BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Mechanism of amyloidogenesis: nucleation-dependent fibrillation versus double-concerted fibrillation

  • Bhak, Ghi-Bom (School of Chemical and Biological Engineering, College of Engineering, Seoul National University) ;
  • Choe, Young-Jun (School of Chemical and Biological Engineering, College of Engineering, Seoul National University) ;
  • Paik, Seung-R. (School of Chemical and Biological Engineering, College of Engineering, Seoul National University)
  • Published : 2009.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Amyloidogenesis defines a condition in which a soluble and innocuous protein turns to insoluble protein aggregates known as amyloid fibrils. This protein suprastructure derived via chemically specific molecular self-assembly process has been commonly observed in various neurodegenerative disorders such as Alzheimer's, Parkinson's, and Prion diseases. Although the major culprit for the cellular degeneration in the diseases remains unsettled, amyloidogenesis is considered to be etiologically involved. Recent recognition of fibrillar polymorphism observed mostly from in vitro amyloidogeneses may indicate that multiple mechanisms for the amyloid fibril formation would be operated. Nucleation-dependent fibrillation is the prevalent model for assessing the self-assembly process. Following thermodynamically unfavorable seed formation, monomeric polypeptides bind to the seeds by exerting structural adjustments to the template, which leads to accelerated amyloid fibril formation. In this review, we propose another in vitro model of amyloidogenesis named double-concerted fibrillation. Here, two consecutive assembly processes of monomers and subsequent oligomeric species are responsible for the amyloid fibril formation of $\alpha$-synuclein, a pathological component of Parkinson's disease, following structural rearrangement within the oligomers which then act as a growing unit for the fibrillation.

Keywords

References

  1. Sipe, J. D. (1992) Amyloidosis. Annu. Rev. Biochem. 61, 947-975 https://doi.org/10.1146/annurev.bi.61.070192.004503
  2. Chiti, F. and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366 https://doi.org/10.1146/annurev.biochem.75.101304.123901
  3. Virchow, R. (1854) Zur celluslose-frage. Virchows Arch. 6, 415-426
  4. Selkoe, D. J. (2003) Folding proteins in fatal ways. Nature 426, 900-904 https://doi.org/10.1038/nature02264
  5. Sacchettini, J. C. and Kelly, J. W. (2002) Therapeutic strategies for human amyloid diseases. Nat. Rev. Drug. Discov. 1, 267-275 https://doi.org/10.1038/nrd769
  6. Hardy, J. and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356 https://doi.org/10.1126/science.1072994
  7. Tan, S. Y. and Pepys, M. B. (1994) Amyloidosis. Histopathology 25, 403-414 https://doi.org/10.1111/j.1365-2559.1994.tb00001.x
  8. Merlini, G. and Bellotti, V. (2003) Molecular mechanisms of amyloidosis. N. Engl. J. Med. 349, 583-596 https://doi.org/10.1056/NEJMra023144
  9. Lashuel, H. A., Hartley, D., Petre, B. M., Walz, T. and Lansbury, P. T. Jr. (2002) Amyloid pores from pathogenic mutations. Nature 418, 291
  10. Caughey, B. and Lansbury, P. T. Jr. (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26, 267-298 https://doi.org/10.1146/annurev.neuro.26.010302.081142
