Propagation of Tau aggregates Tim Bliss

Molecular Brain

Volumn 10, Issue 1, 2017, Pages

  Goedert, Michel ^a   Spillantini, Maria Grazia ^b  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Alzheimer's disease; Amyloid; Cell to cell spreading; Disease propagation; Prion like; Protein strains; Tau; Tauopathies

Indexed keywords

TAU PROTEIN; ISOPROTEIN; PROTEIN AGGREGATE;

GENE; GENE MUTATION; HUMAN; MAPT GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; REVIEW; TAUOPATHY; ANIMAL; CHEMISTRY; GENETICS; METABOLISM;

ANIMALS; HUMANS; PROTEIN AGGREGATES; PROTEIN ISOFORMS; TAU PROTEINS;

EID: 85020052225     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/s13041-017-0298-7     Document Type: Review

References (82)

1. Goedert M. Alzheimer's and Parkinson's diseases: The prion concept in relation to assembled Aβ, tau and α-synuclein. Science. 2015;349:1255555.
2. Arendt T, Stieler JT, Holzer M. Tau and tauopathies. Brain Res Bull. 2016;126:238-92.
3. Ghetti B, Oblak AL, Boeve BF, Johnson KA, Dickerson BC, Goedert M. Frontotemporal dementia caused by microtubule-associated protein tau gene (MAPT) mutations: A chameleon for neuropathology and neuroimaging. Neuropathol Appl Neurobiol. 2015;41:24-46.
4. Selkoe DJ, Hardy J. The amyloid hypothesis of Alzheimer's disease at 25 years. EMBO Mol Med. 2016;8:595-608.
5. Wilcock GK, Esiri MM. Plaques, tangles and dementia. A quantitative study. J Neurol Sci. 1982;56:343-56.
6. Nelson PT, Alafuzoff I, Bigio EH, Bouras C, Braak H, Cairns NJ, Castellani RJ, Crain BJ, Davies P, Del Tredici K, Duyckaerts C, Frosch MP, Haroutunian V, Hof PR, Hulette CM, Hyman BT, Iwatsubo T, Jellinger KA, Jicha GA, Kövari E, Kukull WA, Leverenz JB, Love S, Mackenzie IR, Mann DM, Masliah E, McKee AC, Montine TJ, Morris JC, Schneider JA, Sonnen JA, Thal DR, Trojanowski JQ, Troncoso JC, Wisniewski T, Woltjer RL, Beach TG. Correlation of Alzheimer disease neuropathologic changes with cognitive status: A review of the literature. J Neuropathol Exp Neurol. 2012;71:362-81.
7. Bondareff W, Mountjoy CQ, Roth M, Hauser DL. Neurofibrillary degeneration and neuronal loss in Alzheimer's disease. Neurobiol Aging. 1989;10:709-15.
8. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science. 1982;216:136-44.
9. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron. 1989;3:519-26.
10. Goedert M, Spillantini MG, Crowther RA. Cloning of a big tau microtubule-associated protein tau characteristic of the peripheral nervous system. Proc Natl Acad Sci U S A. 1992;89:1983-7.
11. Couchie D, Mavilia C, Georgieff IS, Liem RK, Shelanski ML, Nunez J. Primary structure of high molecular weight tau present in the peripheral nervous system. Proc Natl Acad Sci U S A. 1992;89:4378-81.
12. Wang Y, Mandelkow E. Tau in physiology and pathology. Nat Rev Neurosci. 2016;17:5-21.
13. Janning D, Igaev M, Sündermann F, Bruhmann J, Beutel O, Heinisch JJ, Bakota L, Piehler J, Junge W, Brandt R. Single-molecule tracking of tau reveals fast kiss-and-hop interaction with microtubules in living neurons. Mol Biol Cell. 2014;25:3541-51.
14. Niewidok B, Igaev M, Sündermann F, Janning D, Bakota L, Brandt R. Presence of a carboxy-terminal pseudorepeat and disease-like pseudohyperphosphorylation critically influence tau's interaction with microtubules in axon-like processes. Mol Biol Cell. 2016;27:3537-49.
