Computational modeling of the relationship between amyloid and disease

Biophysical Reviews

Volumn 4, Issue 3, 2012, Pages 205-222

  Hall, Damien ^a   Edskes, Herman ^b  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Alzheimer's; Amyloid; Amyloidosis; Computational modeling; Diabetes; Simulation; Yeast prions

Indexed keywords

EID: 84873120108     PISSN: 18672450     EISSN: 18672469     Source Type: Journal    
DOI: 10.1007/s12551-012-0091-x     Document Type: Review

References (143)

1. Abeln S, Frenkel D (2008) Disordered flanks prevent peptide aggregation. PLoS Comput Biol 4: e1000241.
2. Ban T, Hamada D, Hasegawa K, Naiki H, Goto Y (2003) Directobservation of amyloid fibril growth monitored by thioflavin Tfluorescence. J Biol Chem 278: 16462-16465.
3. Baxa U (2008) Structural basis of infectious and non-infectious amyloids. Curr Alzheimer Res 5: 308-318.
4. Bennhold H (1922) Eine spezifische amyloidfärbung mit Kongorot [Specific staining of amyloid with Congo red]. Münch Med Wochenschr 69: 1537-1538, as cited by Steensma (2001) page 252.
5. Bernacki JP, Murphy RM (2009) Model discrimination and mechanistic interpretation of kinetic data in protein aggregation studies. Biophys J 96: 2871-2887.
6. Biewend ML, Menke DM, Calamia KT (2006) The spectrum of localized amyloidosis: a case series of 20 patients and review of the literature. Amyloid 13: 135-142.
7. Binger KJ, Pham CL, Wilson LM, Bailey MF, Lawrence LJ, Schuck P, Howlett GJ (2008) Apolipoprotein C-II amyloid fibrils assemble via a reversible pathway that includes fibril breaking and rejoining. J Mol Biol 376: 1116-1129.
8. Bush AI (2003) The metallobiology of Alzheimer's disease. Trends Neurosci 26: 207-214.
9. Caflisch A (2006) Computational models for the prediction of polypeptide aggregation propensity. Curr Opin Chem Biol 10: 437-444.
10. Carulla N, Caddy GL, Hall DR, Zurdo J, Gairí M, Feliz M, Giralt E, Robinson CV, Dobson CM (2005) Molecular recycling within amyloid fibrils. Nature 436: 554-558.
11. Chamberlain AK, MacPhee CE, Zurdo J, Morozova-Roche LA, Hill HA, Dobson CM, Davis JJ (2000) Ultrastructural organization of amyloid fibrils by atomic force microscopy. Biophys J 79: 3282-3293.
12. Cohen AS, Calkins E (1959) Electron microscopic observation on a fibrous component in a amyloid of diverse origins. Nature 183: 1202-1203.
13. Cohen SI, Vendruscolo M, Dobson CM, Knowles TP (2011) Nucleated polymerization with secondary pathways. III. Equilibrium behavior and oligomer populations. J Chem Phys 135: 065107.
14. Collinge J, Clarke AR (2007) A general model of prion strains and their pathogenicity. Science 318: 930-936.
15. Connelly L, Jang H, Arce FT, Capone R, Kotler SA, Ramachandran S, Kagan BL, Nussinov R, Lal R (2012) Atomic force microscopy and MD simulations reveal pore-like structures of all-D-enantiomer of Alzheimer's β-amyloid peptide: relevance to the ion channel mechanism of AD pathology. J Phys Chem B 116: 1728-1735.
16. Craft DL, Wein LM, Selkoe DJ (2002) A mathematical model of the impact of novel treatments on the A beta burden in the Alzheimer's brain, CSF and plasma. Bull Math Biol 64: 1011-1031.
17. Csermely P (2001) Chaperone overload is a possible contributor to 'civilization diseases'. Trends Genet 17: 701-704.
18. Cuille J, Chelle PL (1939) Experimental transmission of trembling to the goat. C R Seances Acad Sci 208: 1058-1060.
19. Derkatch IL, Chernoff YO, Kushnirov VV, Inge-Vechtomov SG, Liebman SW (1996) Genesis and variability of [PSI] prion factors in Saccharomyces cerevisiae. Genetics 144: 1375-1386.
20. Dobson CM (2001) The structural basis of protein folding and its links with human disease. Philos Trans R Soc Lond B 356(1406): 133-145.
