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Prion-Like Properties of Assembled Tau Protein

  • Florence Clavaguera
  • Markus Tolnay
  • Michel GoedertEmail author
Chapter
Part of the Research and Perspectives in Alzheimer's Disease book series (ALZHEIMER)

Abstract

The soluble microtubule-associated protein tau becomes hyperphosphorylated, insoluble and filamentous in a number of neurodegenerative diseases collectively referred to as tauopathies. In Alzheimer’s disease (AD), tau pathology develops in a stereotypical manner, with the first lesions appearing in the locus coeruleus and the transentorhinal cortex, from where they appear to spread to the entorhinal cortex, the hippocampus and the neocortex. The staging of tau pathology has also been described in argyrophilic grain disease (AGD), where tau lesions spread stereotypically throughout the limbic system. The isoform composition and morphology of tau filaments differ between diseases, suggesting the possible existence of different tau strains, reminiscent of prion strains. Prion diseases result from the misfolding of the cellular prion protein that can occur sporadically, as the result of dominantly inherited mutations or following infection. Recent experimental work has shown that prion-like mechanisms are also at work in the tauopathies.

Keywords

Entorhinal Cortex Braak Stage Argyrophilic Grain Disease Transentorhinal Cortex Posterior Medial Temporal Lobe 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Allen B, Ingram E, Takao M, Smith MJ, Jakes R, Virdee K, Yoshida H, Holzer M, Craxton M, Emson PC, Atzori C, Migheli A, Crowther RA, Ghetti B, Spillantini MG, Goedert M (2002) Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J Neurosci 22:9340–9351PubMedGoogle Scholar
  2. Asuni AA, Boutajangout A, Quartermain D, Sigurdsson EM (2007) Immunotherapy targeting pathological tau conformers in a tangle mouse model reduces brain pathology with associated functional improvements. J Neurosci 27:9115–9129PubMedCrossRefGoogle Scholar
  3. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239–259PubMedCrossRefGoogle Scholar
  4. Braak H, Del Tredici K (2011) The pathological process underlying Alzheimer’s disease in individuals under thirty. Acta Neuropathol 121:171–181PubMedCrossRefGoogle Scholar
  5. Bugiani O, Murrell JR, Giaccone G, Hasegawa M, Ghigo G, Tabaton M, Morbin M, Primavera A, Carella F, Solaro C, Grisoli M, Savoiardo M, Spillantini MG, Tagliavini F, Goedert M, Ghetti B (1999) Frontotemporal dementia and corticobasal degeneration in a family with a P301S mutation in tau. J Neuropathol Exp Neurol 58:667–677PubMedCrossRefGoogle Scholar
  6. Caughey B, Raymond GJ (1991) The scrapie-associated form of PrP is made from a cell surface precursor that is both protease- and phospholipase-sensitive. J Biol Chem 266:18217–18223PubMedGoogle Scholar
  7. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A, Fraser G, Stalder AK, Beibel M, Staufenbiel M, Jucker M, Goedert M, Tolnay M (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11:909–913PubMedCrossRefGoogle Scholar
  8. Colby DW, Prusiner SB (2011) Prions. Cold Spring Harb Perspect Biol 3:a006833PubMedCrossRefGoogle Scholar
  9. Colby DW, Giles K, Legname G, Wille H, Baskakov IV, DeArmond SJ, Prusiner SB (2009) Design and construction of diverse mammalian prion strains. Proc Natl Acad Sci USA 106:20417–20422PubMedCrossRefGoogle Scholar
  10. Collinge J, Clarke AR (2007) A general model of prion strains and their pathogenicity. Science 318:930–936PubMedCrossRefGoogle Scholar
  11. Crowther RA, Goedert M (2000) Abnormal tau-containing filaments in neurodegenerative diseases. J Struct Biol 130:271–279PubMedCrossRefGoogle Scholar
  12. De Calignon A, Polydoro M, Suárez-Calvet M, William C, Adamowicz DH, Kopeikina KJ, Pitstick R, Sahara N, Ashe KH, Carlson GA, Spires-Jones TL, Hyman BT (2012) Propagation of tau pathology in a model of early Alzheimer’s disease. Neuron 73:685–697PubMedCrossRefGoogle Scholar
