Proteopathic Strains and the Heterogeneity of Neurodegenerative Diseases

Annual Review of Genetics

Volumn 50, Issue , 2016, Pages 329-346

  Walker, Lary C ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Amyloid; A ; Parkinson's disease; Prion; Synuclein; Tau

Indexed keywords

AMYLOID BETA PROTEIN; PRION PROTEIN; TAU PROTEIN; MAPT PROTEIN, HUMAN; PRION;

ALZHEIMER DISEASE; CREUTZFELDT JAKOB DISEASE; DEGENERATIVE DISEASE; EPIGENETICS; GENETIC VARIATION; HUMAN; NONHUMAN; PARKINSON DISEASE; PHENOTYPE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; REVIEW; GENETICS; METABOLISM; PATHOLOGY; PRION; PRION DISEASE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; HUMANS; NEURODEGENERATIVE DISEASES; PRION DISEASES; PRIONS; TAU PROTEINS;

EID: 85000733357     PISSN: 00664197     EISSN: 15452948     Source Type: Book Series    
DOI: 10.1146/annurev-genet-120215-034943     Document Type: Review

References (159)

1. Aguzzi A, Polymenidou M. 2004. Mammalian prion biology: one century of evolving concepts. Cell 116:313-27
2. Alpers MP. 2008. The epidemiology of kuru: monitoring the epidemic from its peak to its end. Philos. Trans. R. Soc. Lond. Ser. B 363:3707-13
3. Angers R, Christiansen J, Nalls AV, Kang HE, Hunter N, et al. 2014. Structural effects of PrP polymorphisms on intra-and interspecies prion transmission. PNAS 111:11169-74
4. Asante EA, Smidak M, Grimshaw A, Houghton R, Tomlinson A, et al. 2015. A naturally occurring variant of the human prion protein completely prevents prion disease. Nature 522:478-81
5. Ayers JI, Fromholt S, Koch M, DeBosier A, McMahon B, et al. 2014. Experimental transmissibility of mutant SOD1 motor neuron disease. Acta Neuropathol. 128:791-803
6. Bachevalier J, Landis LS, Walker LC, Brickson M, Mishkin M, et al. 1991. Aged monkeys exhibit behavioral deficits indicative of widespread cerebral dysfunction. Neurobiol. Aging 12:99-111
7. BasunH, BogdanovicN, IngelssonM, AlmkvistO,Naslund J, et al. 2008. Clinical and neuropathological features of the arctic APP gene mutation causing early-onset Alzheimer disease. Arch. Neurol. 65:499-505
8. Benilova I, Gallardo R, Ungureanu AA, Castillo Cano V, Snellinx A, et al. 2014. The Alzheimer disease protective mutation A2T modulates kinetic and thermodynamic properties of amyloid-and beta(A and beta) aggregation. J. Biol. Chem. 289:30977-89
9. Berry DB, Lu D, Geva M, Watts JC, Bhardwaj S, et al. 2013. Drug resistance confounding prion therapeutics. PNAS 110:E4160-69
10. Bierer LM, Hof PR, Purohit DP, Carlin L, Schmeidler J, et al. 1995. Neocortical neurofibrillary tangles correlate with dementia severity in Alzheimer's disease. Arch. Neurol. 52:81-88
11. Boluda S, IbaM,Zhang B, Raible KM,Lee VM,Trojanowski JQ. 2015. 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. 129:221-37
12. BushmanDM, Kaeser GE, Siddoway B, Westra JW, Rivera RR, et al. 2015. Genomicmosaicism with increased amyloid precursor protein (APP) gene copy number in single neurons from sporadic Alzheimer's disease brains. eLife 4:05116
13. Buxbaum JN, Linke RP. 2012. A molecular history of the amyloidoses. J. Mol. Biol. 421:142-59