15. Morris M, Knudsen GM, Maeda S, Trinidad JC, Ioanoviciu A, Burlingame AL, Mucke L. Tau post-translational modifications in wild-type and human amyloid precursor protein transgenic mice. Nat Neurosci. 2015;18:1183-9.
16. 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;9:4225-30.
17. Yoshida H, Goedert M. Molecular cloning and functional characterization of chicken brain tau: isoforms with up to five tandem repeats. Biochemistry. 2002;41:15203-11.
18. r 190,000. J Biol Chem. 1990;265:13849-55.
19. Lewis SA, Wang D, Cowan NJ. Microtubule-associated protein MAP2 shares a microtubule binding motif with tau protein. Science. 1988;242:936-9.
20. Sündermann F, Fernandez M-P, Morgan RO. An evolutionary roadmap to the microtubule-associated protein MAP Tau. BMC Genomics. 2016;17:264.
21. Goedert M, Baur CP, Ahringer J, Jakes R, Hasegawa M, Spillantini MG, Smith MJ, Hill F. PTL-1, a microtubule-associated protein with tau-like repeats from the nematode Caenorhabditis elegans. J Cell Sci. 1996;109:2661-72.
22. Heidary G, Fortini ME. Identification and characterization of the Drosophila tau homolog. Mech Dev. 2001;108:171-8.
23. Goedert M, Wischik CM, Crowther RA, Walker JE, Klug A. Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: identification as the microtubule-associated protein tau. Proc Natl Acad Sci U S A. 1988;85:4051-5.
24. Wischik CM, Novak M, Thogersen HC, Edwards PC, Runswick MJ, Jakes R, Walker JE, Milstein C, Roth M, Klug A. Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci U S A. 1988;85:4506-10.
25. Wischik CM, Novak M, Edwards PC, Klug A, Tichelaar W, Crowther RA. Structural characterization of the core of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci U S A. 1988;85:4884-8.
26. Kondo J, Honda T, Mori H, Hamada Y, Miura R, Ogawara M, Ihara Y. The carboxyl third of tau is tightly bound to paired helical filaments. Neuron. 1988;1:827-34.
27. Wegmann S, Medalsy ID, Mandelkow E, Müller DJ. The fuzzy coat of pathological human tau fibrils is a two-layered polyelectrolyte brush. Proc Natl Acad Sci U S A. 2013;110:E313-21.
28. Berriman J, Serpell LC, Oberg KA, Fink AL, Goedert M, Crowther RA. Tau filaments from human brain and from in vitro assembly of recombinant proteins show cross-beta structure. Proc Natl Acad Sci U S A. 2003;100:9034-8.
29. Iqbal K, Liu F, Gong CX. Tau and neurodegenerative disease: The story so far. Nat Rev Neurol. 2016;12:15-27.
30. Arendt T, Stieler J, Strijkstra AM, Hut RA, Rüdiger J, Van der Zee EA, Harkany T, Holzer M, Härtig W. Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J Neurosci. 2003;23:6972-81.
31. Crowther RA. Straight and paired helical filaments in Alzheimer disease have a common structural unit. Proc Natl Acad Sci U S A. 1991;88:2288-92.
32. Crary JF, Trojanowski JQ, Schneider JA, Abisambra JF, Abner EL, Alazuloff I, Arnold SE, Attems J, Beach TG, Bigio EH, Cairns NJ, Dickson DW, Gearing M, Grinberg LT, Hof PR, Hyman BT, Jellinger K, Jicha GA, Kovacs GG, Knopman DS, Kofler J, Kukull WA, Mackenzie IR, Masliah E, McKee A, Montine TJ, Murray ME, Neltner JH, Santa-Maria I, Seeley WW, Serrano-Pozo A, Shelanski ML, Stein T, Takao M, Thal DR, Toledo JB, Troncoso JC, Vonsattel JP, White CL, Wisniewski T, Woltier RL, Yamada M, Nelson PT. Primary age-related tauopathy (PART): A common pathology associated with human aging. Acta Neuropathol. 2014;128:755-66.
33. Duyckaerts C, Braak H, Brion JP, Buée L, Del Tredici K, Goedert M, Halliday G, Neumann M, Spillantini MG, Tolnay M, Uchihara T. PART is part of Alzheimer disease. Acta Neuropathol. 2015;129:749-56.
