Enhanced Tau Aggregation in the Presence of Amyloid β

American Journal of Pathology

Volumn 187, Issue 7, 2017, Pages 1601-1612

  Bennett, Rachel E ^a   DeVos, Sarah L ^a   Dujardin, Simon ^a   Corjuc, Bianca ^a   Gor, Rucha ^a   Gonzalez, Jose ^a   Roe, Allyson D ^a   Frosch, Matthew P ^a   Pitstick, Rose ^b   Carlson, George A ^b   Hyman, Bradley T ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MCLAUGHLIN RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; PRESENILIN; TAU PROTEIN; MAPT PROTEIN, HUMAN; MAPT PROTEIN, MOUSE;

ADULT; AGED; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN TISSUE; CEREBELLUM; COMPARATIVE STUDY; CONTROLLED STUDY; ENTORHINAL CORTEX; FEMALE; HIPPOCAMPUS; HISTOLOGY; HUMAN; HUMAN TISSUE; MALE; MIDDLE AGED; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PARAHIPPOCAMPAL GYRUS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SENILE PLAQUE; TRANSGENE; VERY ELDERLY; ANIMAL; DISEASE MODEL; GENETICS; METABOLISM; NEOCORTEX; NEUROFIBRILLARY TANGLE; PATHOLOGY; PHOSPHORYLATION; PROTEINOSIS; TRANSGENIC MOUSE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; NEOCORTEX; NEUROFIBRILLARY TANGLES; PHOSPHORYLATION; PLAQUE, AMYLOID; PROTEIN AGGREGATION, PATHOLOGICAL; TAU PROTEINS;

EID: 85020805737     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2017.03.011     Document Type: Article

References (36)