14. Cancellotti E, Mahal SP, Somerville R, Diack A, Brown D, et al. 2013. Post-translational changes to PrP alter transmissible spongiform encephalopathy strain properties. EMBO J. 32:756-69
15. Castellani RJ, Smith MA. 2011. Compounding artefacts with uncertainty, and an amyloid cascade hypothesis that is "too big to fail." J. Pathol. 224:147-52
16. Chandler RL. 1961. Encephalopathy inmice produced by inoculation with scrapie brain material. Lancet 1:1378-79
17. Chiti F, Dobson CM. 2006. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75:333-66
18. Chouraki V, Seshadri S. 2014. Genetics of Alzheimer's disease. Adv. Genet. 87:245-94
19. Clavaguera F, Hench J,Goedert M, Tolnay M. 2015. Invited review: prion-like transmission and spreading of tau pathology. Neuropathol. Appl. Neurobiol. 41:47-58
20. CohenML, Kim C, Haldiman T, ElHagM,Mehndiratta P, et al. 2015. Rapidly progressive Alzheimer's disease features distinct structures of amyloid-and beta. Brain 138:1009-22
21. Collinge J, Clarke AR. 2007. A general model of prion strains and their pathogenicity. Science 318:930-36
22. Collinge J, Whitfield J, McKintosh E, Frosh A,Mead S, et al. 2008. A clinical study of kuru patients with long incubation periods at the end of the epidemic in Papua New Guinea. Philos. Trans. R. Soc. Lond. Ser. B 363:3725-39
23. Crary JF, Trojanowski JQ, Schneider JA, Abisambra JF, Abner EL, et al. 2014. Primary age-related tauopathy (PART): a common pathology associated with human aging. Acta Neuropathol. 128:755-66
24. Crowell J, Hughson A, Caughey B, Bessen RA. 2015. Host determinants of prion strain diversity independent of prion protein genotype. J. Virol. 89:10427-41
25. Crystal H, Dickson D, Fuld P, Masur D, Scott R, et al. 1988. Clinico-pathologic studies in dementia: nondemented subjects with pathologically confirmed Alzheimer's disease. Neurology 38:1682-87
26. DeArmond SJ, Ironside JW, Bouzamondo-Bernstein E, Peretz D, Fraser JR. 2004. Neuropathology of prion diseases. In Prion Biology and Diseases, ed. SB Prusiner, pp. 777-856. Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press
27. Di Fede G, Catania M, Morbin M, Rossi G, Suardi S, et al. 2009. A recessive mutation in the APP gene with dominant-negative effect on amyloidogenesis. Science 323:1473-77
28. Duncan GW. 2011. The aging brain and neurodegenerative diseases. Clin. Geriatr. Med. 27:629-44
29. Eisele YS, Fritschi SK, Hamaguchi T, Obermuller U, Fuger P, et al. 2014. Multiple factors contribute to the peripheral induction of cerebral β-amyloidosis. J. Neurosci. 34:10264-73
30. Eisele YS, Obermuller U, Heilbronner G, Baumann F, Kaeser SA, et al. 2010. Peripherally applied Aβ-containing inoculates induce cerebral β-amyloidosis. Science 330:980-82
31. Eisenberg D, Jucker M. 2012. The amyloid state of proteins in human diseases. Cell 148:1188-203
32. Fang YS, Tsai KJ, Chang YJ, Kao P, Woods R, et al. 2014. Full-length TDP-43 forms toxic amyloid oligomers that are present in frontotemporal lobar dementia-TDP patients. Nat. Commun. 5:4824
33. Farquhar J, Gajdusek DC. 1981. Kuru: Early Letters and Field Notes from the Collection of D. Carleton Gajdusek. New York: Raven Press
34. Ferreira ST, Lourenco MV, Oliveira MM, De Felice FG. 2015. Soluble amyloid-βoligomers as synaptotoxins leading to cognitive impairment in Alzheimer's disease. Front. Cell. Neurosci. 9:191