34. Goedert M, Jakes R, Spillantini MG, Hasegawa M, Smith MJ, Crowther RA. Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature. 1996;383:550-3.
35. Pérez M, Valpuesta JM, Medina M, De Garcini EM, Avila J. Polymerization of tau into filaments in the presence of heparin: The minimal sequence required for tau-tau interaction. J Neurochem. 1996;67:1183-90.
36. Goedert M, Spillantini MG, Cairns NJ, Crowther RA. Tau proteins of Alzheimer paired helical filaments: Abnormal phosphorylation of all six brain isoforms. Neuron. 1992;8:159-68.
37. Von Bergen M, Friedhoff P, Biernat J, Heberle J, Mandelkow EM, Mandelkow E. Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif (306-VQIVYK-311) forming beta structure. Proc Natl Acad Sci U S A. 2000;97:5129-34.
38. Von Bergen M, Barghorn S, Li L, Marx A, Biernat J, Mandelkow EM, Mandelkow E. Mutations of tau protein in frontotemporal dementia promote aggregation of paired helical filaments by enhancing local beta structure. J Biol Chem. 2001;276:48165-74.
39. Sawaya MR, Sambashivan S, Nelson R, Ivanova MI, Sievers SA, Apostol MI, Thompson MJ, Balbirnie M, Wiltzius JJ, McFarlane HT, Madsen AO, Riekel C, Eisenberg D. Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature. 2007;447:453-7.
40. Kadavath H, Jaremko M, Jaremko L, Biernat J, Mandelkow E, Zweckstetter M. Folding of the tau protein on microtubules. Angew Chem Int Ed. 2015;54:10347-51.
41. Xie C, Soeda Y, Shinzaki Y, In Y, Tomoo K, Ihara Y, Miyasaka T. Identification of key amino acids responsible for the distinct aggregation properties of microtubule-associated protein 2 and tau. J Neurochem. 2015;135:19-26.
42. Poorkaj P, Bird TD, Wijsman E, Nemens E, Garruto RM, Anderson L, Andreadis A, Wiederholt WC, Raskind M, Schellenberg GD. Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol. 1998;43:815-25.
43. 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 Graaf E, Wauters E, van Baren J, Hillebrand M, Joosse M, Kwon JM, Nowotny P, Che LK, Norton J, Morris JC, Reed LA, Trojanowski JQ, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd PR, Hayward N, Kwok JBJ, 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. Association of missense and 5′-splice site mutations in tau with the inherited demenmtia FTDP-17. Nature. 1998;393:702-5.
44. Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, Ghetti B. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci U S A. 1998;95:7737-41.
45. Crowther RA, Goedert M. Abnormal tau-containing filaments in neurodegenerative diseases. J Struct Biol. 2000;130:271-9.
46. Iovino M, Agathou S, González-Rueda A, Del Castillo-Herrera M, Borroni B, Alberici A, Lynch T, O'Dowd S, Geti I, Gaffney D, Vallier L, Paulsen O, Káradóttir RT, Spillantini MG. Early maturation and distinct tau pathology in induced pluripotent stem cell-derived neurons from patients with MAPT mutations. Brain. 2015;138:3345-59.
47. Sposito T, Preza E, Mahoney CJ, Setó-Salvia N, Ryan NS, Morris HR, Arber C, Devine MJ, Goulden H, Warner TT, Bushell TJ, Zagnoni M, Kunath T, Livesey FJ, Fox NC, Rossor MN, Hardy J, Wray S. Developmental regulation of tau splicing is disrupted in stem cell-derived neurons from frontotemporal dementia patients with the 10 + 16 splice-site mutation in MAPT. Hum Mol Genet. 2015;24:5260-9.
48. Goedert M, Eisenberg DS, Crowther RA. Propagation of Tau aggregates and neurodegeneration. Annu Rev Neurosci 2017;40:189-210.
49. Stefansson H, Helgason A, Thorleifsson G, Steinthorsdottir V, Masson G, Barnard J, Baker A, Jonasdottir A, Ingason A, Gudnadottir VG, Desnica N, Hicks A, Gylfason A, Gudbjartsson DF, Jonsdottir GM, Sainz J, Agnarsson K, Birgisdottir B, Ghosh S, Olafsdottir A, Cazier JB, Kristjansson K, Frigge ML, Thorgeirsson TE, Gulcher JR, Kong A, Stefansson K. A common inversion under selection in Europeans. Nat Genet. 2005;37:129-37.
