Extracellular monomeric tau protein is sufficient to initiate the spread of tau protein pathology

Journal of Biological Chemistry

Volumn 289, Issue 2, 2014, Pages 956-967

  Michel, Claire H ^a   Kumar, Satish ^b,c   Pinotsi, Dorothea ^a   Tunnacliffe, Alan ^a   George Hyslop, Peter St ^d,e   Mandelkow, Eckhard ^b,c,f   Mandelkow, Eva Maria ^b,c,f   Kaminski, Clemens F ^a   Schierle, Gabriele S Kaminski ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^c DESY   (Germany)

^d ADDENBROOKE S HOSPITAL   (United Kingdom)

^e UNIVERSITY OF TORONTO   (Canada)

^f CENTER OF ADVANCED EUROPEAN STUDIES AND RESEARCH CAESAR   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; EXTRACELLULAR; TAU PROTEINS;

MOLECULAR BIOLOGY;

PROTEINS;

TAU PROTEIN;

ARTICLE; BIOSENSOR; CELL COMPARTMENTALIZATION; CELL MIGRATION; CELL TRANSPORT; CORRELATION ANALYSIS; ENDOCYTOSIS; HUMAN; IN VIVO STUDY; NEUROFILAMENT; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN SECRETION; PROTEIN TRANSPORT; TAUOPATHY;

ALZHEIMER DISEASE; AMYLOID; ENDOCYTOSIS; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; PROPAGATION; PROTEIN AGGREGATION; SUPERRESOLUTION MICROSCOPY; TAU;

ANIMALS; BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; ENDOCYTOSIS; ENDOSOMES; EXOCYTOSIS; EXTRACELLULAR SPACE; HUMANS; LYSOSOMES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MODELS, BIOLOGICAL; NEUROFIBRILLARY TANGLES; NEURONS; TAU PROTEINS; TAUOPATHIES; TRANSPORT VESICLES;

EID: 84891905725     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.515445     Document Type: Article

References (42)