35. Frank SA. 2014. Somatic mosaicism and disease. Curr. Biol. 24:R577-81
36. Fritschi SK, Cintron A, Ye L, Mahler J, Buhler A, et al. 2014.Aβseeds resist inactivation by formaldehyde. Acta Neuropathol. 128:477-84
37. Frontzek K, Lutz MI, Aguzzi A, Kovacs GG, BudkaH. 2016. Amyloid-βpathology and cerebral amyloid angiopathy are frequent in iatrogenic Creutzfeldt-Jakob disease after dural grafting. Swiss Med. Wkly. 146:w14287
38. Gajdusek DC, Gibbs CJ, Alpers M. 1966. Experimental transmission of a Kuru-like syndrome to chimpanzees. Nature 209:794-96
39. Gambetti P, Cali I, Notari S, Kong Q, ZouWQ, Surewicz WK. 2011. Molecular biology and pathology of prion strains in sporadic human prion diseases. Acta Neuropathol. 121:79-90
40. Ghaemmaghami S, Watts JC, Nguyen HO, Hayashi S, DeArmond SJ, Prusiner SB. 2011. Conformational transformation and selection of synthetic prion strains. J. Mol. Biol. 413:527-42
41. Ghiso J, Frangione B. 2002. Amyloidosis and Alzheimer's disease. Adv. Drug Deliv. Rev. 54:1539-51
42. Glenner GG,WongCW.1984. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120:885-90
43. Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, et al. 1991. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349:704-6
44. Goedert M. 2015. Alzheimer's and Parkinson's diseases: the prion concept in relation to assembled Aβ, tau, and α-synuclein. Science 349:1255555
45. Goldgaber D, Lerman MI, McBride OW, Saffiotti U, Gajdusek DC. 1987. Characterization and chromosomal localization of a cDNA encoding brain amyloid of Alzheimer's disease. Science 235:877-80
46. Greenwald J, Riek R. 2010. Biology of amyloid: structure, function, and regulation. Structure 18:1244-60
47. Haass C, Kaether C, Thinakaran G, Sisodia S. 2012. Trafficking and proteolytic processing of APP. Cold Spring Harb. Perspect. Med. 2:a006270
48. HaassC, Selkoe DJ. 2007. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide. Nat. Rev. Mol. Cell Biol. 8:101-12
49. HamaguchiT, Eisele YS, Varvel NH, Lamb BT,Walker LC, JuckerM. 2012. The presence of Aβseeds, and not age per se, is critical to the initiation of Aβdeposition in the brain. Acta Neuropathol. 123:31-37
50. HamaguchiT,Taniguchi Y, Sakai K, KitamotoT,Takao M, et al. 2016. Significant association of cadaveric duramater grafting with subpial Aβdeposition and meningeal amyloid angiopathy. Acta Neuropathol. 132:313-15
51. Hardy J. 2006. A hundred years of Alzheimer's disease research. Neuron 52:3-13
52. Hardy J, Selkoe DJ. 2002. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-56
53. Hardy JA, Higgins GA. 1992. Alzheimer's disease: the amyloid cascade hypothesis. Science 256:184-85
54. Heilbronner G, Eisele YS, Langer F, Kaeser SA, Novotny R, et al. 2013. Seeded strain-like transmission of β-amyloid morphotypes in APP transgenic mice. EMBO Rep. 14:1017-22
55. HeuerE,Rosen RF, Cintron A, Walker LC. 2012. Nonhuman primate models of Alzheimer-like cerebral proteopathy. Curr. Pharm. Des. 18:1159-69
56. Hoffner G, Djian P. 2014. Polyglutamine aggregation in Huntington disease: Does structure determine toxicity? Mol. Neurobiol. 52:1297-314
