In vitro generation of tau aggregates conformationally distinct from parent tau seeds of Alzheimer’s brain

References

• Binder LI, Frankfurter A, Rebhun LI. The distribution of tau in the mammalian central nervous system. J Cell Biol. 1985;101:1371–1378.
   PubMed Web of Science ®Google Scholar
• Iqbal K, Grundke-Iqbal I, Zaidi T, et al. Defective brain microtubule assembly in Alzheimer’s disease. Lancet. 1986;2:421–426.
   PubMed Web of Science ®Google Scholar
• Goedert M, Spillantini MG, Jakes R, et al. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer’s disease. Neuron. 1989;3:519–526.
   PubMed Web of Science ®Google Scholar
• Goedert M, Jakes R. Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. Embo J. 1990;9:4225–4230.
   PubMed Web of Science ®Google Scholar
• Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991;82:239–259.
   PubMed Web of Science ®Google Scholar
• Spillantini MG, Goedert M. Tau pathology and neurodegeneration. Lancet Neurol. 2013;12:609–622.
   PubMed Web of Science ®Google Scholar
• Hof PR, Bouras C, Buee L, et al. Differential distribution of neurofibrillary tangles in the cerebral cortex of dementia pugilistica and Alzheimer’s disease cases. Acta Neuropathol. 1992;85:23–30.
   PubMed Web of Science ®Google Scholar
• McKee AC, Kosik KS, Kowall NW. Neuritic pathology and dementia in Alzheimer’s disease. Ann Neurol. 1991;30:156–165.
   PubMed Web of Science ®Google Scholar
• Saito Y, Ruberu NN, Sawabe M, et al. Staging of argyrophilic grains: an age-associated tauopathy. J Neuropathol Exp Neurol. 2004;63:911–918.
   PubMed Web of Science ®Google Scholar
• McKee AC, Stern RA, Nowinski CJ, et al. The spectrum of disease in chronic traumatic encephalopathy. Brain. 2013;136:43–64.
   PubMed Web of Science ®Google Scholar
• Frost B, Jacks RL, Diamond MI. Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem. 2009;284:12845–12852.
   PubMed Web of Science ®Google Scholar
• Holmes BB, DeVos SL, Kfoury N, et al. Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc Natl Acad Sci U S A. 2013;110:E3138–47.
   PubMed Web of Science ®Google Scholar
• Liu L, Drouet V, Wu JW, et al. Trans-synaptic spread of tau pathology in vivo. PLoS One. 2012;7:e31302.
   PubMed Web of Science ®Google Scholar
• Clavaguera F, Tolnay M, Goedert M. The prion-like behavior of assembled tau in transgenic mice. Cold Spring Harb Perspect Med. 2017;7.
   PubMed Web of Science ®Google Scholar
• Stancu IC, Vasconcelos B, Ris L, et al. Templated misfolding of Tau by prion-like seeding along neuronal connections impairs neuronal network function and associated behavioral outcomes in Tau transgenic mice. Acta Neuropathol. 2015;129:875–894.
   PubMed Web of Science ®Google Scholar
• Iba M, McBride JD, Guo JL, et al. Tau pathology spread in PS19 tau transgenic mice following locus coeruleus (LC) injections of synthetic tau fibrils is determined by the LC’s afferent and efferent connections. Acta Neuropathol. 2015;130:349–362.
   PubMed Web of Science ®Google Scholar
• Guo JL, Narasimhan S, Changolkar L, et al. Unique pathological tau conformers from Alzheimer’s brains transmit tau pathology in nontransgenic mice. J Exp Med. 2016;213:2635–2654.
   PubMed Web of Science ®Google Scholar
• Boluda S, Iba M, Zhang B, et al. Differential induction and spread of tau pathology in young PS19 tau transgenic mice following intracerebral injections of pathological tau from Alzheimer’s disease or corticobasal degeneration brains. Acta Neuropathol. 2015;129:221–237.
   PubMed Web of Science ®Google Scholar
• Clavaguera F, Akatsu H, Fraser G, et al. Brain homogenates from human tauopathies induce tau inclusions in mouse brain. Proc Natl Acad Sci U S A. 2013;110:9535–9540.
   PubMed Web of Science ®Google Scholar
• Kaufman SK, Sanders DW, Thomas TL, et al. Tau prion strains dictate patterns of cell pathology, progression rate, and regional vulnerability in vivo. Neuron. 2016;92:796–812.
   PubMed Web of Science ®Google Scholar
• Sanders DW, Kaufman SK, DeVos SL, et al. Distinct tau prion strains propagate in cells and mice and define different tauopathies. Neuron. 2014;82:1271–1288.
   PubMed Web of Science ®Google Scholar
• Falcon B, Cavallini A, Angers R, et al. Conformation determines the seeding potencies of native and recombinant Tau aggregates. J Biol Chem. 2015;290:1049–1065.
   PubMed Web of Science ®Google Scholar
• Silveira JR, Raymond GJ, Hughson AG, et al. The most infectious prion protein particles. Nature. 2005;437:257–261.
