The relationship between truncation and phosphorylation at the C-terminus of tau protein in the paired helical filaments of Alzheimer's disease

Frontiers in Neuroscience

Volumn 9, Issue FEB, 2015, Pages

  Flores Rodríguez, Paola ^a   Ontiveros Torres, Miguel A ^a   Cárdenas Aguayo, María C ^a   Luna Arias, Juan P ^a   Meraz Ríos, Marco A ^a   Viramontes Pintos, Amparo ^a   Harrington, Charles R ^b   Wischik, Claude M ^b   Mena, Raúl ^a   Florán Garduño, Benjamin ^a   Luna Muñoz, José ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Alzheimer's disease; Neurofibrillary tangles; Neurotoxicity; PHFs; Tau oligomers; Tau protein; Truncation

Indexed keywords

ASPARTIC ACID; TAU PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN TISSUE; CARBOXY TERMINAL SEQUENCE; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MIDDLE AGED; NEUROFIBRILLARY TANGLE; NEUROPROTECTION; NEUROTOXICITY; PAIRED HELICAL FILAMENT; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; VERY ELDERLY;

EID: 84949116801     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00033     Document Type: Article

References (62)

1. Abraha, A., Ghoshal, N., Gamblin, T. C., Cryns, V., Berry, R. W., Kuret, J., et al. (2000). C-Terminal inhibition of tau assembly in vitro and in Alzheimer's disease. J. Cell Sci. 113 Pt 21, 3737-3745. Available online at: http://jcs.biologists.org/content/117/24/5721
2. Alonso, A. C., Grundke-Iqbal, I., and Iqbal, K. (1996). Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nat. Med. 2, 783-787. doi: 10.1038/nm0796-783
3. Alonso, A., Zaidi, T., Novak, M., Grundke-Iqbal, I., and Iqbal, K. (2001). Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc. Natl. Acad. Sci. U.S.A. 98, 6923-6928. doi: 10.1073/pnas.121119298
4. Arendt, T., Stieler, J., Strijkstra, A. M., Hut, R. A., Rudiger, J., Van Der Zee, E. A., et al. (2003). Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J. Neurosci. 23, 6972-6981. Available online at: http://www.jneurosci.org/content/23/18/6972
5. Augustinack, J. C., Schneider, A., Mandelkow, E. M., and Hyman, B. T. (2002). Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol. 103, 26-35. doi: 10.1007/s004010100423
6. Basurto-Islas, G., Luna-Munoz, J., Guillozet-Bongaarts, A. L., Binder, L. I., Mena, R., and Garcia-Sierra, F. (2008). Accumulation of aspartic acid421-and glutamic acid391-cleaved tau in neurofibrillary tangles correlates with progression in Alzheimer disease. J. Neuropathol. Exp. Neurol. 67, 470-483. doi: 10.1097/NEN.0b013e31817275c7
7. Berry, R. W., Abraha, A., Lagalwar, S., Lapointe, N., Gamblin, T. C., Cryns, V. L., et al. (2003). Inhibition of tau polymerization by its carboxy-terminal caspase cleavage fragment. Biochemistry 42, 8325-8331. doi: 10.1021/bi027348m
8. Binder, L. I., Frankfurter, A., and Rebhun, L. I. (1985). The distribution of tau in the mammalian central nervous system. J. Cell Biol. 101, 1371-1378. doi: 10.1083/jcb.101.4.1371
9. Bondareff, W., Wischik, C. M., Novak, M., Amos, W. B., Klug, A., and Roth, M. (1990). Molecular analysis of neurofibrillary degeneration in Alzheimer's disease. An immunohistochemical study. Am. J. Pathol. 137, 711-723.