57. Holtzman DM, Morris JC, Goate AM. 2011. Alzheimer's disease: the challenge of the second century. Sci. Trans. Med. 3:77sr1
58. Humphries C, Kohli MA. 2014. Rare variants and transcriptomics in Alzheimer disease. Curr. Genet. Med. Rep. 2:75-84
59. Ikonomovic MD, Abrahamson EE, Price JC,Hamilton RL,Mathis CA, et al. 2012. Early AD pathology in a [C-11]PiB-negative case: a PiB-amyloid imaging, biochemical, and immunohistochemical study. Acta Neuropathol. 123:433-47
60. Imran M, Mahmood S. 2011. An overview of animal prion diseases. Virol. J. 8:493
61. Imran M, Mahmood S. 2011. An overview of human prion diseases. Virol. J. 8:559
62. Ironside JW, Head MW, Bell JE, McCardle L, Will RG. 2000. Laboratory diagnosis of variant Creutzfeldt-Jakob disease. Histopathology 37:1-9
63. Irwin DJ, Abrams JY, Schonberger LB, Leschek EW, Mills JL, et al. 2013. Evaluation of potential infectivity of Alzheimer and Parkinson disease proteins in recipients of cadaver-derived human growth hormone. JAMA Neurol. 70(4):462-68
64. Jack CR Jr., Holtzman DM. 2013. Biomarker modeling of Alzheimer's disease. Neuron 80:1347-58
65. JaunmuktaneZ,Mead S,Ellis M, Wadsworth JD, Nicoll AJ, et al. 2015. Evidence for human transmission of amyloid-βpathology and cerebral amyloid angiopathy. Nature 525(7568):247-50
66. Erratum in Nature 526(7574):595
67. Johnson KA, GregasM, Becker JA, Kinnecom C, Salat DH, et al. 2007. Imaging of amyloid burden and distribution in cerebral amyloid angiopathy. Ann. Neurol. 62:229-34
68. Jonsson T, Atwal JK, Steinberg S, Snaedal J, Jonsson PV, et al. 2012. A mutation in APP protects against Alzheimer's disease and age-related cognitive decline. Nature 488:96-99
69. Jucker M, Walker LC. 2013. Self-propagation of pathogenic protein aggregates in neurodegenerative diseases. Nature 501:45-51
70. Jucker M, Walker LC. 2015. Neurodegeneration: amyloid-β pathology induced in humans. Nature 525(7568):193-94
71. Kalimo H, Lalowski M, Bogdanovic N, Philipson O, Bird TD, et al. 2013. The Arctic AβPP mutation leads to Alzheimer's disease pathology with highly variable topographic deposition of differentially truncated A and beta. Acta Neuropathol. Commun. 1:60
72. Kane MD, Lipinski WJ, Callahan MJ, Bian F, Durham RA, et al. 2000. Evidence for seeding of β-amyloid by intracerebral infusion of Alzheimer brain extracts in β-amyloid precursor protein-transgenic mice. J. Neurosci. 20:3606-11
73. Kang J, Lemaire HG, Unterbeck A, Salbaum JM, Masters CL, et al. 1987. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 325:733-36
74. Klunk WE, Engler H, Nordberg A, Wang Y, Blomqvist G, et al. 2004. Imaging brain amyloid in Alzheimer's disease with Pittsburgh compound-B. Ann. Neurol. 55:306-19
75. Klunk WE, Lopresti BJ, Ikonomovic MD, Lefterov IM, Koldamova RP, et al. 2005. Binding of the positron emission tomography tracer Pittsburgh compound-B reflects the amount of amyloid-β in Alzheimer's disease brain but not in transgenic mouse brain. J. Neurosci. 25:10598-606
76. Knowles TP, Vendruscolo M, Dobson CM. 2014. The amyloid state and its association with protein misfolding diseases.Nat. Rev. Mol. Cell Biol. 15:384-96
77. Kovacs GG. 2015. Invited review: Neuropathology of tauopathies: principles and practice. Neuropathol. Appl. Neurobiol. 41:3-23