50. Zhao Y, Tseng I-C, Heyser CJ, Rockenstein E, Mante M, Adame A, Zheng Q, Huang T, Wang X, Arslan PE, Chakrabarty P, Wu C, Bu G, Mobley WC, Y-w Z, St George-Hyslop P, Masliah E, Fraser PK, Xu H. Appoptosin-mediated caspase cleavage of tau contributes to progressive supranuclear palsy pathogenesis. Neuron. 2015;87:963-75.
51. Höglinger GU, Melhem NM, Dickson DW, Sleiman PM, Wamng LS, Klei L, Rademakers R, de Silva R, Litvan I, Riley DE, van Swieten JC, Heutink P, Wszolek ZK, Uitti RJ, Vandrovcova J, Hurtig HI, Gross RG, Maetzler W, Goldwurm S, Tolosa E, Borroni B, Pastor P, Cantwell LB, Han MR, Dillman A, van der Brug MP, Gibbs JR, Cookson MR, Hernandez DG, Singleton AB, Farrer MJ, Yu CE, Golbe LI, Revesz T, Hardy J, Lees AJ, Devlin B, Hakonarson H, Müller U, Schellenberg GD. Identification of common variants influencing risk of the tauopathy progressive supranuclear palsy. Nat Genet. 2011;43:699-705.
52. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science. 1993;261:921-3.
53. Caffrey TM, Joachim C, Wade-Martins R. Haplotype-specific expression of the N-terminal exon 2 and 3 at the human MAPT locus. Neurobiol Aging. 2008;29:1923-9.
54. Valenca GT, Srivastava GP, Oliveira-Filho J, White CC, Yu L, Schneider JA, Buchman AS, Shulman JM, Bennett DA, Jager PL. The role of MAPT haplotype H2 and isoform 1 N/4R in parkinsonism of older adults. PLoS One. 2016;11:e0157452.
55. Zhong Q, Condon EE, Nagaraja HN, Kuret J. Tau isoform composition influences rate and extent of filament formation. J Biol Chem. 2012;287:20711-9.
56. Kovacs GG, Wöhrer A, Ströbel T, Botond G, Attems J, Budka H. Unclassifiable tauopathy associated with an A152T variation in MAPT exon 7. Clin Neuropathol. 2011;30:3-10.
57. Kara E, Ling H, Pittman AM, Shaw K, de Silva R, Simone R, Holton JL, Warren JD, Rohrer JD, Xiromerisiou G, Lees A, Hardy J, Houlden H, Revesz T. The MAPT p.A152T variant is a risk factor associated with tauopathies with atypical clinical and neuropathological features. Neurobiol Aging. 2012;33:2231.e7-e14.
58. Coppola G, Chinnathambi S, Lee JJ, Dombroski BA, Baker MC, Soto-Ortolazo AI, Lee SE, Klein E, Huang AY, Sears R, Lane JR, Karydas AM, Kenet RO, Biernat J, Wanf L-S, Cotman CW, DeCarli CS, Levey AI, Ringman JM, Mendez MF, Chui HC, Le Ber I, Brice A, Lupton MK, Preza E, Lovestone S, Powell J, Graff-Radford N, Petersen RC, Boeve BF, Lippa CF, Bigio EH, Mackenzie I, Finger E, Kertesz A, Caselli RJ, Gearing M, Juncos JL, Ghetti B, Spina S, Bordelon YM, Tourtelotte WW, Frosch MP, Vonsattel JPG, Zarow C, Beach TG, Albin RL, Lieberman AP, Lee VMY, Trojanowski JQ, Van Deerlin VM, Bird TD, Galasko DR, Masliah E, White CL, Troncoso JC, Hannequin D, Boxer AL, Geschwind MD, Kumar S, Mandelkow EM, Wszolek ZK, Uitti RJ, Dickson DW, Haines JL, Mayeux R, Pericak-Vance MA, Farrer LA, Ross OA, Rademakers R, Schellenberg GD, Miller BL, Mandelkow E, Geschwind DH. Evidence for a role of the rare p.A152T variant in MAPT in increasing the risk for FTD-spectrum and Alzheimer's diseases. Hum Mol Genet. 2012;21:3500-12.