21. Eanes ED, Glenner GG (1968) X-ray diffraction studies on amyloid filaments. J Histochem Cytochem 16: 673-677.
22. Edelstein-Keshet L (2006) Mathematical models in biology, SIAM, Philadelphia.
23. Eisenberg D, Jucker M (2012) The amyloid state of proteins in human diseases. Cell 148: 1188-1203.
24. Esler WP, Stimson ER, Jennings JM, Vinters HV, Ghilardi JR, Lee JP, Mantyh PW, Maggio JE (2000) Alzheimer's disease amyloid propagation by a template-dependent dock-lock mechanism. Biochemistry 39: 6288-6295.
25. Fändrich M (2007)On the structural definition of amyloid fibrils and other polypeptide aggregates. Cell Mol Life Sci 64: 2066-2078.
26. Foderà V, Donald AM (2010) Tracking the heterogeneous distribution of amyloid spherulites and their population balance with free fibrils. Eur Phys J E Soft Matter 33: 273-282.
27. Friedman R (2011) Aggregation of amyloids in a cellular context: modeling and experiment. Biochem J 438: 415-426.
28. Ghosh P, Kumar A, Datta B, Rangachari V (2010) Dynamics of protofibril elongation and association involved in Aβ42 peptide aggregation in Alzheimer's disease. BMC Bioinforma 6: S24.
29. Gibbs CJ Jr, Amyx HL, Bacote A, Masters CL, Gajdusek DC (1980) Oral transmission of kuru, Creutzfeldt-Jacob disease and scrapie to nonhuman primates. J Infect Dis 142: 205-208.
30. Gillmore JD, Tennent GA, Hutchinson WL, Gallimore JR, Lachmann HJ, Goodman HJ, Offer M, Millar DJ, Petrie A, Hawkins PN, Pepys MB (2010) Sustained pharmacological depletion of serum amyloid P component in patients with systemic amyloidosis. Br J Haematol 148: 760-767.
31. Glabe CG (2006) Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol Aging 27: 570-575.
32. Glenner GG (1980) Amyloid deposits and amyloidosis. (Part 1). N Engl J Med 302: 1283-1292.
33. Glenner GG, Wong CW (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 122: 1131-1135.
34. Hall D (2003) The effects of Tubulin denaturation on the characterization of its polymerization behavior. Biophys Chem 104: 655-682.
35. Hall CK (2008) Thermodynamic and kinetic origins of alzheimer's and related diseases: a chemical engineer's perspective. AICHE J 54: 1956-1962.
36. Hall D (2012) Semi-automated methods for simulation and measurement of amyloid fiber distributions obtained from transmission electron microscopy experiments. Anal Biochem 421: 262-277.
37. Hall D, Edskes H (2004) Silent prions lying in wait: a two-hit model of prion/amyloid formation and infection. J Mol Biol 336: 775-786.
38. Hall D, Edskes H (2009) A model of amyloid's role in disease based on fibril fracture. Biophys Chem 145: 17-28.
39. Hall D, Hirota N (2008) Multi-scale modelling of amyloid formation from unfolded proteins using a set of theory derived rate constants. Biophys Chem 140: 122-128.
40. Hall D, Minton AP (2002) Effects of inert volume-excluding macromolecules on protein fiber formation. I. Equilibrium models. Biophys Chem 98: 93-104.
41. Hall D, Minton AP (2004) Effects of inert volume-excluding macromolecules on protein fiber formation. II. Kinetic models for nucleated fiber growth. Biophys Chem 107: 299-316.
42. Hall D, Hirota N, Dobson CM (2005) A toy model for predicting the rate of amyloid formation from unfolded protein. J Mol Biol 351: 195-205.
43. Harris H, Rubinsztein DC (2012) Control of autophagy as a therapy for neurodegenerative disease. Nat Rev Neurol 8: 108-117.
44. Hawkins PN, Myers MJ, Epenetos AA, Caspi D, Pepys MB (1988) Specific localization and imaging of amyloid deposits in vivo using 123I-labeled serum amyloid P component. J Exp Med 167: 903-913.
45. Higuchi M, Iwata N, Matsuba Y, Sato K, Sasamoto K, Saido TC (2005) 19F and 1H MRI detection of amyloid beta plaques in vivo. Nat Neurosci 8: 527-533.
46. Hope J, Shearman MS, Baxter HC, Chong A, Kelly SM, Price NC (1996) Cytotoxicity of prion protein peptide (PrP106-126) differs in mechanism from the cytotoxic activity of the Alzheimer's disease amyloid peptide, A beta 25-35. Neurodegeneration 5: 1-11.