1. Frost, B., and Diamond, M. I. (2010) Prion-like mechanisms in neurodegenerative diseases. Nat. Rev. Neurosci. 11, 155-159
2. Goedert, M., Clavaguera, F., and Tolnay, M. (2010) The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci. 33, 317-325
3. Lee, S.-J., Desplats, P., Sigurdson, C., Tsigelny, I., and Masliah, E. (2010) Cell-to-cell transmission of non-prion protein aggregates. Nat. Rev. Neurol. 6, 702-706
4. Braak, H., and Del Tredici, K. (2011) Alzheimer's pathogenesis. Is there neuron-to-neuron propagation? Acta Neuropathol. 121, 589-595
5. Danzer, K. M., Kranich, L. R., Ruf, W. P., Cagsal-Getkin, O., Winslow, A. R., Zhu, L., Vanderburg, C. R., and McLean, P. J. (2012) Exosomal cell-to-cell transmission of synuclein oligomers. Mol. Neurodegener. 7, 42
6. Braak, H., and Braak, E. (1995) Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol. Aging 16, 271-284
7. Thal, D. R., Rüb, U., Orantes, M., and Braak, H. (2002) Phases of A-deposition in the human brain and its relevance for the development of AD. Neurology 58, 1791-1800
8. Blurton-Jones, M., and Laferla, F. M. (2006) Pathways by which A-facilitates Tau pathology. Curr. Alzheimer Res. 3, 437-448
9. Arnaud, L., Robakis, N. K., and Figueiredo-Pereira, M. E. (2006) It may take inflammation, phosphorylation and ubiquitination to "tangle" in Alzheimer's disease. Neurodegener. Dis. 3, 313-319
10. Clavaguera, F., Bolmont, T., Crowther, R. A., Abramowski, D., Frank, S., Probst, A., Fraser, G., Stalder, A. K., Beibel, M., Staufenbiel, M., Jucker, M., Goedert, M., and Tolnay, M. (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat. Cell Biol. 11, 909-913
11. Frost, B., Jacks, R. L., and Diamond, M. I. (2009) Propagation of Tau misfolding from the outside to the inside of a cell. J. Biol. Chem. 284, 12845-12852
12. Guo, J. L., and Lee, V. M.-Y. (2011) Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles. J. Biol. Chem. 286, 15317-15331
13. Kim, W., Lee, S., Jung, C., Ahmed, A., Lee, G., and Hall, G. F. (2010) Interneuronal transfer of human Tau between Lamprey central neurons in situ. J. Alzheimers Dis. 19, 647-664
14. de Calignon, A., Polydoro, M., Suárez-Calvet, M., William, C., Adamowicz, D. H., Kopeikina, K. J., Pitstick, R., Sahara, N., Ashe, K. H., Carlson, G. A., Spires-Jones, T. L., and Hyman, B. T. (2012) Propagation of Tau pathology in a model of early Alzheimer's disease. Neuron 73, 685-697
15. Kfoury, N., Holmes, B. B., Jiang, H., Holtzman, D. M., and Diamond, M. I. (2012) Trans-cellular propagation of Tau aggregation by fibrillar species. J. Biol. Chem. 287, 19440-19451
16. Wu, J. W., Herman, M., Liu, L., Simoes, S., Acker, C. M., Figueroa, H., Steinberg, J. I., Margittai, M., Kayed, R., Zurzolo, C., Di Paolo, G., and Duff, K. E. (2013) Small misfolded Tau species are internalized via bulk endocytosis and anterogradely and retrogradely transported in neurons. J. Biol. Chem. 288, 1856-1870
17. Saman, S., Kim, W., Raya, M., Visnick, Y., Miro, S., Saman, S., Jackson, B., McKee, A. C., Alvarez, V. E., Lee, N. C., and Hall, G. F. (2012) ExosomeassociatedTauis secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease. J. Biol. Chem. 287, 3842-3849
18. Pooler, A. M., Phillips, E. C., Lau, D. H., Noble, W., and Hanger, D. P. (2013) Physiological release of endogenous Tau is stimulated by neuronal activity. EMBO Rep. 14, 389-394
19. Kaminski Schierle, G. S., Bertoncini, C. W., Chan, F. T., van der Goot, A. T., Schwedler, S., Skepper, J., Schlachter, S., van Ham, T., Esposito, A., Kumita, J. R., Nollen, E. A., Dobson, C. M., and Kaminski, C. F. (2011) A FRET sensor for non-invasive imaging of amyloid formation in vivo. Chemphyschem. 12, 673-680
20. Chan, F. T., Kaminski Schierle, G. S., Kumita, J. R., Bertoncini, C. W., Dobson, C. M., and Kaminski, C. F. (2013) Protein amyloids develop an intrinsic fluorescence signature during aggregation. Analyst 138, 2156-2162
21. Pinotsi, D., Buell, A. K., Dobson, C. M., Kaminski Schierle, G. S., and Kaminski, C. F. (2013) A label-free, quantitative assay of amyloid fibril growth based on intrinsic fluorescence. ChemBioChem. 14, 846-850
