A three-stage kinetic model of amyloid fibrillation

Biophysical Journal

Volumn 92, Issue 10, 2007, Pages 3448-3458

  Lee, Chuang Chung ^a   Nayak, Arpan ^b   Sethuraman, Ananthakrishnan ^b   Belfort, Georges ^b   McRae, Gregory J ^a  

^a Massachusetts Institute of Technology   (United States)

^b Rensselaer Polytechnic Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; INSULIN;

ARTICLE; CHEMICAL REACTION; ENVIRONMENTAL FACTOR; MATHEMATICAL MODEL; PHYSICAL CHEMISTRY; POSITIVE FEEDBACK; PROTEIN FOLDING; SIMULATION; ULTRAVIOLET SPECTROSCOPY;

EID: 34247862247     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.098608     Document Type: Article

References (47)

1. Sipe, J. D. 2005. Amyloid Protein: The Beta Sheet Conformation and Disease. John Wiley and Sons, New York.
2. Bitan, G., A. Lomakin, and D. B. Teplow. 2001. Amyloid-β-protein oligomerization: prenucleation interactions revealed by photo-induced cross-linking of unmodified proteins. J. Biol. Chem. 276:35176-35184.
3. Collins, S. R., A. Douglass, R. D. Vale, and J. S. Weissman. 2004. Mechanism of prion propagation: amyloid growth occurs by monomer addition. PLoS Biol. 2:1582-1590.
4. Lashuel, H. A., and P. T. Lansbury, Jr. 2006. Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? Quarterly Reviews of Biophysics, Cambridge University Press, Cambridge, UK.
5. Selkoe, D. J. 2004. Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat. Cell Biol. 6:1054-1061.
6. Khurana, R., C. Ionescu-Zanetti, M. Pope, J. Li, L. Nielson, M. Ramírez-Alvarado, L. Regan, A. L. Fink, and S. A. Cartery. 2003. A general model for amyloid fibril assembly based on morphological studies using atomic force microscopy. Biophys. J. 85:1135-1144.
7. Kayed, R., E. Head, J. L. Thompson, T. M. McIntire, S. C. Milton, C. W. Cotman, and C. G. Glabe. 2003. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science. 5618:486-489.
8. Padrick, S. B., and A. D. Miranker. 2002. Islet amyloid: phase partitioning and secondary nucleation are central to the mechanism of firillogenesis. Biochemistry. 41:4694-4703.
9. Slusky, V., J. A. Tamada, A. M. Klibanov, and R. Langer. 1991. Kinetics of insulin aggregation in aqueous solutions upon agitation in the presence of hydrophobic surfaces. Proc. Natl. Acad. Sci. USA. 88:9377-9381.
10. Nielsen, L. R., R. Khurana, A. Coats, S. Frokjaer, J. Brange, S. Vyas, V. N. Uversky, and A. L. Fink. 2001. Effect of environmental factors on the kinetics of insulin fibril formation: elucidation of the molecular mechanism. Biochemistry. 40:6036-6046.
11. Evans, K. C., E. P. Berger, C. Cho, K. H. Weisgraber, and P. T. Lansbury Jr. 1995. Apolipoprotein E is a kinetic but not a thermodynamic inhibitor of amyloid formation: implications for the pathogenesis and treatment of Alzheimer disease. Proc. Natl. Acad. Sci. USA. 92:763-767.
12. Lomakin, A., D. B. Teplow, D. A. Kirschner, and G. B. Benedek. 1997. Kinetic theory of fibrillogenesis of amyloid-protein. Proc. Natl. Acad. Sci. USA. 94:7942-7947.
13. Flyvbjerg, H., E. Jobs, and S. Leibler. 1996. Kinetics of self-assembling microtubules: an "inverse problem" in biochemistry. Proc. Natl. Acad. Sci. USA. 93:5975-5979.
14. Scheibel, T., J. Bloom, and S. L. Lindquist. 2004. The elongation of yeast prion fibers involves separable steps of association and conversion. Proc. Natl. Acad. Sci. USA. 101:2287-2292.
15. Pasternack, R. F., E. J. Gibbs, S. Sibley, L. Woodard, P. Hutchinson, J. Genereux, and K. Kristian. 2006. Formation kinetics of insulin-based amyloid gels and the effect of added metalloporphyrins. Biophys. J. 90:1033-1042.
16. Shoghi-Jadid, K., J. R. Barrio, V. Kepe, H. M. Wu, G. W. Small, M. E. Phelps, and S. C. Huang. 2005. Imaging β-amyloid fibrils in Alzheimer's disease: a critical analysis through simulation of amyloid fibril polymerization. Nucl. Med. Biol. 32:337-351.
17. Uversky, V. N., J. Li, and A. L. Fink. 2001. Metal-triggered structural transformations, aggregation, and fibrillation of human α-synuclein. J. Biol. Chem. 276:44284-44296.
18. Levine III, H. 1999. Quantification of beta-sheet amyloid fibril structure with thioflavin T. Methods Enzymol. 309:274-284.
19. Levine III, H. 2005. Multiple ligand binding sites on Aβ(1-40) fibrils. Protein Folding Symposium #7, Amyloids. 12:5-14.