  13. Dickinson AG, Meikle VM (1969) A comparison of some biological characteristics of the mouse-passaged scrapie agents, 22A and ME7. Genet Res 13:213–225PubMedCrossRefGoogle Scholar
  14. Friedhoff P, von Bergen M, Mandelkow EM, Davies P, Mandelkow E (1998) A nucleated assembly mechanism of Alzheimer paired helical filaments. Proc Natl Acad Sci USA 95:15712–15717PubMedCrossRefGoogle Scholar
  15. Frost B, Jacks RL, Diamond MI (2009a) Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 284:12845–12852PubMedCrossRefGoogle Scholar
  16. Frost B, Ollesch J, Wille H, Diamond MI (2009b) Conformational diversity of wild-type Tau fibrils specified by templated conformation change. J Biol Chem 284:3546–3551PubMedCrossRefGoogle Scholar
  17. Goedert M, Spillantini MG (2006) A century of Alzheimer’s disease. Science 314:777–781PubMedCrossRefGoogle Scholar
  18. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer’s disease. Neuron 3:519–526PubMedCrossRefGoogle Scholar
  19. Goedert M, Clavaguera F, Tolnay M (2010) The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 33:317–325PubMedCrossRefGoogle Scholar
  20. Guo JL, Lee VM (2011) Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles. J Biol Chem 286:15317–15331PubMedCrossRefGoogle Scholar
  21. Hutton M, Lendon CL, 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 RC, Stevens M, de Graaff E, Wauters E, van Baren J, Hillebrand M, Joosse M, Kwon JM, Nowotny P, Che LK, Norton J, Morris JC, Reed LA, Trojanowski J, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd PR, Hayward N, Kwok JB, Schofield PR, Andreadis A, Snowden J, Craufurd D, Neary D, Owen F, Oostra BA, Hardy J, Goate A, van Swieten J, Mann D, Lynch T, Heutink P (1998) Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393:702–705PubMedCrossRefGoogle Scholar
  22. Lee VM, Goedert M, Trojanowski JQ (2001) Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121–1159PubMedCrossRefGoogle Scholar
  23. Liu L, Drouet V, Wu JW, Witter MP, Small SA, Clelland C, Duff K (2012) Trans-synaptic spread of tau pathology in vivo. PLoS One 7:e31302PubMedCrossRefGoogle Scholar
  24. Nonaka T, Watanabe ST, Iwatsubo T, Hasegawa M (2010) Seeded aggregation and toxicity of {alpha}-synuclein and tau: cellular models of neurodegenerative diseases. J Biol Chem 285:34885–34898PubMedCrossRefGoogle Scholar
  25. Poorkaj P, Bird TD, Wijsman E, Nemens E, Garruto RM, Anderson L, Andreadis A, Wiederholt WC, Raskind M, Schellenberg GD (1998) Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol 43:815–825PubMedCrossRefGoogle Scholar
  26. Probst A, Götz J, Wiederhold KH, Tolnay M, Mistl C, Jaton AL, Hong M, Ishihara T, Lee VM, Trojanowski JQ, Jakes R, Crowther RA, Spillantini MG, Bürki K, Goedert M (2000) Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein. Acta Neuropathol 99:469–481PubMedCrossRefGoogle Scholar
  27. Prusiner SB (1982) Novel proteinaceous infectious particles cause scrapie. Science 216:136–144PubMedCrossRefGoogle Scholar
  28. Saito Y, Ruberu NN, Sawabe M, Arai T, Tanaka N, Kakuta Y, Yamanouchi H, Murayama S (2004) Staging of argyrophilic grains: an age-associated tauopathy. J Neuropathol Exp Neurol 63:911–918PubMedGoogle Scholar
  29. Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, Ghetti B (1998) Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci USA 95:7737–7741PubMedCrossRefGoogle Scholar
  30. Tanaka M, Collins SR, Toyama BH, Weissman JS (2006) The physical basis of how prion conformations determine strain phenotypes. Nature 442:585–589PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Florence Clavaguera
    • 1
  • Markus Tolnay
    • 1
  • Michel Goedert
    • 2
    Email author
  1. 1.Institute of PathologyUniversity of BaselBaselSwitzerland
  2. 2.MRC Laboratory of Molecular BiologyCambridgeUK

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