  11. Huang, X., Cuajungco, M. P., Atwood, C. S., Hartshorn, M. A., Tyndall, J. D. A., Hanson, G. R., Stokes, K. C., Leopold, M., Multhaup, G., Goldstein, L. E., Scarpa, R. C., Saunders, A. J., Lim, J., Moir, R. D., Glabe, C., Bowden, E. F., Masters, C. L., Fairlie, D. P., Tanzi, R. E. and Bush, A. I. (1999) Cu(II) potentiation of Alzheimer Ab neurotoxicity. J. Biol. Chem. 274, 37111-37116 https://doi.org/10.1074/jbc.274.52.37111
  12. Huang, X., Atwood, C. S., Hartshorn, M. A., Multhaup, G., Goldstein, L. E., Scarpa, R. C., Cuajungco, M. P., Gray, D. N., Lim, J., Moir, R. D., Tanzi, R. E. and Bush, A. I. (1999) The Ab peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry 38, 7609-7616 https://doi.org/10.1021/bi990438f
  13. Cuajungco, M. P., Goldstein, L. E., Nunomura, A., Smith, M. A., Lim, J. T., Atwood, C. S., Huang, X., Farrag, Y. W., Perry, G. and Bush, A. I. (2000) Evidence that the b-amyloid plaques of Alzhermer's disease represent the redox-silencing and entombment of Ab by zinc. J. Biol. Chem. 275, 19439-19442 https://doi.org/10.1074/jbc.C000165200
  14. Opazo, C., Huang, X., Cherny, R. A., Moir, R. D., Roher, A. E., White, A. R., Cappai, R., Masters, C. L., Tanzi, R. E., Inestrosa, N. C. and Bush, A. I. (2002) Metalloenzyme-like activity of Alzheimer's disease $\beta$-amyloid. J. Biol. Chem. 277, 40302-40308 https://doi.org/10.1074/jbc.M206428200
  15. Barnham, K. J., Ciccotosto, G. D., Tickler, A. K., Ali, F. E., Smith, D. G., Williamson, N. A., Lam, Y. -H., Carrington, D., Tew, D., Kocak, G., Volitakis, I., Separovic, F., Barrow, C. J., Wade, J. D., Masters, C. L., Cherny, R. A., Curtain, C. C., Bush, A. I. and Cappai, R. (2003) Neurotoxic, redox-competent Alzheimer's b-amyloid is released from lipid membrane by methionine oxidation. J. Biol. Chem. 278, 42959-42965 https://doi.org/10.1074/jbc.M305494200
  16. Fowler, D. M., Koulov, A. V., Balch, W. E. and Kelly, J. W. (2007) Functional amyloid - from bacteria to humans. Trends Biochem. Sci. 32, 217-224 https://doi.org/10.1016/j.tibs.2007.03.003
  17. Barnhart, M. M. and Chapman, M. R. (2006) Curli biogenesis and function. Annu. Rev. Microbiol. 60, 131-147 https://doi.org/10.1146/annurev.micro.60.080805.142106
  18. Costerton, J. W., Stewart, P. S. and Greenberg, E. P. (1999) Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322 https://doi.org/10.1126/science.284.5418.1318
  19. Kikuchi, T., Mizunoe, Y., Takade, A., Naito, S. and Yoshida, S. (2005) Curli fibers are required for development of biofilm architecture in Escherichia coli K-12 and enhance bacterial adhearence to human uroepithelial cells. Microbiol. Immunol. 49, 875-884 https://doi.org/10.1111/j.1348-0421.2005.tb03678.x
  20. Gebbink, M. F. B. G., Claessen, D., Bouma, B., Dijkhuizen, L. and Wosten, H. A. B. (2005) Amyloids - a functional coat for microorganisms. Nat. Rev. Microbiol. 3, 333-341 https://doi.org/10.1038/nrmicro1127
  21. Talbot, N. J. (2003) Aerial morphogenesis: enter the chaplins. Curr. Biol. 13, R696-R698 https://doi.org/10.1016/j.cub.2003.08.040
  22. Iconomidou, V. A., Vriend, G. and Hamodrakas, S. J. (2000) Amyloids protect the silkmoth oocyte and embryo. FEBS Lett. 479, 141-145 https://doi.org/10.1016/S0014-5793(00)01888-3