78. Kovacs GG, Lutz MI, Ricken G, Ströbel T, Höftberger R, et al. 2016. Dura mater is a potential source of Aβseeds. Acta Neuropathol. 131(6):911-23
79. Lardenoije R, Iatrou A, Kenis G, Kompotis K, Steinbusch HW, et al. 2015. The epigenetics of aging and neurodegeneration. Prog. Neurobiol. 131:21-64
80. Lee VM. 2001. Biomedicine. Tauists and β-aptists united-well almost! Science 293:1446-47
81. Levine H,Walker LC. 2010. Molecular polymorphism of Aβin Alzheimer's disease. Neurobiol. Aging 31:542-48
82. Levy E, Carman MD, Fernandez-Madrid IJ, Power MD, Lieberburg I, et al. 1990. Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type. Science 248:1124-26
83. Li J, Browning S, Mahal SP, Oelschlegel AM, Weissmann C. 2010. Darwinian evolution of prions in cell culture. Science 327:869-72
84. Liu CC, Kanekiyo T, Xu H, Bu G. 2013. Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy. Nat. Rev. Neurol. 9:106-18
85. Liu P, Reed MN, Kotilinek LA, GrantMK, Forster CL, et al. 2015. Quaternary structure defines a large class of amyloid-βoligomers neutralized by sequestration. Cell Rep. 11:1760-71
86. Lu JX, Qiang W, Yau WM, Schwieters CD, Meredith SC, Tycko R. 2013. Molecular structure of β-amyloid fibrils in Alzheimer's disease brain tissue. Cell 154:1257-68
87. Maat-Schieman M, Roos R, van Duinen S. 2005. Hereditary cerebral hemorrhage with amyloidosis-Dutch type. Neuropathology 25:288-97
88. Magnusson K, Simon R, Sjolander D, Sigurdson CJ, Hammarstrom P, Nilsson KP. 2014. Multimodal fluorescencemicroscopy of prion strain specific PrP deposits stained by thiophene-based amyloid ligands. Prion 8:319-29
89. MastersCL, Simms G, WeinmanNA, Multhaup G, McDonald BL, Beyreuther K. 1985. Amyloid plaque core protein in Alzheimer disease and Down syndrome. PNAS 82:4245-49
90. McKintosh E, Tabrizi SJ, Collinge J. 2003. Prion diseases. J. Neurovirol. 9:183-93
91. Mead S, Reilly MM. 2015. A new prion disease: relationship with central and peripheral amyloidoses. Nat. Rev. Neurol. 11:90-97
92. Meinhardt J, Sachse C, Hortschansky P, Grigorieff N, Fandrich M. 2009. Aβ(1-40) fibril polymorphism implies diverse interaction patterns in amyloid fibrils. J. Mol. Biol. 386:869-77
93. Melki R. 2015. Role of different α-synuclein strains in synucleinopathies, similarities with other neurodegenerative diseases. J. Parkinson's Dis. 5:217-27
94. Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, et al. 2006. Exogenous induction of cerebral β-amyloidogenesis is governed by agent and host. Science 313:1781-84
95. Meyer-Luehmann M, Spires-Jones TL, Prada C, Garcia-Alloza M, de Calignon A, et al. 2008. Rapid appearance and local toxicity of amyloid-β plaques in a mouse model of Alzheimer's disease. Nature 451:720-24
96. Nelson PT, Alafuzoff I, Bigio EH, Bouras C, Braak H, et al. 2012. Correlation of Alzheimer disease neuropathologic changes with cognitive status: a review of the literature. J. Neuropathol. Exp. Neurol. 71:362-81
97. Nilsson KP, Aslund A, Berg I, Nystrom S, Konradsson P, et al. 2007. Imaging distinct conformational states of amyloid-βfibrils in Alzheimer's disease using novel luminescent probes. ACS Chem. Biol. 2:553-60
