Extracellular Monomeric and Aggregated Tau Efficiently Enter Human Neurons through Overlapping but Distinct Pathways

Cell Reports

Volumn 22, Issue 13, 2018, Pages 3612-3624

  Evans, Lewis D ^a,b   Wassmer, Thomas ^a   Fraser, Graham ^c   Smith, James ^a,b   Perkinton, Michael ^c   Billinton, Andrew ^c   Livesey, Frederick J ^a,b  

^a Babraham Research Campus   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c ASTRAZENECA   (United Kingdom)

Author keywords

Alzheimer's disease; endocytosis; frontotemporal dementia; human neurons; intracellular transport; iPSC; MAPT; Tau

Indexed keywords

ACTIN; DYNAMIN; MONOMER; PROTEIN ANTIBODY; TAU PROTEIN; MAPT PROTEIN, HUMAN;

ACTIN POLYMERIZATION; ARTICLE; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; INTERNALIZATION; MICROPINOCYTOSIS; NERVE CELL; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN TRANSPORT; BRAIN CORTEX; CYTOLOGY; HUMAN EMBRYONIC STEM CELL; INDUCED PLURIPOTENT STEM CELL; METABOLISM; PHOSPHORYLATION; PROTEINOSIS;

CEREBRAL CORTEX; DYNAMINS; ENDOCYTOSIS; HUMAN EMBRYONIC STEM CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; NEURONS; PHOSPHORYLATION; PROTEIN AGGREGATION, PATHOLOGICAL; TAU PROTEINS;

EID: 85044301147     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2018.03.021     Document Type: Article

References (36)