1. Braak, H., Braak, E., Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82 (1991), 239–259.
2. Thal, D.R., Rüb, U., Orantes, M., Braak, H., Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology 58 (2002), 1791–1800.
3. Arriagada, P.V., Growdon, J.H., Hedley-Whyte, E.T., Hyman, B.T., Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42 (1992), 631–639.
4. Bierer, L.M., Hof, P.R., Purohit, D.P., Carlin, L., Schmeidler, J., Davis, K.L., Perl, D.P., Neocortical neurofibrillary tangles correlate with dementia severity in Alzheimer's disease. Arch Neurol 52 (1995), 81–88.
5. Bolmont, T., Clavaguera, F., Meyer-Luehmann, M., Herzig, M.C., Radde, R., Staufenbiel, M., Lewis, J., Hutton, M., Tolnay, M., Jucker, M., Induction of tau pathology by intracerebral infusion of amyloid-β-containing brain extract and by amyloid-β deposition in APP × Tau transgenic mice. Am J Pathol 171 (2007), 2012–2020.
6. Héraud, C., Goufak, D., Ando, K., Leroy, K., Suain, V., Yilmaz, Z., De Decker, R., Authelet, M., Laporte, V., Octave, J.N., Brion, J.P., Increased misfolding and truncation of tau in APP/PS1/tau transgenic mice compared to mutant tau mice. Neurobiol Dis 62 (2014), 100–112.
7. Hurtado, D.E., Molina-Porcel, L., Iba, M., Aboagye, A.K., Paul, S.M., Trojanowski, J.Q., Lee, V.M., Aβ accelerates the spatiotemporal progression of tau pathology and augments tau amyloidosis in an Alzheimer mouse model. Am J Pathol 177 (2010), 1977–1988.
8. Pérez, M., Ribe, E., Rubio, A., Lim, F., Morán, M.A., Ramos, P.G., Ferrer, I., Isla, M.T.G., Avila, J., Characterization of a double (amyloid precursor protein-tau) transgenic: tau phosphorylation and aggregation. Neuroscience 130 (2005), 339–347.
9. Ribé, E.M., Pérez, M., Puig, B., Gich, I., Lim, F., Cuadrado, M., Sesma, T., Catena, S., Sánchez, B., Nieto, M., Gómez-Ramos, P., Morán, M.A., Cabodevilla, F., Samaranch, L., Ortiz, L., Pérez, A., Ferrer, I., Avila, J., Gómez-Isla, T., Accelerated amyloid deposition, neurofibrillary degeneration and neuronal loss in double mutant APP/tau transgenic mice. Neurobiol Dis 20 (2005), 814–822.
10. Saul, A., Sprenger, F., Bayer, T.A., Wirths, O., Accelerated tau pathology with synaptic and neuronal loss in a novel triple transgenic mouse model of Alzheimer's disease. Neurobiol Aging 34 (2013), 2564–2573.
11. Seino, Y., Kawarabayashi, T., Wakasaya, Y., Watanabe, M., Takamura, A., Yamamoto-Watanabe, Y., Kurata, T., Abe, K., Ikeda, M., Westaway, D., Murakami, T., Hyslop, P.S.G., Matsubara, E., Shoji, M., Amyloid β accelerates phosphorylation of tau and neurofibrillary tangle formation in an amyloid precursor protein and tau double-transgenic mouse model. J Neurosci Res 88 (2010), 3547–3554.
12. Forny-Germano, L., Lyra e Silva, N.M., Batista, A.F., Brito-Moreira, J., Gralle, M., Boehnke, S.E., Coe, B.C., Lablans, A., Marques, S.A., Martinez, A.M.B., Klein, W.L., Houzel, J.C., Ferreira, S.T., Munoz, D.P., De Felice, F.G., Alzheimer's disease-like pathology induced by amyloid-β oligomers in nonhuman primates. J Neurosci 34 (2014), 13629–13643.
13. Oddo, S., Caccamo, A., Shepherd, J.D., Murphy, M.P., Golde, T.E., Kayed, R., Metherate, R., Mattson, M.P., Akbari, Y., LaFerla, F.M., Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39 (2003), 409–421.
14. Götz, J., Chen, F., van Dorpe, J., Nitsch, R.M., Lewis, J., Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils. Science 293 (2001), 1491–1495.
15. Lewis, J., Dickson, D.W., Lin, W.L., Chisholm, L., Corral, A., Jones, G., Yen, S.H., Sahara, N., Skipper, L., Yager, D., Eckman, C., Hardy, J., Hutton, M., McGowan, E., Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293 (2001), 1487–1491.
16. Pooler, A.M., Polydoro, M., Maury, E.A., Nicholls, S.B., Reddy, S.M., Wegmann, S., William, C., Saqran, L., Cagsal-Getkin, O., Pitstick, R., Beier, D.R., Carlson, G.A., Spires-Jones, T.L., Hyman, B.T., Amyloid accelerates tau propagation and toxicity in a model of early Alzheimer's disease. Acta Neuropathol Commun, 3, 2015, 14.
17. Hyman, B.T., Phelps, C.H., Beach, T.G., Bigio, E.H., Cairns, N.J., Carrillo, M.C., Dickson, D.W., Duyckaerts, C., Frosch, M.P., Masliah, E., Mirra, S.S., Nelson, P.T., Schneider, J.A., Thal, D.R., Thies, B., Trojanowski, J.Q., Vinters, H.V., Montine, T.J., National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease. Alzheimers Dement 8 (2012), 1–13.
18. Mayford, M., Bach, M.E., Huang, Y.Y., Wang, L., Hawkins, R.D., Kandel, E.R., Control of memory formation through regulated expression of a CaMKII transgene. Science 274 (1996), 1678–1683.
