Mechanisms of Protein Fibril Formation: Nucleated Polymerization with Competing Off-Pathway Aggregation

Selkoe, 2003, Folding proteins in fatal ways, Nature, 426, 900, 10.1038/nature02264 Pepys, 2006, Amyloidosis, Annu. Rev. Med., 57, 223, 10.1146/annurev.med.57.121304.131243 Hardy, 2002, Medicine—the amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics, Science, 297, 353, 10.1126/science.1072994 Fink, 2006, The aggregation and fibrillation of alpha-synuclein, Acc. Chem. Res., 39, 628, 10.1021/ar050073t Buxbaum, 2003, Diseases of protein conformation: what do in vitro experiments tell us about in vivo diseases?, Trends Biochem. Sci., 28, 585, 10.1016/j.tibs.2003.09.009 Ferrone, 2006, Nucleation: the connections between equilibrium and kinetic behavior, Methods Enzymol., 412, 285, 10.1016/S0076-6879(06)12017-0 Oosawa, 1975 Andrews, 2007, A Lumry-Eyring nucleated polymerization model of protein aggregation kinetics. 1. Aggregation with pre-equilibrated unfolding, J. Phys. Chem. B, 111, 7897, 10.1021/jp070212j Powers, 2006, The kinetics of nucleated polymerizations at high concentrations: amyloid fibril formation near and above the “supercritical concentration”, Biophys. J., 91, 122, 10.1529/biophysj.105.073767 Ahmad, 2005, Early events in the fibrillation of monomeric insulin, J. Biol. Chem., 280, 42669, 10.1074/jbc.M504298200 Baskakov, 2002, Pathway complexity of prion protein assembly into amyloid, J. Biol. Chem., 277, 21140, 10.1074/jbc.M111402200 Bieschke, 2005, Oxidative metabolites accelerate Alzheimer’s amyloidogenesis by a two-step mechanism, eliminating the requirement for nucleation, Biochemistry, 44, 4977, 10.1021/bi0501030 Bitan, 2001, Amyloid beta-protein oligomerization: prenucleation interactions revealed by photo-induced cross-linking of unmodified proteins, J. Biol. Chem., 276, 35176, 10.1074/jbc.M102223200 Conway, 2000, Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson’s disease: implications for pathogenesis and therapy, Proc. Natl. Acad. Sci. USA, 97, 571, 10.1073/pnas.97.2.571 Kaylor, 2005, Characterization of oligomeric intermediates in alpha-synuclein fibrillation: FRET studies of Y125W/Y133F/Y136F alpha-synuclein, J. Mol. Biol., 353, 357, 10.1016/j.jmb.2005.08.046 Kirkitadze, 2001, Identification and characterization of key kinetic intermediates in amyloid beta-protein fibrillogenesis, J. Mol. Biol., 312, 1103, 10.1006/jmbi.2001.4970 Plakoutsi, 2005, Evidence for a mechanism of amyloid formation involving molecular reorganisation within native-like precursor aggregates, J. Mol. Biol., 351, 910, 10.1016/j.jmb.2005.06.043 Rhoades, 2000, Aggregation of an amyloidogenic fragment of human islet amyloid polypeptide, Biochim. Biophys. Acta, 1476, 230, 10.1016/S0167-4838(99)00248-4 Sabate, 2005, Evidence of the existence of micelles in the fibrillogenesis of beta-amyloid peptide, J. Phys. Chem. B, 109, 11027, 10.1021/jp050716m Serio, 2000, Nucleated conformational conversion and the replication of conformational information by a prion determinant, Science, 289, 1317, 10.1126/science.289.5483.1317 Sokolowski, 2003, Formation of critical oligomers is a key event during conformational transition of recombinant Syrian hamster prion protein, J. Biol. Chem., 278, 40481, 10.1074/jbc.M304391200 Souillac, 2002, Elucidation of the molecular mechanism during the early events in immunoglobulin light chain amyloid fibrillation. Evidence for an off-pathway oligomer at acidic pH, J. Biol. Chem., 277, 12666, 10.1074/jbc.M109229200 Souillac, 