10. Bramblett, G. T., Goedert, M., Jakes, R., Merrick, S. E., Trojanowski, J. Q., and Lee, V. M. (1993). Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10, 1089-1099. doi: 10.1016/0896-6273(93)90057-X
11. Bretteville, A., and Planel, E. (2008). Tau aggregates: toxic, inert, or protective species? J. Alzheimers Dis. 14, 431-436. Available online at: http://iospress.metapress.com/content/u728283612717902/?p=d4887e285c9f4488bb56ef7f0ab33933&pi=10
12. Buee-Scherrer, V., Condamines, O., Mourton-Gilles, C., Jakes, R., Goedert, M., Pau, B., et al. (1996). AD2, a phosphorylation-dependent monoclonal antibody directed against tau proteins found in Alzheimer's disease. Mol. Brain Res. 39, 79-88. doi: 10.1016/0169-328X(96)00003-4
13. Bussiere, T., Hof, P. R., Mailliot, C., Brown, C. D., Caillet-Boudin, M. L., Perl, D. P., et al. (1999). Phosphorylated serine422 on tau proteins is a pathological epitope found in several diseases with neurofibrillary degeneration. Acta Neuropathol. 97, 221-230. doi: 10.1007/s004010050978
14. Carmel, G., Mager, E. M., Binder, L. I., and Kuret, J. (1996). The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology. J. Biol. Chem. 271, 32789-32795. doi: 10.1074/jbc.271.51.32789
15. Castellani, R. J., Nunomura, A., Lee, H. G., Perry, G., and Smith, M. A. (2008). Phosphorylated tau: toxic, protective, or none of the above. J. Alzheimers Dis. 14, 377-383. Available online at: http://iospress.metapress.com/content/113j815w7l183677/?p=28549b94ac544bfbaf4a84338dc77961&pi=3
16. Congdon, E. E., and Duff, K. E. (2008). Is tau aggregation toxic or protective? J. Alzheimers Dis. 14, 453-457. Available online at: http://iospress.metapress.com/content/r87481658n170407/?p=d4887e285c9f4488bb56ef7f0ab33933&pi=14
17. Fasulo, L., Ugolini, G., and Cattaneo, A. (2005). Apoptotic effect of caspase-3 cleaved tau in hippocampal neurons and its potentiation by tau FTDP-mutation N279K. J. Alzheimers Dis. 7, 3-13. Available online at: http://iospress.metapress.com/content/kb88pvc7r3f6lh9q/?p=bad17d8369ff4adab62b8ee2f276c054&pi=0
18. Fasulo, L., Ugolini, G., Visintin, M., Bradbury, A., Brancolini, C., Verzillo, V., et al. (2000). The neuronal microtubule-associated protein tau is a substrate for caspase-3 and an effector of apoptosis. J. Neurochem. 75, 624-633. doi: 10.1046/j.1471-4159.2000.0750624.x
19. Fasulo, L., Visintin, M., Novak, M., and Cattaneo, A. (1998). Tau truncation in Alzheimer's disease: encompassing PHF core tau induces apoptosis ina COS cells. Alzheimers Rep. 1, 25-32.
20. Galván, M., David, J. P., Delacourte, A., Luna, J., and Mena, R. (2001). Sequence of neurofibrillary changes in aging and Alzheimer's disease: a confocal study with phospho-tau antibody, AD2. J. Alzheimers Dis. 3, 417-425. Available online at: http://iospress.metapress.com/content/ckuryq0rcnawvhe3/?p=e550743ccbe2444f9664dab061e37a72&pi=8
21. Gamblin, T. C., Berry, R. W., and Binder, L. I. (2003a). Modeling tau polymerization in vitro: a review and synthesis. Biochemistry 42, 15009-15017. doi: 10.1021/bi035722s
22. Gamblin, T. C., Berry, R. W., and Binder, L. I. (2003b). Tau polymerization: role of the amino terminus. Biochemistry 42, 2252-2257. doi: 10.1021/bi0272510
23. Gamblin, T. C., Chen, F., Zambrano, A., Abraha, A., Lagalwar, S., Guillozet, A. L., et al. (2003c). Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 100, 10032-10037. doi: 10.1073/pnas.1630428100
24. Garcia-Sierra, F., Ghoshal, N., Quinn, B., Berry, R. W., and Binder, L. I. (2003). Conformational changes and truncation of tau protein during tangle evolution in Alzheimer's disease. J. Alzheimers Dis. 5, 65-77. Available online at: http://iospress.metapress.com/content/m7ka6gvpnuecmnen/?p=6253aa9c54de4167ab966562d0f7b858&pi=0
25. Garcia-Sierra, F., Mondragon-Rodriguez, S., and Basurto-Islas, G. (2008). Truncation of tau protein and its pathological significance in Alzheimer's disease. J. Alzheimers Dis. 14, 401-409. Available online at: http://iospress.metapress.com/content/u067t3140870nh36/?p=61ba08d2baaa4e9d883be4a6be165217&pi=6
26. Goedert, M., Spillantini, M. G., Cairns, N. J., and Crowther, R. A. (1992). Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8, 159-168. doi: 10.1016/0896-6273(92)90117-V
27. Goedert, M., Jakes, R., Crowther, R.A., Six, J., Lübke, U., Vandermeeren, M., et al. (1993). The abnormal phosphorylation of tau protein at Ser-202 in Alzheimer's disease recapitulates phosphorylation during development. Proc. Natl. Acad. Sci. U.S.A. 90, 5066-5070.
