dendritic structure and synaptic integration,” Nature Reviews Neuroscience, vol. 9, no. 3, pp. 206–221, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. D. F. Swaab, E. J. G. Dubelaar, M. A. Hofman, E. J. A. Scherder, E. J. W. Van Someren, and R. W. H. Verwer, “Brain aging and Alzheimer's disease; use it or lose it,” Progress in Brain Research, vol. 138, pp. 343–373, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. E. Planel, T. Miyasaka, T. Launey et al., “Alterations in glucose metabolism induce hypothermia leading to Tau hyperphosphorylation through differential inhibition of kinase and phosphatase activities: implications for Alzheimer's disease,” Journal of Neuroscience, vol. 24, no. 10, pp. 2401–2411, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. T. Arendt, J. Stieler, A. M. Strijkstra et al., “Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals,” Journal of Neuroscience, vol. 23, no. 18, pp. 6972–6981, 2003. View at Scopus
  68. W. Härtig, J. Stieler, A. S. Boerema et al., “Hibernation model of tau phosphorylation in hamsters: selective vulnerability of cholinergic basal forebrain neurons—implications for Alzheimer's disease,” European Journal of Neuroscience, vol. 25, no. 1, pp. 69–80, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. M. Oklejewicz, S. Daan, and A. M. Strijkstra, “Temporal organisation of hibernation in wild-type and tau mutant Syrian hamsters,” Journal of Comparative Physiology, vol. 171, no. 5, pp. 431–439, 2001. View at Publisher · View at Google Scholar · View at Scopus
  70. W. Härtig, M. Oklejewicz, A. M. Strijkstra, A. S. Boerema, J. Stieler, and T. Arendt, “Phosphorylation of the tau protein sequence 199-205 in the hippocampal CA3 region of Syrian hamsters in adulthood and during aging,” Brain Research, vol. 1056, no. 1, pp. 100–104, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. C. G. Von Der Ohe, C. Darian-Smith, C. C. Garner, and H. C. Heller, “Ubiquitous and temperature-dependent neural plasticity in hibernators,” Journal of Neuroscience, vol. 26, no. 41, pp. 10590–10598, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. A. S. I. Loudon, Q. J. Meng, E. S. Maywood, D. A. Bechtold, R. P. Boot-Handford, and M. H. Hastings, “The biology of the circadian CK1ε tau mutation in mice and Syrian hamsters: a tale of two species,” Cold Spring Harbor Symposia on Quantitative Biology, vol. 72, pp. 261–271, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. Q. J. Meng, E. S. Maywood, D. A. Bechtold et al., “Entrainment of disrupted circadian behavior through inhibition of casein kinase 1 (CK1) enzymes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 34, pp. 15240–15245, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Fotuhi, V. Hachinski, and P. J. Whitehouse, “Changing perspectives regarding late-life dementia,” Nature Reviews Neurology, vol. 5, no. 12, pp. 649–658, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. F. Benedetti, A. Serretti, C. Colombo, C. Lorenzi, V. Tubazio, and E. Smeraldi, “A glycogen synthase kinase 3-β promoter gene single nucleotide polymorphism is associated with age at onset and response to total sleep deprivation in bipolar depression,” Neuroscience Letters, vol. 368, no. 2, pp. 123–126, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. B. Su, X. Wang, K. L. Drew, G. Perry, M. A. Smith, and X. Zhu, “Physiological regulation of tau phosphorylation during hibernation,” Journal of Neurochemistry, vol. 105, no. 6, pp. 2098–2108, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. V. Srinivasan, D. W. Spence, S. R. Pandi-Perumal, G. M. Brown, and D. P. Cardinali, “Melatonin in mitochondrial dysfunction and related disorders,” International Journal of Alzheimer's Disease, vol. 2011, Article ID 326320, 16 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. E. Planel, K. E. G. Richter, C. E. Nolan et al., “Anesthesia leads to tau hyperphosphorylation through inhibition of phosphatase activity by hypothermia,” Journal of Neuroscience, vol. 27, no. 12, pp. 3090–3097, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. M. T. Lin and M. F. Beal, “Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases,” Nature, vol. 443, no. 7113, pp. 787–795, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. J. Avila, “Common mechanisms in neurodegeneration,” Nature Medicine, vol. 16, no. 12, p. 1372, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. M. D. Ledesma, P. Bonay, C. Colaco, and J. Avila, “Analysis of microtubule-associated protein tau glycation in paired helical filaments,” Journal of Biological Chemistry, vol. 269, no. 34, pp. 21614–21619, 1994. View at Scopus
  82. S. G. de Arriba, G. Stuchbury, J. Yarin, J. Burnell, C. Loske, and G. Münch, “Methylglyoxal impairs glucose metabolism and leads to energy depletion in neuronal cells-protection by carbonyl scavengers,” Neurobiology of Aging, vol. 28, no. 7, pp. 1044–1050, 2007. View at Publisher · View at Google Scholar · View at Scopus