98. Paravastu AK, Leapman RD, YauWM, Tycko R. 2008. Molecular structural basis for polymorphism in Alzheimer's β-amyloid fibrils. PNAS 105:18349-54
99. Parchi P, Saverioni D. 2012. Molecular pathology, classification, and diagnosis of sporadic human prion disease variants. Folia Neuropathol. 50:20-45
100. Pattison IH. 1972. Scrapie: a personal view. J. Clin. Pathol. Suppl. (R. Coll. Pathol) 6:110-14
101. Pattison IH, Millson GC. 1961. Scrapie produced experimentally in goats with special reference to the clinical syndrome. J. Comp. Pathol. 71:101-9
102. Pedersen JS, Otzen DE. 2008. Amyloid-A state in many guises: survival of the fittest fibril fold. Protein Sci. 17:2-10
103. PeelaertsW, Bousset L, Van der Perren A,Moskalyuk A, Pulizzi R, et al. 2015. Synuclein strains cause distinct synucleinopathies after local and systemic administration. Nature 522:340-44
104. Peretz D, WilliamsonRA, LegnameG,Matsunaga Y, Vergara J, et al. 2002.Achange in the conformation of prions accompanies the emergence of a new prion strain. Neuron 34:921-32
105. Petkova AT, LeapmanRD, Guo Z, YauWM,Mattson MP, Tycko R. 2005. Self-propagating,molecularlevel polymorphism in Alzheimer's β-amyloid fibrils. Science 307:262-65
106. Phinney AL, Deller T, Stalder M, Calhoun ME, Frotscher M, et al. 1999. Cerebral amyloid induces aberrant axonal sprouting and ectopic terminal formation in amyloid precursor protein transgenic mice. J. Neurosci. 19:8552-59
107. Piccini A, Russo C, Gliozzi A, Relini A, Vitali A, et al. 2005. Amyloid is different in normal aging and in Alzheimer disease. J. Biol. Chem. 34:186-92
108. Portelius E, BogdanovicN,GustavssonMK, Volkmann I, Brinkmalm G, et al. 2010. Mass spectrometric characterization of brain amyloid βisoform signatures in familial and sporadic Alzheimer's disease. Acta Neuropathol. 120:185-93
109. Portelius E, Lashley T, Westerlund A, Persson R, Fox NC, et al. 2015. Brain amyloid-βfragment signatures in pathological ageing and Alzheimer's disease by hybrid immunoprecipitation mass spectrometry. Neurodegener. Dis. 15:50-57
110. Potter H, Wisniewski T. 2012. Apolipoprotein E: essential catalyst of the Alzheimer amyloid cascade. Int. J. Alzheimers Dis. 2012:489428
111. Prusiner SB. 1998. Prions. PNAS 95:13363-83
112. Prusiner SB. 2013. Biology and genetics of prions causing neurodegeneration. Annu. Rev. Genet. 47:601-23
113. Puchtler H, Sweat F. 1966. A review of early concepts of amyloid in context with contemporary chemical literature from 1839 to 1859. J. Histochem. Cytochem. 14:123-34
114. Radde R, Bolmont T, Kaeser SA, Coomaraswamy J, Lindau D, et al. 2006. Aβ42-driven cerebral amyloidosis in transgenic mice reveals early and robust pathology. EMBO Rep. 7:940-46
115. Reitz C, Brayne C, Mayeux R. 2011. Epidemiology of Alzheimer disease. Nat. Rev. Neurol. 7:137-52
116. Requena JR,Wille H. 2014. The structure of the infectious prion protein: experimental data and molecular models. Prion 8:60-66
117. Resnick SM, Bilgel M, Moghekar A, An Y, Cai Q, et al. 2015. Changes in Aβbiomarkers and associations with APOE genotype in 2 longitudinal cohorts. Neurobiol. Aging 36:2333-39
118. Revesz T, Ghiso J, Lashley T, Plant G, Rostagno A, et al. 2003. Cerebral amyloid angiopathies: a pathologic, biochemical, and genetic view. J. Neuropathol. Exp. Neurol. 62:885-98