20. Serio, T. R., A. G. Cashikar, A. S. Kowal, G. J. Sawicki, J. J. Moslehi, M. F. Arnsdorf, and S. L. Lindquist. 2000. Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science. 289:1317-1321.
21. Reference deleted in proof.
22. Lee, C.-C., A. Nayak, G. Belfort, and G. J. McRae. 2006. A Mathematical Model of Amyloid Fibrillation: The Case for Insulin. Biophysical Society Conference, Salt Lake City, Utah.
23. Wang, F., R. L. Hull, J. Vidal, M. Cnop, and S. E. Kahn. 2001. Islet amyloid develops diffusely throughout the pancreas before becoming severe and replacing endocrine cells. Diabetes. 50:2514-2520.
24. Krishnan, R., and S. L. Lindquist. 2005. Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature. 435:765-772.
25. Pallitto, M. M., and R. M. Murphy. 2001. A mathematical model of the kinetics of β-amyloid fibril growth from the denatured state. Biophys. J. 81:1805-1822.
26. Gosal, W. S., I. J. Morten, E. W. Hewitt, D. A. Smith, N. H. Thomson, and S. E. Radford. 2005. Competing pathways determine fibril morphology in the self-assembly of β2-microglobulin into amyloid. J. Mol. Biol. 351:850-864.
27. Gill, R. 1994. Protein engineering of insulin-like growth factor. PhD Thesis. University of London, London, UK.
28. Jiménez, J. L., E. J. Nettleton, M. Bouchard, C. V. Robinson, C. M. Dobson, and H. R. Saibil. 2002. The protofilament structure of insulin amyloid fibrils. Proc. Natl. Acad. Sci. USA. 99:9196-9201.
29. Manno, M., E. F. Craparo, V. Martorana, D. Bulone, and P. L. San Biagio. 2006. Kinetics of insulin aggregation: disentanglement of amyloid fibrillation from large-size cluster formation. Biophys. J. 90:4585-4591.
30. Oysterbye, T., K. H. Jørgensen, and P. Fredman. 2001. Sulfatide promotes the folding of proinsulin, preserves insulin crystals, and mediates its monomerization. Glycobiology. 11:473-479.
31. Seinfeld, J. H., and S. N. Pandis. 1998. Atmospheric Chemistry and Physics. John Wiley and Sons, New York.
32. Hasegawa, K., K. Ono, M. Yamada, and H. Naiki. 2002. Kinetic modeling and determination of reaction constants of Alzheimer's β-amyloid fibril extension and dissociation using surface plasmon resonance. Biochemistry. 41:13489-13498.
33. Hassiepen, U., M. Federwisch, T. Mülders, and A. Wollmer. 1999. The lifetime of insulin hexamers. Biophys. J. 77:1638-1654.
34. Fogler, H. S. 1998. Elements of Chemical Reaction Engineering. Prentice Hall, Upper Saddle River, NJ.
35. Bird, R. B., W. E. Stewart, and E. N. Lightfoot. 2002. Transport Phenomena, 2nd Ed. John Wiley and Sons, New York.
36. Reference deleted in proof.
37. Seber, G. A. F., and C. J. Wild. 2003. Nonlinear Regression. John Wiley and Sons, New York.
38. Kingsland, S. E. 1995. Modeling Nature. University Of Chicago Press, Chicago, IL.
39. Nelson, R., M. R. Sawaya, M. Balbirnie, A. O. Madsen, C. Riekel, R. Grothe, and D. Eisenberg. 2005. Structure of the cross-β spine of amyloid-like fibrils. Nature. 435:773-778.
40. Neu, J. C., J. A. Canizo, and L. L. Bonilla. 2002. Three eras of micellization. Phys. Rev. E. 66:061406.
41. Agena, S. M., I. D. L. Bogle, and F. L. P. Pessoas. 1997. An activity coefficient model for proteins. Biotechnol. Bioeng. 55:65-71.
42. Wood, S. J., J. Wypych, S. Steavenson, J. C. Louis, M. Citron, and A. L. Biere. 1999. Alpha-synuclein fibrillogenesis is nucleationdependent. J. Biol. Chem. 274:19509-19512.
43. Hong, D.-P., and A. L. Fink. 2005. Independent heterologous fibrillation of insulin and its β-chain peptide. Biochemistry. 44:16701-16709.
44. Levenspiel, O. 1999. Chemical Reaction Engineering. John Wiley and Sons, New York.
45. Quist, A., I. Doudevski, H. Lin, R. Azimova, D. Ng, B. Frangione, B. Kagan, J. Ghiso, and R. Lal. 2005. Amyloid ion channels: a common structural link for protein-misfolding disease. Proc. Natl. Acad. Sci. USA. 102:10427-10432.
46. Nguyen, H. D., and C. K. Hall. 2004. Molecular dynamics simulations of spontaneous fibril formation. Proc. Natl. Acad. Sci. USA. 101:16180-16185.
47. Liu, Y., H. A. Lashuel, S. Choi, X. Xing, A. Case, J. Ni, L.-A. Yeh, G. D. Cuny, R. L. Stein, and P. T. Lansbury, Jr. 2003. Discovery of inhibitors that elucidate the role of UCH-L1 activity in the H1299 lung cancer cell line. Chem. Biol. 10:837-846.