22. Barghorn, S., and Mandelkow, E. (2002) Toward a unified scheme for the aggregation of tau into Alzheimer paired helical filaments. Biochemistry 41, 14885-14896
23. Kaminski Schierle, G. S., van de Linde, S., Erdelyi, M., Esbjörner, E. K., Klein, T., Rees, E., Bertoncini, C. W., Dobson, C. M., Sauer, M., and Kaminski, C. F. (2011) In situ measurements of the formation and morphology of intracellular-amyloid fibrils by super-resolution fluorescence imaging. J. Am. Chem. Soc. 133, 12902-12905
24. Rees, E. J., Erdelyi, M., Pinotsi, D., Knight, A., Metcalf, D., and Kaminski, C. F. (2012) Blind assessment of localisation microscope image resolution. Opt. Nanoscopy 1, 12
25. Frank, J. H., Elder, A. D., Swartling, J., Venkitaraman, A. R., Jeyasekharan, A. D., and Kaminski, C. F. (2007) A white light confocal microscope for spectrally resolved multidimensional imaging. J. Microsc. 227, 203-215
26. Barghorn, S., Biernat, J., and Mandelkow, E. (2005) Purification of recombinant Tau protein and preparation of Alzheimer-paired helical filaments in vitro. Methods Mol. Biol. 299, 35-51
27. von Bergen, M., Barghorn, S., Müller, S. A., Pickhardt, M., Biernat, J., Mandelkow, E.-M., Davies, P., Aebi, U., and Mandelkow, E. (2006) The core of Tau-paired helical filaments studied by scanning transmission electron microscopy and limited proteolysis. Biochemistry 45, 6446-6457
28. Goedert, M., Jakes, R., Spillantini, M. G., Hasegawa, M., Smith, M. J., and Crowther, R. A. (1996) Assembly of microtubule-associated protein Tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature 383, 550-553
29. Esko, J. D., Stewart, T. E., and Taylor, W. H. (1985) Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 82, 3197-3201
30. Niles, W. D., and Malik, A. B. (1999) Endocytosis and exocytosis events regulate vesicle traffic in endothelial cells. J. Membr. Biol. 167, 85-101
31. Kaganovich, D., Kopito, R., and Frydman, J. (2008) Misfolded proteins partition between two distinct quality control compartments. Nature 454, 1088-1095
32. Mellman, I., Fuchs, R., and Helenius, A. (1986) Acidification of the endocytic and exocytic pathways. Annu. Rev. Biochem. 55, 663-700
33. Wille, H., Drewes, G., Biernat, J., Mandelkow, E. M., and Mandelkow, E. (1992) Alzheimer-like paired helical filaments and antiparallel dimers formed from microtubule-associated protein Tau in vitro. J. Cell Biol. 118, 573-584
34. Johnson, V. E., Stewart, W., and Smith, D. H. (2012) Widespread Tau and amyloid-pathology many years after a single traumatic brain injury in humans. Brain Pathol. 22, 142-149
35. Yang, A. J., Chandswangbhuvana, D., Margol, L., and Glabe, C. G. (1998) Loss of endosomal/lysosomal membrane impermeability is an early event in amyloid A 1-42 pathogenesis. J. Neurosci. Res. 52, 691-698
36. Ditaranto, K., Tekirian, T. L., and Yang, A. J. (2001) Lysosomal membrane damage in soluble A-mediated cell death in Alzheimer's disease. Neurobiol. Dis. 8, 19-31
37. Jones, E. M., Dubey, M., Camp, P. J., Vernon, B. C., Biernat, J., Mandelkow, E., Majewski, J., and Chi, E. Y. (2012) Interaction of Tau protein with model lipid membranes induces Tau structural compaction and membrane disruption. Biochemistry 51, 2539-2550
38. Wang, Y., Martinez-Vicente, M., Krüger, U., Kaushik, S., Wong, E., Mandelkow, E.-M., Cuervo, A. M., and Mandelkow, E. (2009) Tau fragmentation, aggregation and clearance. The dual role of lysosomal processing. Hum. Mol. Genet. 18, 4153-4170
39. Lee, H.-J., Patel, S., and Lee, S.-J. (2005) Intravesicular localization and exocytosis of-synuclein and its aggregates. J. Neurosci. 25, 6016-6024
40. Simón, D., García-García, E., Royo, F., Falcón-Pérez, J. M., and Avila, J. (2012) Proteostasis of Tau. Tau overexpression results in its secretion via membrane vesicles. FEBS Lett. 586, 47-54
41. Karch, C. M., Jeng, A. T., and Goate, A. M. (2012) Extracellular Tau levels are influenced by variability in Tau that is associated with tauopathies. J. Biol. Chem. 287, 42751-42762
42. Karch, C. M., Jeng, A. T., and Goate, A. M. (2013) Calcium phosphatase calcineurin influences Tau metabolism. Neurobiol. Aging 34, 374-386