119. Roberts HL, Brown DR. 2015. Seeking a mechanism for the toxicity of oligomeric α-synuclein. Biomolecules 5:282-305
120. Robinson JL, Geser F, Stieber A, Umoh M, Kwong LK, et al. 2013. TDP-43 skeins show properties of amyloid in a subset of ALS cases. Acta Neuropathol. 125:121-31
121. Rodriguez JA, Ivanova MI, Sawaya MR, Cascio D, Reyes FE, et al. 2015. Structure of the toxic core of α-synuclein from invisible crystals. Nature 525:486-90
122. Rosen RF, Ciliax BJ,Wingo TS, Gearing M, Dooyema J, et al. 2010. Deficient high-affinity binding of Pittsburgh compound B in a case of Alzheimer's disease. Acta Neuropathol. 119:221-33
123. Rosen RF, Tomidokoro Y, Farberg AS, Dooyema J, Ciliax B, et al. 2016. Comparative pathobiology of β-amyloid and the unique susceptibility of humans to Alzheimer's disease. Neurobiol. Aging 44:185-96
124. Rosen RF, Walker LC, Levine H. 2011. PIB binding in aged primate brain: enrichment of highaffinity sites in humans with Alzheimer's disease. Neurobiol. Aging 32:223-34
125. Safar J,Wille H, Itri V, Groth D, Serban H, et al. 1998. Eight prion strains have PrPSc molecules with different conformations. Nat. Med. 4:1157-65
126. Safar JG, Xiao X, Kabir ME, Chen S, Kim C, et al. 2015. Structural determinants of phenotypic diversity and replication rate of human prions. PLOS Pathog. 11:e1004832
127. Sanders DW, Kaufman SK, Holmes BB, DiamondMI. 2016. Prions and protein assemblies that convey biological information in health and disease. Neuron 89:433-48
128. Selkoe DJ. 1999. Biology of β-amyloid precursor protein and the mechanism of Alzheimer disease. In AlzheimerDisease, ed.RDTerry,RKatzman,KL Bick, SS Sisodia, pp. 293-310. Philadelphia: Lippincott, Williams, andWilkins
129. Selkoe DJ. 2011. Resolving controversies on the path to Alzheimer's therapeutics. Nat.Med. 17:1060-65
130. Sipe JD, Benson MD, Buxbaum JN, Ikeda S, Merlini G, et al. 2014. Nomenclature 2014: amyloid fibril proteins and clinical classification of the amyloidosis. Amyloid 21:221-24
131. Sipe JD, Cohen AS. 2000. Review: history of the amyloid fibril. J. Struct. Biol. 130:88-98
132. Smethurst P, Sidle KC, Hardy J. 2015. Review: Prion-like mechanisms of transactive response DNA binding protein of 43 kDa (TDP-43) in amyotrophic lateral sclerosis (ALS). Neuropathol. Appl. Neurobiol. 41:578-97
133. Spillantini MG, Goedert M. 2013. Tau pathology and neurodegeneration. Lancet Neurol. 12:609-22
134. Spirig T, Ovchinnikova O, Vagt T, Glockshuber R. 2014. Direct evidence for self-propagation of different amyloid-βfibril conformations. Neurodegener. Dis. 14:151-59
135. Stohr J, Condello C, Watts JC, Bloch L, Oehler A, et al. 2014. Distinct synthetic Aβ prion strains producing different amyloid deposits in bigenic mice. PNAS 111:10329-34
136. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, et al. 1997. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. PNAS 94:13287-92
137. Surmacz-Chwedoruk W, Nieznanska H, Wojcik S, Dzwolak W. 2012. Cross-seeding of fibrils from two types of insulin induces new amyloid strains. Biochemistry 51:9460-69
138. Tanaka M, Collins SR, Toyama BH,Weissman JS. 2006. The physical basis of how prion conformations determine strain phenotypes. Nature 442:585-89