47. Howard S, Jagannathan J, Krajewski K, Giardino A, Zukotynski K, O'Regan K, Ghobrial I, Ramaiya N (2012) Multimodality imaging in amyloidosis. Cancer Imaging 12: 109-117.
48. Iwata K, Fujiwara T, Matsuki Y, Akutsu H, Takahashi S, Naiki H, Goto Y (2006) 3D structure of amyloid protofilaments of beta-2-microglobulin fragment probed by solid-state NMR. Proc Natl Acad Sci USA 103: 18119-18124.
49. Jahn TR, Makin OS, Morris KL, Marshall KE, Tian P, Sikorski P, Serpell LC (2010) The common architecture of cross-beta amyloid. J Mol Biol 395: 717-727.
50. Jarrett JT, Lansbury PT Jr (1993) Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73: 1055-1058.
51. Jimenez JL, Tennent G, Pepys M, Saibil HR (2001) Structural diversity of ex vivo amyloid fibrils studied by cryo-electron microscopy. J Mol Biol 311: 241-247.
52. Jones M, Wight D, Barron R, Jeffrey M, Manson J, Prowse C, Ironside JW, Head MW (2009) Molecular model of prion transmission to humans. Emerg Infect Dis 15: 2013-2016.
53. Jucker M, Walker LC (2011) Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders. Ann Neurol 70: 532-540.
54. Kayed R, Lasagna-Reeves C (2012) Molecular mechanisms of amyloid oligomers toxicity. J Alzheimer's Dis. doi: 10. 3233/JAD-2012-129001.
55. King CY, Diaz-Avalos R (2004) Protein-only transmission of three yeast prion strains. Nature 428: 319-323.
56. Klein WL (2006) Synaptic targeting by A beta oligomers (ADDLS) as a basis for memory loss in early Alzheimer's disease. Alzheimers Dement 2: 43-55.
57. Klunk WL (2011) Amyloid imaging as a biomarker for cerebral beta-amyloidosis and risk prediction for Alzheimer dementia. Neurobiol Aging 32: S20-S36.
58. Knudson AG Jr (1971) Mutation and cancer: statistical study of retinoblastoma. Proc Natl Acad Sci USA 68: 820-823.
59. Koyama J, Ray-Sequin PA, Falk RH (2002) Prognostic significance of ultrasound myocardial tissue characterization in patients with cardiac amyloidosis. Circulation 106: 556-561.
60. Krebs MR, Domike KR, Donald AM (2009) Protein aggregation: more than just fibrils. Biochem Soc Trans 37: 682-686.
61. Kuner P, Bohrmann B, Tjernberg LO, Näslund J, Huber G, Celenk S, Grüninger-Leitch F, Richards JG, Jakob-Roetne R, Kemp JA, Nordstedt C (2000) Controlling polymerization of beta-amyloid and prion-derived peptides with synthetic small molecule ligands. J Biol Chem 275: 1673-1678.
62. Kyle RA, Bayrd ED (1975) Amyloidosis: review of 236 cases. Medicine 54: 271-299.
63. Lansbury PT, Lashuel HA (2006) A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature 443: 774-779.
64. Lashuel HA, Lansbury PT Jr (2006) Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? Q Rev Biophys 39: 167-201.
65. Lee CC, Nayak A, Sethuraman A, Belfort G, McRae GJ (2007) A three-stage kinetic model of amyloid fibrillation. Biophys J 92: 3448-3458.
66. Lee YJ, Savtchenko R, Ostapchenko VG, Makarava N, Baskakov IV (2011) Molecular structure of amyloid fibrils controls the relationship between fibrillar size and toxicity. PLoS One 6: e20244.
67. Leliveld SR, Korth C (2007) The use of conformation-specific ligands and assays to dissect the molecular mechanisms of neurodegenerative diseases. J Neurosci Res 85: 2285-2297.
68. Levine H 3rd, Walker LC (2010) Molecular polymorphism of Abeta in Alzheimer's disease. Neurobiol Aging 31: 542-548.
69. Liang FC, Chen RP, Lin CC, Huang KT, Chan SI (2006) Tuning the conformation properties of a peptide by glycosylation and phosphorylation. Biochem Biophys Res Commun 342: 482-488.
70. Liberski P, Streichenberger N, Giraud P, Soutrenon M, Meyronnet D, Sikorska B, Kopp N (2005) Ultrastructural pathology of prion diseases revisited: brain biopsy studies. Neuropathol Appl Neurobiol 31: 88-96.