1. Blennow, K., Wallin, A., Agren, H., Spenger, C., Siegfried, J., Vanmechelen, E., Tau protein in cerebrospinal fluid: a biochemical marker for axonal degeneration in Alzheimer disease?. Mol. Chem. Neuropathol. 26 (1995), 231–245.
2. Braak, H., Braak, E., Demonstration of amyloid deposits and neurofibrillary changes in whole brain sections. Brain Pathol. 1 (1991), 213–216.
3. Bright, J., Hussain, S., Dang, V., Wright, S., Cooper, B., Byun, T., Ramos, C., Singh, A., Parry, G., Stagliano, N., Griswold-Prenner, I., Human secreted tau increases amyloid-beta production. Neurobiol. Aging 36 (2015), 693–709.
4. Bugiani, O., Murrell, J.R., Giaccone, G., Hasegawa, M., Ghigo, G., Tabaton, M., Morbin, M., Primavera, A., Carella, F., Solaro, C., et al. Frontotemporal dementia and corticobasal degeneration in a family with a P301S mutation in tau. J. Neuropathol. Exp. Neurol. 58 (1999), 667–677.
5. Butner, K.A., Kirschner, M.W., Tau protein binds to microtubules through a flexible array of distributed weak sites. J. Cell Biol. 115 (1991), 717–730.
6. Chai, X., Wu, S., Murray, T.K., Kinley, R., Cella, C.V., Sims, H., Buckner, N., Hanmer, J., Davies, P., O'Neill, M.J., et al. Passive immunization with anti-Tau antibodies in two transgenic models: reduction of Tau pathology and delay of disease progression. J. Biol. Chem. 286 (2011), 34457–34467.
7. Chai, X., Dage, J.L., Citron, M., Constitutive secretion of tau protein by an unconventional mechanism. Neurobiol. Dis. 48 (2012), 356–366.
8. Congdon, E.E., Lin, Y., Rajamohamedsait, H.B., Shamir, D.B., Krishnaswamy, S., Rajamohamedsait, W.J., Rasool, S., Gonzalez, V., Levenga, J., Gu, J., et al. Affinity of Tau antibodies for solubilized pathological Tau species but not their immunogen or insoluble Tau aggregates predicts in vivo and ex vivo efficacy. Mol. Neurodegener., 11, 2016, 62.
9. Frost, B., Jacks, R.L., Diamond, M.I., Propagation of tau misfolding from the outside to the inside of a cell. J. Biol. Chem. 284 (2009), 12845–12852.
10. Funk, K.E., Mirbaha, H., Jiang, H., Holtzman, D.M., Diamond, M.I., Distinct Therapeutic Mechanisms of Tau Antibodies: Promoting Microglial Clearance Versus Blocking Neuronal Uptake. J. Biol. Chem. 290 (2015), 21652–21662.
11. Ghetti, B., Oblak, A.L., Boeve, B.F., Johnson, K.A., Dickerson, B.C., Goedert, M., Invited review: Frontotemporal dementia caused by microtubule-associated protein tau gene (MAPT) mutations: a chameleon for neuropathology and neuroimaging. Neuropathol. Appl. Neurobiol. 41 (2015), 24–46.
12. Goedert, M., Spillantini, M.G., Cairns, N.J., Crowther, R.A., Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8 (1992), 159–168.
13. Grundke-Iqbal, I., Iqbal, K., Quinlan, M., Tung, Y.C., Zaidi, M.S., Wisniewski, H.M., Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J. Biol. Chem. 261 (1986), 6084–6089.
14. Gu, J., Sigurdsson, E.M., Immunotherapy for tauopathies. J. Mol. Neurosci. 45 (2011), 690–695.
15. Gu, J., Congdon, E.E., Sigurdsson, E.M., Two novel Tau antibodies targeting the 396/404 region are primarily taken up by neurons and reduce Tau protein pathology. J. Biol. Chem. 288 (2013), 33081–33095.
16. Guo, T., Noble, W., Hanger, D.P., Roles of tau protein in health and disease. Acta Neuropathol. 133 (2017), 665–704.
17. Holmes, B.B., DeVos, S.L., Kfoury, N., Li, M., Jacks, R., Yanamandra, K., Ouidja, M.O., Brodsky, F.M., Marasa, J., Bagchi, D.P., et al. Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc. Natl. Acad. Sci. USA 110 (2013), E3138–E3147.
18. Iba, M., Guo, J.L., McBride, J.D., Zhang, B., Trojanowski, J.Q., Lee, V.M., Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer's-like tauopathy. J. Neurosci. 33 (2013), 1024–1037.
19. Kanmert, D., Cantlon, A., Muratore, C.R., Jin, M., O'Malley, T.T., Lee, G., Young-Pearse, T.L., Selkoe, D.J., Walsh, D.M., C-Terminally Truncated Forms of Tau, But Not Full-Length Tau or Its C-Terminal Fragments, Are Released from Neurons Independently of Cell Death. J. Neurosci. 35 (2015), 10851–10865.
20. Kfoury, N., Holmes, B.B., Jiang, H., Holtzman, D.M., Diamond, M.I., Trans-cellular propagation of Tau aggregation by fibrillar species. J. Biol. Chem. 287 (2012), 19440–19451.
21. Kosik, K.S., Joachim, C.L., Selkoe, D.J., Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc. Natl. Acad. Sci. USA 83 (1986), 4044–4048.
22. Liu, L., Drouet, V., Wu, J.W., Witter, M.P., Small, S.A., Clelland, C., Duff, K., Trans-synaptic spread of tau pathology in vivo. PLoS ONE, 7, 2012, e31302.
23. Loebrich, S., The role of F-actin in modulating Clathrin-mediated endocytosis: Lessons from neurons in health and neuropsychiatric disorder. Commun. Integr. Biol., 7, 2014, e28740.
24. Mallery, D.L., McEwan, W.A., Bidgood, S.R., Towers, G.J., Johnson, C.M., James, L.C., Antibodies mediate intracellular immunity through tripartite motif-containing 21 (TRIM21). Proc. Natl. Acad. Sci. USA 107 (2010), 19985–19990.
25. Mao, X., Ou, M.T., Karuppagounder, S.S., Kam, T.I., Yin, X., Xiong, Y., Ge, P., Umanah, G.E., Brahmachari, S., Shin, J.H., et al. Pathological α-synuclein transmission initiated by binding lymphocyte-activation gene 3. Science, 353, 2016, aah3374.
26. McEwan, W.A., Falcon, B., Vaysburd, M., Clift, D., Oblak, A.L., Ghetti, B., Goedert, M., James, L.C., Cytosolic Fc receptor TRIM21 inhibits seeded tau aggregation. Proc. Natl. Acad. Sci. USA 114 (2017), 574–579.
27. Mooren, O.L., Galletta, B.J., Cooper, J.A., Roles for actin assembly in endocytosis. Annu. Rev. Biochem. 81 (2012), 661–686.
28. Nicholls, S.B., DeVos, S.L., Commins, C., Nobuhara, C., Bennett, R.E., Corjuc, D.L., Maury, E., Eftekharzadeh, B., Akingbade, O., Fan, Z., et al. Characterization of TauC3 antibody and demonstration of its potential to block tau propagation. PLoS ONE, 12, 2017, e0177914.
29. Olsson, A., Vanderstichele, H., Andreasen, N., De Meyer, G., Wallin, A., Holmberg, B., Rosengren, L., Vanmechelen, E., Blennow, K., Simultaneous measurement of beta-amyloid(1-42), total tau, and phosphorylated tau (Thr181) in cerebrospinal fluid by the xMAP technology. Clin. Chem. 51 (2005), 336–345.
30. Preta, G., Cronin, J.G., Sheldon, I.M., Dynasore - not just a dynamin inhibitor. Cell Commun. Signal., 13, 2015, 24.
31. Shi, Y., Kirwan, P., Livesey, F.J., Directed differentiation of human pluripotent stem cells to cerebral cortex neurons and neural networks. Nat. Protoc. 7 (2012), 1836–1846.
32. Shi, Y., Kirwan, P., Smith, J., Robinson, H.P., Livesey, F.J., Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses. Nat. Neurosci. 15 (2012), 477–486.
33. Wang, Y., Balaji, V., Kaniyappan, S., Krüger, L., Irsen, S., Tepper, K., Chandupatla, R., Maetzler, W., Schneider, A., Mandelkow, E., Mandelkow, E.M., The release and trans-synaptic transmission of Tau via exosomes. Mol. Neurodegener., 12, 2017, 5.
34. Wu, J.W., Herman, M., Liu, L., Simoes, S., Acker, C.M., Figueroa, H., Steinberg, J.I., Margittai, M., Kayed, R., Zurzolo, C., et al. Small misfolded Tau species are internalized via bulk endocytosis and anterogradely and retrogradely transported in neurons. J. Biol. Chem. 288 (2013), 1856–1870.
35. Yamada, K., Cirrito, J.R., Stewart, F.R., Jiang, H., Finn, M.B., Holmes, B.B., Binder, L.I., Mandelkow, E.M., Diamond, M.I., Lee, V.M., Holtzman, D.M., In vivo microdialysis reveals age-dependent decrease of brain interstitial fluid tau levels in P301S human tau transgenic mice. J. Neurosci. 31 (2011), 13110–13117.
36. Yanamandra, K., Kfoury, N., Jiang, H., Mahan, T.E., Ma, S., Maloney, S.E., Wozniak, D.F., Diamond, M.I., Holtzman, D.M., Anti-tau antibodies that block tau aggregate seeding in vitro markedly decrease pathology and improve cognition in vivo. Neuron 80 (2013), 402–414.