59. Pastor P, Moreno F, Clarimón J, Ruiz A, Combarros O, Calero M, López de Munain A, Bullido MJ, de Pancorbo MM, Carro E, Antonell A, Coto E, Ortega-Cubero S, Hernandez I, Tárraga L, Boada M, Lleó A, Dois-Icardo O, Kulisevsky J, Vázquez-Higuera JL, Infante J, Rábano A, Fernández-Blázquez MA, Valenti M, Indakoetxea B, Barandiarán M, Gorostidin A, Frank-Garcia A, Sastre I, Lorenzo E, Pastor MA, Elcoroaristizabal X, Lennarz M, Maier W, Rámirez A, Serrano-Rios M, Lee SE, Sánchez-Juan P. MAPT H1 haplotype is associated with late-onset Alzheimer's disease risk in APOEϵ4 noncarriers: results from the Dementia Genetics Spanish Consortium. J Alzheimer's Dis. 2016;49:343-52.
60. 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. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol. 2009;11:909-13.
61. Frost B, Jacks RL, Diamond MI. Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem. 2009;284:12845-52.
62. Falcon B, Cavallini A, Angers R, Glover S, Murray TK, Barnham L, Jackson S, O'Neill MJ, Isaacs AM, Hutton ML, Szekeres PG, Goedert M, Bose S. Conformation determines the seeding potencies of native and recombinant tau aggregates. J Biol Chem. 2015;290:1049-65.
63. Holmes BB, DeVos SL, Kfoury N, Li M, Jacks R, Yanamandra K, Ouidja MO, Brodsky FM, Marasa J, Bagchi DP, Kotzbauer PT, Miller TM, Papy-Garcia D, Diamond MI. Heparan sulphate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc Natl Acad Sci U S A. 2013;110:E3138-47.
64. Chai X, Wu S, Murray TK, Kinley R, Cella CV, Sims H, Buckner N, Hanmer J, Davies P, O'Neill MJ, Hutton ML, Citron M. Passive immunization with anti-tau antibodies in two transgenic models. J Biol Chem. 2011;286:34457-67.
65. Yanamandra K, Kfoury N, Jiang H, Mahan TE, Ma S, Maloney SE, Wozniak DF, Diamond MI, Holtzman DM. Anti-tau antibodies that block tau aggregate seeding in vitro markedly decrease pathology and improve cognition in vivo. Neuron. 2013;80:402-14.
66. Sankaranarayanan S, Barten DM, Vana L, Devidze N, Yang L, Cadelina G, Hoque N, DeCarr L, Keenan S, Lin A, Cao Y, Snyder B, Zhang B, Nitla M, Hirschfeld G, Barrezueta N, Polson C, Wes P, Rangan VS, Cacace A, Albright CF, Meredith J, Trojanowski JQ, Lee VMY, Brunden KR, Ahlijanian M. Passive immunization with phosphor-tau antibodies reduces tau pathology and functional deficits in two distinct mouse tauopathy models. PLoS One. 2015;10:e0l25614.
67. DeVos SL, Miller RL, Schoch KM, Holmes BB, Kebodeaux CS, Wegener AJ, Chen G, Shen T, Tran H, Nichols B, Zanardi TA, Kordasiewicz HB, Swayze EE, Bennett CF, Diamond MI, Miller TM. Tau reduction prevents neuronal loss and reverses pathological tau deposition and seeding in mice with tauopathy. Science Transl Med. 2017;9:eaag0481.
68. McEwan WA, Falcon B, Vaysburd M, Clift D, Oblak AL, Ghetti B, Goedert M, James LC. Cytosolic Fc receptor TRIM21 inhibits seeded tau aggregation. Proc Natl Acad Sci U S A. 2017;113:E8187-96.
69. Asai H, Ikezu S, Tsunoda S, Medalla M, Luebke J, Haydar T, Wolozin B, Butovsky O, Kügler S, Ikezu T. Depletion of microglia and inhibition of exosome synthesis halt tau propagation. Nat Neurosci. 2015;18:1584-93.