19. Jankowsky, J.L., Fadale, D.J., Anderson, J., Xu, G.M., Gonzales, V., Jenkins, N.A., Copeland, N.G., Lee, M.K., Younkin, L.H., Wagner, S.L., Younkin, S.G., Borchelt, D.R., Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum Mol Genet 13 (2004), 159–170.
20. Jankowsky, J.L., Slunt, H.H., Ratovitski, T., Jenkins, N.A., Copeland, N.G., Borchelt, D.R., Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol Eng 17 (2001), 157–165.
21. Santacruz, K., Lewis, J., Spires, T., Paulson, J., Kotilinek, L., Ingelsson, M., Guimaraes, A., DeTure, M., Ramsden, M., McGowan, E., Forster, C., Yue, M., Orne, J., Janus, C., Mariash, A., Kuskowski, M., Hyman, B., Hutton, M., Ashe, K.H., Tau suppression in a neurodegenerative mouse model improves memory function. Science 309 (2005), 476–481.
22. Carlson, G.A., Borchelt, D.R., Dake, A., Turner, S., Danielson, V., Coffin, J.D., Eckman, C., Meiners, J., Nilsen, S.P., Younkin, S.G., Hsiao, K.K., Genetic modification of the phenotypes produced by amyloid precursor protein overexpression in transgenic mice. Hum Mol Genet 6 (1997), 1951–1959.
23. Sanders, D.W., Kaufman, S.K., DeVos, S.L., Sharma, A.M., Mirbaha, H., Li, A., Barker, S.J., Foley, A.C., Thorpe, J.R., Serpell, L.C., Miller, T.M., Grinberg, L.T., Seeley, W.W., Diamond, M.I., Distinct Tau prion strains propagate in cells and mice and define different tauopathies. Neuron 82 (2014), 1271–1288.
24. Halfmann, R., Lindquist, S., Screening for amyloid aggregation by semi-denaturing detergent-agarose gel electrophoresis. J Vis Exp, 17, 2008, 838.
25. Holmes, B.B., Furman, J.L., Mahan, T.E., Yamasaki, T.R., Mirbaha, H., Eades, W.C., Belaygorod, L., Cairns, N.J., Holtzman, D.M., Diamond, M.I., Proteopathic tau seeding predicts tauopathy in vivo. Proc Natl Acad Sci U S A 111 (2014), E4376–E4385.
26. Takeda, S., Wegmann, S., Cho, H., DeVos, S.L., Commins, C., Roe, A.D., Nicholls, S.B., Carlson, G.A., Pitstick, R., Nobuhara, C.K., Costantino, I., Frosch, M.P., Müller, D.J., Irimia, D., Hyman, B.T., Neuronal uptake and propagation of a rare phosphorylated high-molecular-weight tau derived from Alzheimer's disease brain. Nat Commun, 6, 2015, 8490.
27. Usenovic, M., Niroomand, S., Drolet, R.E., Yao, L., Gaspar, R.C., Hatcher, N.G., Schachter, J., Renger, J.J., Parmentier-Batteur, S., Internalized tau oligomers cause neurodegeneration by inducing accumulation of pathogenic tau in human neurons derived from induced pluripotent stem cells. J Neurosci 35 (2015), 14234–14250.
28. Braak, H., Alafuzoff, I., Arzberger, T., Kretzschmar, H., Del Tredici, K., Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112 (2006), 389–404.
29. Mirra, S.S., Heyman, A., McKeel, D., Sumi, S.M., Crain, B.J., Brownlee, L.M., Vogel, F.S., Hughes, J.P., van Belle, G., Berg, L., The Consortium to Establish a Registry for Alzheimer's Disease (CERAD), part II: standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41 (1991), 479–486.
30. Crary, J.F., Trojanowski, J.Q., Schneider, J.A., Abisambra, J.F., Abner, E.L., Alafuzoff, I., et al. Primary age-related tauopathy (PART): a common pathology associated with human aging. Acta Neuropathol 128 (2014), 755–766.
31. 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.
32. Tai, H.C., Serrano-Pozo, A., Hashimoto, T., Frosch, M.P., Spires-Jones, T.L., Hyman, B.T., The synaptic accumulation of hyperphosphorylated tau oligomers in Alzheimer disease is associated with dysfunction of the ubiquitin-proteasome system. Am J Pathol 181 (2012), 1426–1435.
33. Vasconcelos, B., Stancu, I.C., Buist, A., Bird, M., Wang, P., Vanoosthuyse, A., Van Kolen, K., Verheyen, A., Kienlen-Campard, P., Octave, J.N., Baatsen, P., Moechars, D., Dewachter, I., Heterotypic seeding of Tau fibrillization by pre-aggregated Abeta provides potent seeds for prion-like seeding and propagation of Tau-pathology in vivo. Acta Neuropathol 131 (2016), 549–569.
34. Bhaskar, K., Konerth, M., Kokiko-Cochran, O.N., Cardona, A., Ransohoff, R.M., Lamb, B.T., Regulation of tau pathology by the microglial fractalkine receptor. Neuron 68 (2010), 19–31.
35. Kitazawa, M., Oddo, S., Yamasaki, T.R., Green, K.N., LaFerla, F.M., Lipopolysaccharide-induced inflammation exacerbates Tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease. J Neurosci 25 (2005), 8843–8853.
36. Gorlovoy, P., Larionov, S., Pham, T.T.H., Neumann, H., Accumulation of tau induced in neurites by microglial proinflammatory mediators. FASEB J 23 (2009), 2502–2513.