28. Guillozet-Bongaarts, A. L., Cahill, M. E., Cryns, V. L., Reynolds, M. R., Berry, R. W., and Binder, L. I. (2006). Pseudophosphorylation of tau at serine 422 inhibits caspase cleavage: in vitro evidence and implications for tangle formation in vivo. J. Neurochem. 97, 1005-1014. doi: 10.1111/j.1471-4159.2006.03784.x
29. Guillozet-Bongaarts, A. L., Garcia-Sierra, F., Reynolds, M. R., Horowitz, P. M., Fu, Y., Wang, T., et al. (2005). Tau truncation during neurofibrillary tangle evolution in Alzheimer's disease. Neurobiol. Aging 26, 1015-1022. doi: 10.1016/j.neurobiolaging.2004.09.019
30. Horowitz, P. M., Lapointe, N., Guillozet-Bongaarts, A. L., Berry, R. W., and Binder, L. I. (2006). N-terminal fragments of tau inhibit full-length tau polymerization in vitro. Biochemistry 45, 12859-12866. doi: 10.1021/bi061325g
31. Jicha, G. A., Berenfeld, B., and Davies, P. (1999a). Sequence requirements for formation of conformational variants of tau similar to those found in Alzheimer's disease. J. Neurosci. Res. 55, 713-723. doi: 10.1002/(SICI)1097-4547(19990315)55:6<713::AID-JNR6>3.0.CO;2-G
32. Jicha, G. A., Bowser, R., Kazam, I. G., and Davies, P. (1997a). Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau. J. Neurosci. Res. 48, 128-132. doi: 10.1002/(SICI)1097-4547(19970415)48:2<128::AID-JNR5>3.0.CO;2-E
33. Jicha, G. A., Lane, E., Vincent, I., Otvos, L. Jr., Hoffmann, R., and Davies, P. (1997b). A conformation- and phosphorylation-dependent antibody recognizing the paired helical filaments of Alzheimer's disease. J. Neurochem. 69, 2087-2095. doi: 10.1046/j.1471-4159.1997.69052087.x
34. Jicha, G. A., Weaver, C., Lane, E., Vianna, C., Kress, Y., Rockwood, J., et al. (1999b). cAMP-dependent protein kinase phosphorylations on tau in Alzheimer's disease. J. Neurosci. 19, 7486-7494. Available online at: http://www.jneurosci.org/content/19/17/7486.short?sid=3ff20a88-41ff-40ba-a7af-f667ff106765
35. Liu, F., Iqbal, K., Grundke-Iqbal, I., Rossie, S., and Gong, C. X. (2005). Dephosphorylation of tau by protein phosphatase 5: impairment in Alzheimer's disease. J. Biol. Chem. 280, 1790-1796. doi: 10.1074/jbc. M410775200
36. Luna-Munoz, J., Chavez-Macias, L., Garcia-Sierra, F., and Mena, R. (2007). Earliest stages of tau conformational changes are related to the appearance of a sequence of specific phospho-dependent tau epitopes in Alzheimer's disease. J. Alzheimers Dis. 12, 365-375. Available online at: http://iospress.metapress.com/content/r74v1l5715887357/?p=3f66ae7ae0e145e7a39b2044edd44e43&pi=9
37. Luna-Munoz, J., Garcia-Sierra, F., Falcon, V., Menendez, I., Chavez-Macias, L., and Mena, R. (2005). Regional conformational change involving phosphorylation of tau protein at the Thr231, precedes the structural change detected by Alz-50 antibody in Alzheimer's disease. J. Alzheimers Dis. 8, 29-41. Available online at: http://iospress.metapress.com/content/f4m881fy7pf162qh/?p=0b54107997ae492a8414e820915b4f02&pi=3
38. McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., and Stadlan, E. M. (1984). Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA work group under the auspices of department of health and human services task force on Alzheimer's disease. Neurology 34, 939-944. doi: 10.1212/WNL.34.7.939
39. Mena, R., and Luna-muñoz, J. (2009). "Stages of pathological tau-protein processing in Alzheimer's disease: from soluble aggregation to polymetization into insoluble tau-PHFs," in Currents Hypotheses and Research Milestones, eds R. B. Maccioni and G. Perry (Busines) 79-91.
40. Mena, R., Edwards, P. C., Harrington, C. R., Mukaetova-Ladinska, E. B., and Wischik, C. M. (1996). Staging the pathological assembly of truncated tau protein into paired helical filaments in Alzheimer's disease. Acta Neuropathol. 91, 633-641. doi: 10.1007/s004010050477
41. Mena, R., Edwards, P., Perez-Olvera, O., and Wischik, C. M. (1995). Monitoring pathological assembly of tau and beta-amyloid proteins in Alzheimer's disease. Acta Neuropathol. 89, 50-56. doi: 10.1007/BF00294259
42. Mena, R., Wischik, C. M., Novak, M., Milstein, C., and Cuello, A. C. (1991). A progressive deposition of paired helical filaments (PHF) in the brain characterizes the evolution of dementia in Alzheimer's disease. An immunocytochemical study with a monoclonal antibody against the PHF core. J. Neuropathol. Exp. Neurol. 50, 474-490. doi: 10.1097/00005072-199107000-00008
43. Mondragon-Rodriguez, S., Basurto-Islas, G., Santa-Maria, I., Mena, R., Binder, L. I., Avila, J., et al. (2008). Cleavage and conformational changes of tau protein follow phosphorylation during Alzheimer's disease. Int. J. Exp. Pathol. 89, 81-90. doi: 10.1111/j.1365-2613.2007.00568.x
44. Morsch, R., Simon, W., and Coleman, P. D. (1999). Neurons may live for decades with neurofibrillary tangles. J. Neuropathol. Exp. Neurol. 58, 188-197. doi: 10.1097/00005072-199902000-00008
45. Novak, M. (1994). Truncated tau protein as a new marker for Alzheimer's disease. Acta Virol. 38, 173-189.
46. Novak, M., Kabat, J., and Wischik, C. M. (1993). Molecular characterization of the minimal protease resistant tau unit of the Alzheimer's disease paired helical filament. EMBO J. 12, 365-370.
47. Nunomura, A., Takeda, A., Moreira, P. I., Castellanir, J., Hyoung-Gon, L., Zhu, X., et al. (2009). "Neurofibrillary tangle formation as a protective response to oxidative stress in Alzheimer's disease," in Current Hypotheses and Reseach Milestones in Alzheimer's Disease, eds G. P. Ricardo and B. Maccioni (Miami, FL: Springer), 103-124.