  23. Podrabsky, J. E., Carpenter, J. F. and Hand, S. C. (2001) Survival of water stress in annual fish embryos: dehydration avoidance and egg envelope amyloid fibers. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R123-R131
  24. Fowler, D. M., Koulov, A. V., Alory-Jost, C., Marks, M. S., Balch, W. E. and Kelly, J. W. (2006) Functional amyloid formation within mammalian tissue. PLoS Biol. 4, e6 https://doi.org/10.1371/journal.pbio.0040006
  25. Shibayama, Y., Joseph, K., Nakazawa, Y., Ghebreihiwet, B., Peerschke, E. I. B. and Kaplan, A. P. (1999) Zinc-dependent activation of the plasma kinin-forming cascade by aggregated $\beta$ amyloid protein. Clin. Immunol. 90, 89-99 https://doi.org/10.1006/clim.1998.4621
  26. Sunde, M. and Blake, C. C. F. (1998) From the globular to the fibrous state: protein structure and structural conversion in amyloid formation. Q. Rev. Biophys. 31, 1-39 https://doi.org/10.1017/S0033583598003400
  27. Sunde, M., Serpella, L. C., Bartlama, M., Frasera, P. E., Pepysa, M. B. and Blake, C. C. F. (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 273, 729-739 https://doi.org/10.1006/jmbi.1997.1348
  28. Knowles, T. P., Fitzpatrick, A. W., Meehan, S., Mott, H. R., Vendruscolo, M., Dobson, C. M. and Welland, M. E. (2007) Role of intermolecular forces in defining material properties of protein nanofibrils. Science 318, 1900-1903 https://doi.org/10.1126/science.1150057
  29. Cherny, I. and Gazit, E. (2008) Amyloids: Not only pathological agents but also ordered nanomaterials. Angew. Chem. Int. Ed. 47, 4062-4069 https://doi.org/10.1002/anie.200703133
  30. Zhang, S. (2003) Fabrication of novel biomaterials through molecular self-assembly. Nat. Biotechnol. 21, 1171-1178 https://doi.org/10.1038/nbt874
  31. Scheibel, T., Parthasarathy, R., Sawicki, G., Lin, X. -M., Jaeger, H. and Lindquist, S. L. (2003) Conducting nanowires built by controlled self-assembly of amyloid fibers and selective metal deposition. Proc. Natl. Acad. Sci. U.S.A. 100, 4527-4532 https://doi.org/10.1073/pnas.0431081100
  32. Song, Y., Challa, S. R., Medforth, C. J., Qiu, Y., Watt, R. K., Pena, D., Miller, J. E., Swol, F. and Shelnutt, J. A. (2004) Synthesis of peptide-nanotube platinum-nanoparticle composites. Chem. Commun. 1044-1045
  33. Reches, M. and Gazit, E. (2003) Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 300, 625-627 https://doi.org/10.1126/science.1082387
  34. Carny, O., Shalev, D. E. and Gazit, E. (2006) Fabrication of coaxial metal nanocables using a self-assembled peptide nanotube scaffold. Nano Lett. 6, 1594-1597 https://doi.org/10.1021/nl060468l
  35. Fu, X., Wang, Y., Huang, L., Sha, Y., Gui, L., Lai, L. and Tang, Y. (2003) Asseblies of metal nanoparticles and self-assembled peptide fibrils - formation of double helical and single-chain arrays of metal nanoparticles. Adv. Mater. 15, 902-906 https://doi.org/10.1002/adma.200304624
  36. Reches, M. and Gazit, E. (2007) Biological and chemical decoration of peptide nanostructures via biotin-avidin interactions. J. Nanosci. Nanotechnol. 7, 2239-2245 https://doi.org/10.1166/jnn.2007.645
  37. Baxa, U., Speransky, V., Steven, A. C. and Wickner, R. B. (2002) Mechanism of inactivation on prion conversion of the Saccharomyces cerevisiae Ure2 protein. Proc. Natl. Acad. Sci. U.S.A. 99, 5253-5260 https://doi.org/10.1073/pnas.082097899