71. Linse S, Cabaleiro-Lago C, Xue WF, Lynch I, Lindman S, Thulin E, Radford SE, Dawson KA (2007) Nucleation of protein fibrillation by nanoparticles. Proc Natl Acad Sci USA 104: 8691-8696.
72. Lomakin A, Chung DS, Benedek GB, Kirschner DA, Teplow DB (1996) On the nucleation and growth of amyloid beta-protein fibrils: detection of nuclei and quantitation of rate constants. Proc Natl Acad Sci USA 93: 1125-1129.
73. Maggio JE, Mantyh PW (1996)Brain amyloid--a physicochemical perspective. Brain Pathol 6: 147-162.
74. Marsh RF, Bessen RA (1994) Physicochemical and biological characterizations of distinct strains of the transmissible mink encephalopathy agent. Philos Trans R Soc Lond B 343: 413-414.
75. Masel J, Jansen VA, Nowak MA (1999) Quantifying the kinetics of prion replication. Biophys Chem 77: 139-152.
76. Matthäus F (2006) Diffusion versus network models as descriptions for the spread of prion diseases in the brain. J Theor Biol 240: 104-113.
77. McGlinchey RP, Kryndushkin D, Wickner RB (2011) Suicidal [PSI+] is a lethal yeast prion. Proc Natl Acad Sci USA 108: 5337-5341.
78. Merlini G, Bellotti V (2003) Molecular mechanisms of amyloidosis. N Engl J Med 349: 583-596.
79. Mishra R, Sjölander D, Hammarström P (2011) Spectroscopic characterization of diverse amyloid fibrils in vitro by the fluorescent dye Nile red. Mol Biosyst 7: 1232-1240.
80. Mold C, Gresham HD, Du Clos TW (2001) Serum amyloid P component and C-reactive protein mediate phagocytosis through murine Fc gamma Rs. J Immunol 166: 1200-1205.
81. Moreno-Gonzalez I, Soto C (2010) Misfolded protein aggregates: mechanisms, structures and potential for disease transmission. Semin Cell Dev Biol 22(2011): 482-487.
82. Morinaga A, Hasegawa K, Nomura R, Ookoshi T, Ozawa D, Goto Y, Yamada M, Naiki H (2010) Critical role of interfaces and agitation on the nucleation of Abeta amyloid fibrils at low concentrations of Abeta monomers. Biochim Biophys Acta 1804: 986-995.
83. Morris AM, Watzky MA, Finke RG (2009) Protein aggregation kinetics, mechanism, and curve-fitting: a review of the literature. Biochim Biophys Acta 1794: 375-397.
84. Naiki H, Higuchi K, Hosokawa M, Takeda T (1989) Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1. Anal Biochem 177: 244-249.
85. Naiki H, Higuchi K, Nakakuki K, Takeda T (1991) Kinetic analysis of amyloid fibril polymerization in vitro. Lab Investig 65: 104-110.
86. Nalivaeva NN, Beckett C, Belyaev ND, Turner AJ (2012) Are amyloid-degrading enzymes viable therapeutic targets in Alzheimer's disease? J Neurochem 120: 167-185.
87. Narindrasorasak S, Lowery D, Gonzalez-DeWhitt P, Poorman RA, Greenberg B, Kisilevsky R (1991) High affinity interactions between the Alzheimer's beta-amyloid precursor proteins and the basement membrane form of heparan sulfate proteoglycan. J Biol Chem 266: 12878-12883.
88. Nasica-Labouze J, Meli M, Derreumaux P, Colombo G, Mousseau N (2011) A multiscale approach to characterize the early aggregation steps of the amyloid-forming peptide GNNQQNY from the yeast prion sup-35. PLoS Comput Biol 7: e1002051.
89. Ng B, Connors LH, Davidoff R, Skinner M, Falk R (2005) Senile systemic amyloidosis presenting with heart failure: a comparison with light chain-associated amyloidosis. Arch Intern Med 165: 1425-1429.
90. Nguyen HD, Hall CK (2004) Kinetics of fibril formation by polyalanine peptides. J Biol Chem 280: 9074-9082.
91. Nilsson MR (2004) Techniques to study amyloid fibril formation in vitro. Methods 34: 151-160.
92. Norrby E (2011)Prions and protein-folding diseases. J Intern Med 270: 1-14.
93. Olzscha H, Schermann SM, Woerner AC, Pinkert S, Hecht MH, Tartaglia GG, Vendruscolo M, Hayer-Hartl M, Hartl FU, Vabulas RM (2011) Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144: 67-78.