2003, Structural transformations of oligomeric intermediates in the fibrillation of the immunoglobulin light chain LEN, Biochemistry, 42, 8094, 10.1021/bi034652m Teplow, 2006, Elucidating amyloid beta-protein folding and assembly: a multidisciplinary approach, Acc. Chem. Res., 39, 635, 10.1021/ar050063s Ferrone, 1999, Analysis of protein aggregation kinetics, Methods Enzymol., 309, 256, 10.1016/S0076-6879(99)09019-9 Goldstein, 1986, Cooperative polymerization reactions: analytical approximations, numerical examples, and experimental strategy, Biophys. J., 50, 583, 10.1016/S0006-3495(86)83498-1 Hill, 1987 Roberts, 2003, Kinetics of irreversible protein aggregation: analysis of extended Lumry-Eyring models and implications for predicting protein shelf life, J. Phys. Chem. B, 107, 1194, 10.1021/jp026827s McCoy, 2001, Distribution kinetics modeling of nucleation, growth, and aggregation processes, Ind. Eng. Chem. Res., 40, 5147, 10.1021/ie001034i Janin, 1997, The kinetics of protein-protein recognition, Proteins, 28, 153, 10.1002/(SICI)1097-0134(199706)28:2<153::AID-PROT4>3.0.CO;2-G Northrup, 1992, Kinetics of protein-protein association explained by Brownian dynamics computer simulation, Proc. Natl. Acad. Sci. USA, 89, 3338, 10.1073/pnas.89.8.3338 Schlosshauer, 2002, A general expression for bimolecular association rates with orientational constraints, J. Phys. Chem. B, 106, 12079, 10.1021/jp025894j Firestone, 1983, On one dimensional nucleation and growth of living polymers. 1. Homogeneous nucleation, J. Theor. Biol., 104, 535, 10.1016/0022-5193(83)90244-8 Rhoades, 2003, Micelle formation by a fragment of human islet amyloid polypeptide, Biophys. J., 84, 3480, 10.1016/S0006-3495(03)70068-X Kunes, 2005, One-dimensional model of yeast prion aggregation, Phys. Rev. E, 72, 051915, 10.1103/PhysRevE.72.051915 Powers, 2003, A perspective on mechanisms of protein tetramer formation, Biophys. J., 85, 3587, 10.1016/S0006-3495(03)74777-8 LeVine, 1999, Quantification of beta-sheet amyloid fibril structures with thioflavin T, Methods Enzymol., 309, 274, 10.1016/S0076-6879(99)09020-5 Nilsson, 2004, Techniques to study amyloid fibril formation in vitro, Methods, 34, 151, 10.1016/j.ymeth.2004.03.012 Frankenfield, 2005, Influence of the N-terminal domain on the aggregation properties of the prion protein, Protein Sci., 14, 2154, 10.1110/ps.051434005 Hurshman, 2004, Transthyretin aggregation under partially denaturing conditions is a downhill polymerization, Biochemistry, 43, 7365, 10.1021/bi049621l O’Nuallain, 2006, Kinetics and thermodynamics of amyloid assembly using a high-performance liquid chromatography-based sedimentation assay, Methods Enzymol., 413, 34, 10.1016/S0076-6879(06)13003-7 Mok, 2006, Sedimentation velocity analysis of amyloid oligomers and fibrils, Methods Enzymol., 413, 199, 10.1016/S0076-6879(06)13011-6 Rogers, 2005, Measuring the length distribution of a fibril system: a flow birefringence technique applied to amyloid fibrils, Macromolecules, 38, 2948, 10.1021/ma0474224 Chen, 2002, Huntington’s disease age-of-onset linked to polyglutamine aggregation nucleation, Proc. Natl. Acad. Sci. USA, 99, 11884, 10.1073/pnas.182276099 Ferrone, 1985, Kinetics of sickle hemoglobin polymerization. 1. Studies using temperature-jump and laser photolysis techniques, J. Mol. Biol., 183, 591, 10.1016/0022-2836(85)90174-3 Ferrone, 1985, Kinetics of sickle hemoglobin polymerization. 