  38. Baldwin, A. J., Bader, R., Christodoulou, J., MacPhee, C. E., Dobson, C. M. and Barker, P. D. (2006) Cytochrome display on amyloid fibrils. J. Am. Chem. Soc. 128, 2162-2163 https://doi.org/10.1021/ja0565673
  39. Corrigan, A. M., Muller, C. and Krebs, M. R. H. (2006) The formation of nematic liquid crystal phases by hen lysozyme amyloid fibrils. J. Am. Chem. Soc. 128, 14740-14741 https://doi.org/10.1021/ja064455l
  40. Aggeli, A., Bell, M., Boden, N., Keen, J. N., Knowles, P. F., McLeish, T. C. B., Pitkeathly, M. and Radford, S. E. (1997) Responsive gels formed by the spontaneous self-assembly of peptides into polymeric $\beta$-sheet tapes. Nature 386, 259-262 https://doi.org/10.1038/386259a0
  41. Zhang, Y., Gu, H., Yang, Z. and Xu, B. (2003) Supramolecular hydrogels respond to lignad-receptor interaction. J. Am. Chem. Soc. 125, 13680-13681 https://doi.org/10.1021/ja036817k
  42. Yang, Z., Liang, G., Wang, L. and Xu, B. (2006) Using a kinase/phosphatase switch to regulate a supramolecular hydrogel and forming the supramolecular hydrogel in vivo. J. Am. Chem. Soc. 128, 3038-3043 https://doi.org/10.1021/ja057412y
  43. Conway, K. A., Harper, J. D. and Lansbury, P. T. Jr. (1998) Accelerated in vitro fibril formation by a mutant a-synuclein linked to early-onset Parkinson disease. Nat. Med. 4, 1318-1320 https://doi.org/10.1038/3311
  44. Weinreb, P. H., Zhen, W., Poon, A. W., Conway, K. A. and Lansbury, P. T. Jr. (1996) NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry 35, 13709-13715 https://doi.org/10.1021/bi961799n
  45. Kayed, R., Bernhagen, J., Greenfield, N., Sweimeh, K., Brunner, H., Voelter, W. and Kapurniotu, A. (1999) Conformational transitions of islet amyloid polypeptide (IAPP) in amyloid formation in vitro. J. Mol. Biol. 287, 781-796 https://doi.org/10.1006/jmbi.1999.2646
  46. Teplow, D. B. (1998) Structural and kinetic features of amyloid b-protein fibrillogenesis. Amyloid: Int. J. Exp. Clin. Invest. 5, 121-142 https://doi.org/10.3109/13506129808995290
  47. Walsh, D. M., Hartley, D. M., Kusumoto, Y., Fezoui, Y., Condron, M. M., Lomakin, A., Benedek, G. B., Selkoe, D. J. and Teplow, D. B. (1999) Amyloid $\beta$-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J. Biol. Chem. 274, 25945-25952 https://doi.org/10.1074/jbc.274.36.25945
  48. Spillantini, M. G., Crowther, R. A., Jakes, R., Hasegawa, M. and Goedert, M. (1998) $\alpha$-Synuclein in filamentous inclusions of Lewy bodies form Parkinson's disease and dementia with Lewy bodies. Proc. Natl. Acad. Sci. U.S.A. 95, 6469-6473 https://doi.org/10.1073/pnas.95.11.6469
  49. Spillantini, M. G., Schmidt, M. L., Lee, V. M. -Y., Trojanowski, J. Q., Jakes, R. and Goedert, M. (1997) $\alpha$- Synuclein in Lewy bodies. Nature 388, 839-840 https://doi.org/10.1038/42166
  50. Recchia, A., Debetto, P., Negro, A., Guidolin, D., Skaper, S. D. and Giusti, P. (2004) a-Synuclein and Parkinson's disease. FASEB 18, 617-626 https://doi.org/10.1096/fj.03-0338rev
  51. Goedert, M. (2001) Alpha-synuclein and neurodegenerative diseases. Nat. Rev. Neurosci. 2, 492-501 https://doi.org/10.1038/35081564
  52. Fink, A. L. (2006) The aggregation and fibrillation of $\alpha$-synuclein. Acc. Chem. Res. 39, 628-634 https://doi.org/10.1021/ar050073t
  53. Jaikaran, E. T. A. S. and Clark, A. (2001) Islet amyloid and type 2 diabetes: from molecular misfolding to islet pathophysiology. Biochim. Biophys. Acta-Mol. Basis Dis. 1537, 179-203 https://doi.org/10.1016/S0925-4439(01)00078-3