70. Fontaine SN, Zheng D, Sabbagh JJ, Martin MD, Chaput D, Darling A, Trotter JH, Stothert AR, Nordhues BA, Lussier A, Baker J, Shelton L, Kahn M, Blair LJ, Stevens SM, Dickey CA. DnaJ/Hsc70 chaperone complexes control the extracellular release of neurodegenerative-associated proteins. EMBO J. 2016;35:1537-49.
71. Wu JW, Hussaini SA, Bastille IM, Rodriguez GA, Mrejeru A, Rilett K, Sanders DW, Cook C, Fu H, Boonen RA, Herman M, Nahmani E, Emrani S, Figueroa YH, Diamond MI, Clelland CL, Wray S, Duff KE. Neuronal activity enhances tau propagation and tau pathology in vivo. Nat Neurosci. 2016;19:1085-92.
72. Clavaguera F, Lavenir I, Falcon B, Frank S, Goedert M, Tolnay M. "Prion-like" template misfolding in tauopathies. Brain Pathol. 2013;23:342-9.
73. Iba M, Guo JL, McBride JD, Zhang B, Trojanowski JQ, Lee VMY. Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer's-like tauopathy. J Neurosci. 2013;33:1024-37.
74. Ahmed Z, Cooper J, Murray TK, Garn K, McNaughton E, Clarke H, Parhizkar S, Ward MA, Cavallini A, Jackson S, Bose S, Clavaguera F, Tolnay M, Lavenir I, Goedert M, Hutton ML, O'Neill MJ. A novel in vivo model of tau propagation with rapid and progressive neurofibrillary tangle pathology: The pattern of spread is determined by connectivity, not proximity. Acta Neuropathol. 2014;127:667-83.
75. Clavaguera F, Hench J, Lavenir I, Schweighauser G, Frank S, Goedert M, Tolnay M. Peripheral administration of tau aggregates triggers intracerebral tauopathy in transgenic mice. Acta Neuropathol. 2014;127:299-301.
76. Jackson SJ, Kerridge C, Cooper J, Cavallini A, Falcon B, Cella CV, Landi A, Szekeres PG, Murray TK, Ahmed Z, Goedert M, Hutton M, O'Neill MJ, Bose S. Short fibrils constitute the major species of seed-competent tau in the brains of mice transgenic for human P301S tau. J Neurosci. 2016;36:762-72.
77. Clavaguera F, Akatsu H, Fraser G, Crowther RA, Frank S, Hench J, Probst A, Winkler DT, Reichwald J, Staufenbiel M, Ghetti B, Goedert M, Tolnay M. Brain homogenates from human tauopathies induce tau inclusions in mouse brain. Proc Natl Acad Sci U S A. 2013;110:9535-40.
78. Audouard E, Houben S, Masaracchia C, Yilmaz Z, Suain V, Authelet M, De Decker R, Buée L, Boom A, Leroy K, Ando K, Brion JP. 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;186:2709-22.
79. Guo JL, Narasimhan S, Changolkar L, He Z, Stieber A, Zhang B, Gathagan RJ, Iba M, McBride JD, Trojanowski JQ, Lee VMY. Unique pathological tau conformers from Alzheimer's brains transmit tau pathology in nontransgenic mice. J Exp Med. 2016;213:2635-54.
80. Sanders DW, Kaufman SK, DeVos SL, Sharma AM, Mirhaba H, Li A, Barker SJ, Foley AC, Thorpe JR, Serpell LC, Miller TM, Grinberg LT, Seeley WW, Diamond MI. Distinct tau prion strains propagate in cells and mice and define different tauopathies. Neuron. 2014;82:1271-88.
81. Kaufman SK, Sanders DW, Thomas TL, Ruchinskas AJ, Vaquer-Alicea J, Sharma AM, Miller TM, Diamond MI. Tau prion strains dictate patterns of cell pathology, progression rate, and regional vulnerability in vivo. Neuron. 2016;92:796-812.
82. Woerman AL, Aoyagi A, Patel S, Kazmi SA, Lobach I, Grinberg LT, McKee AC, Seeley WW, Olson SH, Prusiner SB. Tau prions from Alzheimer's disease and chronic traumatic encephalopathy patients propagate in cultured cells. Proc Natl Acad Sci U S A. 2016;113:E8187-96.