- About this Journal
- Abstracting and Indexing
- Aims and Scope
- Annual Issues
- Article Processing Charges
- Articles in Press
- Author Guidelines
- Bibliographic Information
- Citations to this Journal
- Contact Information
- Editorial Board
- Editorial Workflow
- Free eTOC Alerts
- Publication Ethics
- Reviewers Acknowledgment
- Submit a Manuscript
- Subscription Information
- Table of Contents
International Journal of Alzheimer’s Disease
Volume 2012 (2012), Article ID 578373, 7 pages
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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- F. Hernández and J. Avila, “Tau aggregates and tau pathology,” Journal of Alzheimer's Disease, vol. 14, no. 4, pp. 449–452, 2008.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- N. Spruston, “Pyramidal neurons: dendritic structure and synaptic integration,” Nature Reviews Neuroscience, vol. 9, no. 3, pp. 206–221, 2008.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- M. T. Lin and M. F. Beal, “Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases,” Nature, vol. 443, no. 7113, pp. 787–795, 2006.
- J. Avila, “Common mechanisms in neurodegeneration,” Nature Medicine, vol. 16, no. 12, p. 1372, 2010.
- 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.
- 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.