139. Taniguchi-Watanabe S, Arai T, Kametani F, Nonaka T, Masuda-Suzukake M, et al. 2015. Biochemical classification of tauopathies by immunoblot, protein sequence and mass spectrometric analyses of sarkosyl-insoluble and trypsin-resistant tau. Acta Neuropathol. 131:267-80
140. Tanzi RE. 2012. The genetics of Alzheimer disease. Cold Spring Harb. Perspect. Med. 2:a006296
141. Tanzi RE, Gusella JF, Watkins PC, Bruns GA, St George-Hyslop P, et al. 1987. Amyloid β protein gene: cDNA, mRNA distribution, and genetic linkage near the Alzheimer locus. Science 235:880-84
142. Tycko R. 2014. Physical and structural basis for polymorphism in amyloid fibrils. Protein Sci. 23:1528-39
143. Tycko R. 2015. Amyloid polymorphism: structural basis and neurobiological relevance. Neuron 86:632-45
144. Van Broeckhoven C, Haan J, Bakker E,Hardy JA, Van HulW, et al. 1990. Amyloid βprotein precursor gene and hereditary cerebral hemorrhage with amyloidosis (Dutch). Science 248:1120-22
145. Vasconcelos B, Stancu IC, Buist A, Bird M, Wang P, et al. 2016. Heterotypic seeding ofTau fibrillization by pre-aggregated Aβ provides potent seeds for prion-like seeding and propagation of Tau-pathology in vivo. Acta Neuropathol. 131:549-69
146. Walker L, Levine H, Jucker M. 2006. Koch's postulates and infectious proteins. Acta Neuropathol. 112:1-4
147. Walker LC, Jucker M. 2015. Neurodegenerative diseases: expanding the prion concept. Annu. Rev. Neurosci. 38:87-103
148. Walker LC, Pahnke J, Madauss M, Vogelgesang S, Pahnke A, et al. 2000. Apolipoprotein E4 promotes the early deposition of Aβ42 and then Aβ40 in the elderly. Acta Neuropathol. 100:36-42
149. Warzok RW, Kessler C, Apel G, Schwarz A, Egensperger R, et al. 1998. Apolipoprotein E4 promotes incipient Alzheimer pathology in the elderly. Alzheimer Dis. Assoc. Disord. 12:33-39
150. Watts JC, Condello C, Stohr J, Oehler A, Lee J, et al. 2014. Serial propagation of distinct strains of Aβ prions from Alzheimer's disease patients. PNAS 111:10323-28
151. Weissmann C. 2004. The state of the prion. Nat. Rev. Microbiol. 2:861-71
152. Weissmann C. 2012. Mutation and selection of prions. PLOS Pathog. 8:e1002582
153. Westermark GT, Fandrich M, Westermark P. 2015. AA amyloidosis: pathogenesis and targeted therapy. Annu. Rev. Pathol. 10:321-44
154. Whitfield JT, PakoWH, Collinge J, Alpers MP. 2008. Mortuary rites of the South Fore and kuru. Philos. Trans. R. Soc. Lond. Ser. B 363:3721-24
155. Will RG, Ironside JW, Zeidler M, Cousens SN, Estibeiro K, et al. 1996. A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347:921-25
156. WingoTS, Lah JJ, Levey AI, Cutler DJ. 2012. Autosomal recessive causes likely in early-onset Alzheimer disease. Arch Neurol. 69(1):59-64
157. Ye L, Fritschi SK, Schelle J, Obermuller U, Degenhardt K, et al. 2015. Persistence of Aβseeds in APP null mouse brain. Nat. Neurosci. 18:1559-61
158. Ye L, Hamaguchi T, Fritschi SK, Eisele YS, Obermuller U, et al. 2015. Progression of seed-induced Aβ deposition within the limbic connectome. Brain Pathol. 25:743-52
159. Yu JT, Tan L, Hardy J. 2014. Apolipoprotein E in Alzheimer's disease: an update. Annu. Rev. Neurosci. 37:79-100