48. Preuss, U., Doring, F., Illenberger, S., and Mandelkow, E. M. (1995). Cell cycle-dependent phosphorylation and microtubule binding of tau protein stably transfected into Chinese hamster ovary cells. Mol. Biol. Cell 6, 1397-1410. doi: 10.1091/mbc.6.10.1397
49. Rissman, R. A., Poon, W. W., Blurton-Jones, M., Oddo, S., Torp, R., Vitek, M. P., et al. (2004). Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J. Clin. Invest. 114, 121-130. doi: 10.1172/JCI20640
50. Schneider, A., Biernat, J., Von Bergen, M., Mandelkow, E., and Mandelkow, E. M. (1999). Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments. Biochemistry 38, 3549-3558. doi: 10.1021/bi981874p
51. Stieler, J. T., Bullmann, T., Kohl, F., Barnes, B. M., and Arendt, T. (2009). PHF-like tau phosphorylation in mammalian hibernation is not associated with p25-formation. J. Neural Transm. 116, 345-350. doi: 10.1007/s00702-008-0181-x
52. Stieler, J. T., Bullmann, T., Kohl, F., Toien, O., Bruckner, M. K., Hartig, W., et al. (2011). The physiological link between metabolic rate depression and tau phosphorylation in mammalian hibernation. PLoS ONE 6:e14530. doi: 10.1371/journal.pone.0014530
53. Su, B., Wang, X., Drew, K. L., Perry, G., Smith, M. A., and Zhu, X. (2008). Physiological regulation of tau phosphorylation during hibernation. J. Neurochem. 105, 2098-2108. doi: 10.1111/j.1471-4159.2008.05294.x
54. Uchihara, T., Nakamura, A., Yamazaki, M., and Mori, O. (2001). Evolution from pretangle neurons to neurofibrillary tangles monitored by thiazin red combined with Gallyas method and double immunofluorescence. Acta Neuropathol. 101, 535-539. doi: 10.1007/s004010000306
55. Wang, J. Z., and Liu, F. (2008). Microtubule-associated protein tau in development, degeneration and protection of neurons. Prog. Neurobiol. 85, 148-175. doi: 10.1016/j.pneurobio.2008.03.002
56. Weaver, C. L., Espinoza, M., Kress, Y., and Davies, P. (2000). Conformational change as one of the earliest alterations of tau in Alzheimer's disease. Neurobiol. Aging 21, 719-727. doi: 10.1016/S0197-4580(00)00157-3
57. Wischik, C. M., Edwards, P. C., Lai, R. Y., Gertz, H. N., Xuereb, J. H., Paykel, E. S., et al. (1995). Quantitative analysis of tau protein in paired helical filament preparations: implications for the role of tau protein phosphorylation in PHF assembly in Alzheimer's disease. Neurobiol. Aging 16, 409-417. Discussion: 418-431. doi: 10.1016/0197-4580(95)97327-D
58. Wischik, C. M., Edwards, P. C., Lai, R. Y., Roth, M., and Harrington, C. R. (1996). Selective inhibition of Alzheimer disease-like tau aggregation by phenothiazines. Proc. Natl. Acad. Sci. U.S.A. 93, 11213-11218. doi: 10.1073/pnas.93.20.11213
59. Wischik, C. M., Novak, M., Edwards, P. C., Klug, A., Tichelaar, W., and Crowther, R. A. (1988a). Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 85, 4884-4888.
60. Wischik, C. M., Novak, M., Thøgersen, H. C., Edwards, P. C., Runswick, M. J., Jakes, R., et al. (1988b). Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 85, 4506-4510.
61. Zhang, Y., Tian, Q., Zhang, Q., Zhou, X., Liu, S., and Wang, J. Z. (2009). Hyperphosphorylation of microtubule-associated tau protein plays dual role in neurodegeneration and neuroprotection. Pathophysiology 16, 311-316. doi: 10.1016/j.pathophys.2009.02.003
62. Zilkova, M., Zilka, N., Kovac, A., Kovacech, B., Skrabana, R., Skrabanova, M., et al. (2011). Hyperphosphorylated truncated protein tau induces caspase-3 independent apoptosis-like pathway in the Alzheimer's disease cellular model. J. Alzheimers Dis. 23, 161-169. doi: 10.3233/JAD-2010-101434