94. Onur MR, Yalni{dotless}z M, Poyraz AK, Özercan IH, Ozkan Y (2012) Pancreatic islet cell amyloidosis manifesting as a large pancreas. Korean J Radiol 13: 94-97.
95. Oosawa F, Asakura S (1975) Thermodynamics of the polymerization of protein. Academic, London.
96. Pallitto MM, Murphy RM (2001) A mathematical model of the kinetics of beta-amyloid fibril growth from the denatured state. Biophys J 81: 1805-1822.
97. Patil SM, Mehta A, Jha S, Alexandrescu AT (2011) Heterogeneous amylin fibril growth mechanisms imaged by total internal reflection fluorescence microscopy. Biochemistry 50: 2808-2819.
98. Pepys M (2001) Pathogenesis, diagnosis and treatment of systemic amyloidosis. Philos Trans R Soc Lond B 356: 203-221.
99. Pepys MB (2006) Amyloidosis. Annu Rev Med 57: 223-241.
100. Pepys MB, Baltz ML, Gomer K, Davis JS, Doenhoff M (1979) Serum amyloid P component is an acute phase reactant in mouse. Nature 278: 259-263.
101. Perrin RJ, Fagan AM, Holtzman DM (2009) Multimodal techniques for diagnosis and prognosis of Alzheimer's disease. Nature 461: 916-922.
102. Petkova AT, Leapman RD, Guo Z, Yau WM, Mattson MP, Tycko R (2005) Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 307: 262-265.
103. Philo JS, Arakawa T (2009) Mechanisms of protein aggregation. Curr Pharm Biotechnol 10: 348-351.
104. Pike CJ, Walencewicz AJ, Glabe CG, Cotman CW (1991) In vitro aging of beta-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res 563: 311-314.
105. Polymenidou M, Cleveland DW (2011) The seeds of neurodegeneration: prion-like spreading in ALS. Cell 147: 498-508.
106. Powers JM, Paolucci S (2006) Strategies for computing slow invariant manifolds in reactive systems. SIAM Eleventh International Conference on Numerical Combustion, Granada, Spain.
107. Powers JM, Paolucci S (2008) Uniqueness of chemical equilibria in ideal mixtures of ideal gases. Am J Phys 76: 848-855.
108. Prusiner SB, Groth DF, Bolton DC, Kent SB, Hood LE (1984) Purification and structural studies of a major scrapie prion protein. Cell 38: 127-134.
109. Pul R, Dodel R, Stangel M (2011) Antibody-based therapy in Alzheimer's disease. Expert Opin Biol Ther 11: 343-357.
110. Quintana C, Wu TD, Delatour B, Dhenain M, Guerquin-Kern JL, Croisy A (2007) Morphological and chemical studies of pathological human and mice brain at the subcellular level: correlation between light, electron, and nanosims microscopies. Microsc Res Tech 70: 281-295.
111. Roberts GW, Gentleman SM, Lynch A, Murray L, Landon M, Graham DI (1994) Beta amyloid protein deposition in the brain after severe head injury: implications for the pathogenesis of Alzheimer's disease. J Neurol Neurosurg Psychiatry 57: 419-425.
112. Rokkitansky C (1842) Handbuch der pathologischen Anatomie. Volume 3, pp. 311, 384, 424. Braumüller and Siedel, Vienna. - as discussed in Cymmers (1956) page 188.
113. Ross ED, Minton A, Wickner RB (2005) Prion domains: sequences, structures and interactions. Nat Cell Biol 11: 1039-1044.
114. Rostagno A, Holton JL, Lashley T, Revesz T, Ghiso J (2010) Cerebral amyloidosis: amyloid subunits, mutants and phenotypes. Cell Mol Life Sci 67: 581-600.
115. Sandberg MK, Al-Doujaily H, Sharps B, Clarke AR, Collinge J (2011) Prion propagation and toxicity in vivo occur in two distinct mechanistic phases. Nature 470: 540-542.
116. Schmit JD, Ghosh K, Dill K (2011) What drives amyloid molecules to assemble into oligomers and fibrils? Biophys J 100: 450-458.
117. Selkoe DJ (2011) Resolving controversies on the path to Alzheimer's therapeutics. Nat Med 17: 1060-1065.
118. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-842.
119. Shewmaker F, McGlinchey RP, Wickner RB (2011) Structural insights into functional and pathological amyloid. J Biol Chem. 286: 16533-16540.