   PubMed Web of Science ®Google Scholar
• Prusiner SB. Prions. Proc Natl Acad Sci U S A. 1998;95:13363–13383.
   PubMed Web of Science ®Google Scholar
• Bessen RA, Marsh RF. Biochemical and physical properties of the prion protein from two strains of the transmissible mink encephalopathy agent. J Virol. 1992;66:2096–2101.
   PubMed Web of Science ®Google Scholar
• Parchi P, Castellani R, Capellari S, et al. Molecular basis of phenotypic variability in sporadic Creutzfeldt-Jakob disease. Ann Neurol. 1996;39:767–778.
   PubMed Web of Science ®Google Scholar
• Collinge J, Sidle KC, Meads J, et al. Molecular analysis of prion strain variation and the aetiology of ‘new variant’ CJD. Nature. 1996;383:685–690.
   PubMed Web of Science ®Google Scholar
• Castilla J, Morales R, Saa P, et al. Cell-free propagation of prion strains. Embo J. 2008;27:2557–2566.
   PubMed Web of Science ®Google Scholar
• Scott MR, Will R, Ironside J, et al. Compelling transgenetic evidence for transmission of bovine spongiform encephalopathy prions to humans. Proc Natl Acad Sci U S A. 1999;96:15137–15142.
   PubMed Web of Science ®Google Scholar
• Telling GC, Parchi P, DeArmond SJ, et al. Evidence for the conformation of the pathologic isoform of the prion protein enciphering and propagating prion diversity. Science. 1996;274:2079–2082.
   PubMed Web of Science ®Google Scholar
• Takahashi M, Miyata H, Kametani F, et al. Extracellular association of APP and tau fibrils induces intracellular aggregate formation of tau. Acta Neuropathol. 2015;129:895–907.
   PubMed Web of Science ®Google Scholar
• Audouard E, Houben S, Masaracchia C, et al. High-molecular-weight paired helical filaments from alzheimer brain induces seeding of wild-type mouse tau into an argyrophilic 4R tau pathology in vivo. Am J Pathol. 2016;186:2709–2722.
   PubMed Web of Science ®Google Scholar
• Santa-Maria I, Varghese M, Ksiezak-Reding H, et al. Paired helical filaments from Alzheimer disease brain induce intracellular accumulation of Tau protein in aggresomes. J Biol Chem. 2012;287:20522–20533.
   PubMed Web of Science ®Google Scholar
• Woerman AL, Stohr J, Aoyagi A, et al. Propagation of prions causing synucleinopathies in cultured cells. Proc Natl Acad Sci U S A. 2015;112:E4949–58.
   PubMed Web of Science ®Google Scholar
• Saijo E, Ghetti B, Zanusso G, et al. Ultrasensitive and selective detection of 3-repeat tau seeding activity in Pick disease brain and cerebrospinal fluid. Acta Neuropathol. 2017;133:751–765.
   PubMed Web of Science ®Google Scholar
• Vasconcelos B, Stancu IC, Buist A, et al. 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. 2016;131:549–569.
   PubMed Web of Science ®Google Scholar
• de Silva R, Lashley T, Gibb G, et al. Pathological inclusion bodies in tauopathies contain distinct complements of tau with three or four microtubule-binding repeat domains as demonstrated by new specific monoclonal antibodies. Neuropathol Appl Neurobiol. 2003;29:288–302.
   PubMed Web of Science ®Google Scholar
• Yoshida H, Goedert M. Sequential phosphorylation of tau protein by cAMP-dependent protein kinase and SAPK4/p38delta or JNK2 in the presence of heparin generates the AT100 epitope. J Neurochem. 2006;99:154–164.
   PubMed Web of Science ®Google Scholar
• Porzig R, Singer D, Hoffmann R. Epitope mapping of mAbs AT8 and Tau5 directed against hyperphosphorylated regions of the human tau protein. Biochem Biophys Res Commun. 2007;358:644–649.
   PubMed Web of Science ®Google Scholar
• Woerman AL, Aoyagi A, Patel S, et al. Tau prions from Alzheimer’s disease and chronic traumatic encephalopathy patients propagate in cultured cells. Proc Natl Acad Sci U S A. 2016;113:E8187–e96.
   PubMed Web of Science ®Google Scholar
• Jackson SJ, Kerridge C, Cooper J, et al. Short fibrils constitute the major species of seed-competent tau in the brains of mice transgenic for human P301S tau. J Neurosci. 2016;36:762–772.
   PubMed Web of Science ®Google Scholar
• Takeda S, Wegmann S, Cho H, et al. Neuronal uptake and propagation of a rare phosphorylated high-molecular-weight tau derived from Alzheimer’s disease brain. Nat Commun. 2015;6:8490.
   PubMed Web of Science ®Google Scholar
• Novak M, Kabat J, Wischik CM. Molecular characterization of the minimal protease resistant tau unit of the Alzheimer’s disease paired helical filament. Embo J. 1993;12:365–370.