2. A double nucleation mechanism, J. Mol. Biol., 183, 611, 10.1016/0022-2836(85)90175-5 Chalikian, 1996, The hydration of globular proteins as derived from volume and compressibility measurements: cross correlating thermodynamic and structural data, J. Mol. Biol., 260, 588, 10.1006/jmbi.1996.0423 Oster, 1947, Light scattering from polymerizing and coagulating systems, J. Colloid Sci., 2, 291, 10.1016/0095-8522(47)90031-7 Berne, 1974, Interpretation of the light scattering from long rods, J. Mol. Biol., 89, 755, 10.1016/0022-2836(74)90049-7 Bauer, 1995, Architecture and polymorphism of fibrillar supramolecular assemblies produced by in vitro aggregation of human calcitonin, J. Struct. Biol., 115, 1, 10.1006/jsbi.1995.1024 Cardoso, 2002, Transthyretin fibrillogenesis entails the assembly of monomers: a molecular model for in vitro assembled transthyretin amyloid-like fibrils, J. Mol. Biol., 317, 683, 10.1006/jmbi.2002.5441 Goldsbury, 1997, Polymorphic fibrillar assembly of human amylin, J. Struct. Biol., 119, 17, 10.1006/jsbi.1997.3858 Goldsbury, 2000, Studies on the in vitro assembly of Abeta 1–40: implications for the search for a beta fibril formation inhibitors, J. Struct. Biol., 130, 217, 10.1006/jsbi.2000.4259 Pallitto, 2001, A mathematical model of the kinetics of beta-amyloid fibril growth from the denatured state, Biophys. J., 81, 1805, 10.1016/S0006-3495(01)75831-6 Shen, 1994, Effect of acid predissolution on fibril size and fibril flexibility of synthetic beta-amyloid peptide, Biophys. J., 67, 1238, 10.1016/S0006-3495(94)80593-4 Chen, 2002, Amyloid-like features of polyglutamine aggregates and their assembly kinetics, Biochemistry, 41, 7391, 10.1021/bi011772q Zhang, 2004, Metabolite-initiated protein misfolding may trigger Alzheimer’s disease, Proc. Natl. Acad. Sci. USA, 101, 4752, 10.1073/pnas.0400924101 Yong, 2002, Structure determination of micelle-like intermediates in amyloid beta-protein fibril assembly by using small angle neutron scattering, Proc. Natl. Acad. Sci. USA, 99, 150, 10.1073/pnas.012584899 Lomakin, 1997, Kinetic theory of fibrillogenesis of amyloid beta-protein, Proc. Natl. Acad. Sci. USA, 94, 7942, 10.1073/pnas.94.15.7942 Lomakin, 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, 10.1073/pnas.93.3.1125 Puvvada, 1990, Molecular-thermodynamic approach to predict micellization, phase behavior and phase separation of micellar solutions. 1. Application to nonionic surfactants, J. Chem. Phys., 92, 3710, 10.1063/1.457829 Tanford, 1980 Schreiber, 2002, Kinetic studies of protein-protein interactions, Curr. Opin. Struct. Biol., 12, 41, 10.1016/S0959-440X(02)00287-7 Koren, 1976, A kinetic study of protein-protein interactions, Biochemistry, 15, 1165, 10.1021/bi00650a032 Bucciantini, 2002, Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases, Nature, 416, 507, 10.1038/416507a Haass, 2007, Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer’s amyloid beta-peptide, Nat. Rev. Mol. Cell Biol., 8, 101, 10.1038/nrm2101 Klein, 2004, Small assemblies of unmodified amyloid beta-protein are the proximate neurotoxin in Alzheimer’s disease, Neurobiol. Aging, 25, 569, 10.1016/j.neurobiolaging.2004.02.010 Lambert, 1998, Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins, Proc. Natl. Acad. Sci. USA, 95, 6448, 10.1073/pnas.95.11.6448 Reixach, 2004, Tissue damage in the amyloidoses: transthyretin monomers and nonnative oligomers are the major cytotoxic species in tissue culture, Proc. Natl. Acad. Sci. USA, 101, 2817, 10.1073/pnas.0400062101 Silveira, 2005, The most infectious prion protein particles, Nature, 437, 257, 10.1038/nature03989