120. Simmons MK, Manjeshwar R, Agdeppa ED, Mattheyses RM, Kiehl TR, Montalto MC (2005) A computational positron emission tomography simulation model for imaging beta-amyloid in mice. Mol Imaging Biol 7: 69-77.
121. Sipe JD, Benson MD, Buxbaum JN, Ikeda S, Merlini G, Saraiva MJM, Westermark P (2010) Amyloid fibril protein nomenclature: 2010 recommendations from the nomenclature committee of the International Society for Amyloidosis. Amyloid 17: 101-104.
122. Sluzky V, Tamada JA, Klibanov AM, Langer R (1991) Kinetics of insulin aggregation in aqueous solutions upon agitation in the presence of hydrophobic surfaces. Proc Natl Acad Sci USA 88: 9377-9381.
123. Smith DG, Cappai R, Barnham KJ (2007) The redox chemistry of the Alzheimer's disease amyloid beta peptide. Biochim Biophys Acta 1768: 1976-1990.
124. Soto C, Castaño EM (1996) The conformation of Alzheimer's beta peptide determines the rate of amyloid formation and its resistance to proteolysis. Biochem J 314: 701-717.
125. Standley DM, Yonezawa Y, Goto Y, Nakamura H (2006) Flexible docking of an amyloid-forming peptide from beta(2)-microglobulin. FEBS Lett 580: 6199-6205.
126. Stefani M (2010) Biochemical and biophysical features of both oligomer/fibril and cell membrane in amyloid cytotoxicity. FEBS J 277: 4602-4613.
127. Straub JE, Thirumalai D (2012) Toward a molecular theory of early and late events in monomer to amyloid fibril formation. Annu Rev Phys Chem 62: 437-463.
128. Symmers WS (1956) Primary amyloidosis: a review. J Clin Pathol 9: 187-211.
129. Tanaka M, Chien P, Naber N, Cooke R, Weissman JS (2004) Conformational variations in an infectious protein determine prion strain differences. Nature 428(6980): 232-328.
130. Treusch S, Lindquist S (2012) An intrinsically disordered yeast prion arrests the cell cycle by sequestering a spindle pole body component. J Cell Biol 197: 369-379.
131. Tycko R (2011) Solid-state NMR studies of amyloid fibril structure. Annu Rev Phys Chem 62: 279-299.
132. Urbanc B, Cruz L, Buldyrev SV, Havlin S, Irizarry MC, Stanley HE, Hyman BT (1999) Dynamics of plaque formation in Alzheimer's disease. Biophys J 76: 1330-1334.
133. Uversky V (2008) Amyloidogenesis of natively unfolded proteins. Curr Alzheimer Res 5: 260-287.
134. Virchow R (1854) Virchows Arch Pathol Anat 6: 135, as discussed by Cymmers (1956) page 188.
135. von Smoluchowski M (1916) Drei vortrage uber diffusion, brownsche bewegung und koagulation von kolloidteilchen. Z Phys 17: 557-585.
136. von Smoluchowski M (1917) Versuch einer mathematischen theorie der koagulationskinetic kolloider losungen. Z Phys 92: 129-168.
137. Westermark G, Westermark P (2009) Serum amyloid A and protein AA: molecular mechanisms of a transmissible amyloidosis. FEBS Lett 583: 2685-2690.
138. Wickner RB, Shewmaker F, Edskes H, Kryndushkin D, Nemecek J, McGlinchey R, Bateman D, Winchester CL (2010) Prion amyloid structure explains templating: how proteins can be genes. FEMS Yeast Res 10(8): 980-991.
139. Wilson MR, Yerbury JJ, Poon S (2008)Potential roles of abundant extracellular chaperones in the control of amyloid formation and toxicity. Mol Biosyst 4: 42-52.
140. Wyss-Coray T, Loike JD, Brionne TC, Lu E, Anankov R, Yan F, Silverstein SC, Husemann J (2003) Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat Med 9: 453-457.
141. Xue WF, Homans SW, Radford SE (2008) Systematic analysis of nucleation-dependent polymerization reveals new insights into the mechanism of amyloid self-assembly. Proc Natl Acad Sci USA 105: 8926-8931.
142. Xue WF, Hellewell AL, Gosal WS, Homans SW, Hewitt EW, Radford SE (2009) Fibril fragmentation enhances amyloid cytotoxicity. J Biol Chem 284: 34272-34282.
143. Xue WF, Hellewell AL, Hewitt EW, Radford SE (2010) Fibril fragmentation in amyloid assembly and cytotoxicity: when size matters. Prion 4: 20-25.