   PubMed Web of Science ®Google Scholar
• Dan A, Takahashi M, Masuda-Suzukake M, et al. Extensive deamidation at asparagine residue 279 accounts for weak immunoreactivity of tau with RD4 antibody in Alzheimer’s disease brain. Acta Neuropathol Commun. 2013;1:54.
   PubMed Web of Science ®Google Scholar
• Jakes R, Novak M, Davison M, et al. Identification of 3- and 4-repeat tau isoforms within the PHF in Alzheimer’s disease. Embo J. 1991;10:2725–2729.
   PubMed Web of Science ®Google Scholar
• Cronier S, Laude H, Peyrin JM. Prions can infect primary cultured neurons and astrocytes and promote neuronal cell death. Proc Natl Acad Sci U S A. 2004;101:12271–12276.
   PubMed Web of Science ®Google Scholar
• Guo JL, Lee VM. Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles. J Biol Chem. 2011;286:15317–15331.
   PubMed Web of Science ®Google Scholar
• Kfoury N, Holmes BB, Jiang H, et al. Trans-cellular propagation of Tau aggregation by fibrillar species. J Biol Chem. 2012;287:19440–19451.
   PubMed Web of Science ®Google Scholar
• Nishida N, Harris DA, Vilette D, et al. Successful transmission of three mouse-adapted scrapie strains to murine neuroblastoma cell lines overexpressing wild-type mouse prion protein. J Virol. 2000;74:320–325.
   PubMed Web of Science ®Google Scholar
• Piccardo P, Dlouhy SR, Lievens PM, et al. Phenotypic variability of Gerstmann-Straussler-Scheinker disease is associated with prion protein heterogeneity. J Neuropathol Exp Neurol. 1998;57:979–988.
   PubMed Web of Science ®Google Scholar
• Parchi P, Chen SG, Brown P, et al. Different patterns of truncated prion protein fragments correlate with distinct phenotypes in P102L gerstmann-straussler-scheinker disease. Proc Natl Acad Sci U S A. 1998;95:8322–8327.
   PubMed Web of Science ®Google Scholar
• Tagliavini F, Lievens PM, Tranchant C, et al. A 7-kDa prion protein (PrP) fragment, an integral component of the PrP region required for infectivity, is the major amyloid protein in Gerstmann-Straussler-Scheinker disease A117V. J Biol Chem. 2001;276:6009–6015.
   PubMed Web of Science ®Google Scholar
• Siddiqua A, Margittai M. Three- and four-repeat Tau coassemble into heterogeneous filaments: an implication for Alzheimer disease. J Biol Chem. 2010;285:37920–37926.
   PubMed Web of Science ®Google Scholar
• Schmidt ML, Zhukareva V, Newell KL, et al. Tau isoform profile and phosphorylation state in dementia pugilistica recapitulate Alzheimer’s disease. Acta Neuropathol. 2001;101:518–524.
   PubMed Web of Science ®Google Scholar
• Hong M, Zhukareva V, Vogelsberg-Ragaglia V, et al. Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science. 1998;282:1914–1917.
   PubMed Web of Science ®Google Scholar
• Kovacs GG, Ferrer I, Grinberg LT, et al. Aging-related tau astrogliopathy (ARTAG): harmonized evaluation strategy. Acta Neuropathol. 2016;131:87–102.
   PubMed Web of Science ®Google Scholar
• Braak H, Alafuzoff I, Arzberger T, et al. Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol. 2006;112:389–404.
   PubMed Web of Science ®Google Scholar
• Bouras C, Hof PR, Giannakopoulos P, et al. Regional distribution of neurofibrillary tangles and senile plaques in the cerebral cortex of elderly patients: a quantitative evaluation of a one-year autopsy population from a geriatric hospital. Cereb Cortex. 1994;4:138–150.
   PubMed Web of Science ®Google Scholar
• Uematsu M, Nakamura A, Ebashi M, et al. Brainstem tau pathology in Alzheimer’s disease is characterized by increase of three repeat tau and independent of amyloid beta. Acta Neuropathol Commun. 2018;6:1.
   PubMed Web of Science ®Google Scholar
• Hara M, Hirokawa K, Kamei S, et al. Isoform transition from four-repeat to three-repeat tau underlies dendrosomatic and regional progression of neurofibrillary pathology. Acta Neuropathol. 2013;125:565–579.
   PubMed Web of Science ®Google Scholar
• Nizynski B, Nieznanska H, Dec R, et al. Amyloidogenic cross-seeding of Tau protein: transient emergence of structural variants of fibrils. PLoS One. 2018;13:e0201182.
   PubMed Web of Science ®Google Scholar
• Orru CD, Wilham JM, Hughson AG, et al. Human variant Creutzfeldt-Jakob disease and sheep scrapie PrP(res) detection using seeded conversion of recombinant prion protein. Protein Eng Des Sel. 2009;22:515–521.
   PubMed Web of Science ®Google Scholar
• Atarashi R, Wilham JM, Christensen L, et al. Simplified ultrasensitive prion detection by recombinant PrP conversion with shaking. Nat Methods. 2008;5:211–212.
   PubMed Web of Science ®Google Scholar