  54. Hardy, J. A. and Higgins, G. A. (1992) Alzheimer's disease: The amyloid cascade hypothesis. Science 256, 184-185 https://doi.org/10.1126/science.1566067
  55. Chiti, F. and Dobson, C. M. (2009) Amyloid formation by globular proteins under native conditions. Nat. Chem. Biol. 5, 15-22 https://doi.org/10.1038/nchembio.131
  56. Harris, D. A. and True, H. L. (2006) New insights into prion structure and toxicity. Neuron 50, 353-357 https://doi.org/10.1016/j.neuron.2006.04.020
  57. Bernier, G. M. (1980) b2-Microglobulin: structure, function and significance. Vox Sanguinis. 38, 323-327 https://doi.org/10.1111/j.1423-0410.1980.tb04500.x
  58. Trinh, C. H., Smith, D. P., Kalverda, A. P., Phillips, S. E. V. and Radford, S. E. (2002) Crystal structure of monomeric human $\beta$-2-microglobulin reveals clues to its amyloidogenic properties. Proc. Natl. Acad. Sci. U.S.A. 99, 9771-9776 https://doi.org/10.1073/pnas.152337399
  59. Artymiuk, P. J. and Blake, C. C. F. (1981) Refinement of human lysozyme at 1.5 A resoution analysis of nonbonded and hydrogen-bond interactions. J. Mol. Biol. 152, 737-762 https://doi.org/10.1016/0022-2836(81)90125-X
  60. Blake, C. C. F., Koenig, D. F., Mair, G. A., North, A. C. T., Phillips, D. C. and Sarma, V. R. (1965) Structure of hen egg-white lysozyme: a three-dimensional fourier synthesis at 2 A resolution. Nature 206, 757-761 https://doi.org/10.1038/206757a0
  61. Kelly, J. W., Colon, W., Lai, Z., Lashuel, H. A., McCulloch, J., McCutchen, S. L., Miroy, G. J. and Peterson, S. A. (1997) Transthyretin quaternary and tertiary structural changes facilitate misassembly into amyloid. Adv. Protein. Chem. 50, 161-181 https://doi.org/10.1016/S0065-3233(08)60321-6
  62. Bellotti, V., Mangione, P. and Merlini, G. (2000) Review: Immunoglobulin light chain amyloidosis - The archetype of structural and pathogenic variability. J. Struct. Biol. 130, 280-289 https://doi.org/10.1006/jsbi.2000.4248
  63. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383 https://doi.org/10.1073/pnas.95.23.13363
  64. Koch, K. M. (1992) Dialysis-related amyloidosis. Kidney Int. 41, 1416-1429 https://doi.org/10.1038/ki.1992.207
  65. Pepys, M. B., Hawkins, P. N., Booth, D. R., Vigushin, D. M., Tennent, G. A., Soutar, A. K., Totty, N., Nguyen, O., Blake, C. C. F., Terry, C. J., Feest, T. G., Zalin, A. M. and Hsuan, J. J. (1993) Human lysozyme gene mutations cause hereditary systemic amyloidosis. Nature 362, 553-557 https://doi.org/10.1038/362553a0
  66. Teale, F. W. J. (1959) Cleavage of the haem-protein link by acid methylethylketone. Biochim. Biophys. Acta. 35, 543 https://doi.org/10.1016/0006-3002(59)90407-X
  67. Fandrich, M., Fletcher, M. A. and Dobson, C. M. (2001) Amyloid fibrils from muscle myoglobin. Nature 410, 165-166 https://doi.org/10.1038/35065514
  68. Fandrich, M., Forge, V., Buder, K., Kittler, M., Dobson, C. M. and Diekmann, S. (2003) Myoglobin forms amyloid fibrils by association of unfolded polypeptide segments. Proc. Natl. Acad. Sci. U.S.A. 100, 15463-15468 https://doi.org/10.1073/pnas.0303758100
  69. Kodali, R. and Wetzel, R. (2007) Polymorphism in the intermediates and products of amyloid assembly. Curr. Opin. Struct. Biol. 17, 48-57 https://doi.org/10.1016/j.sbi.2007.01.007
  70. Petkova, A. T., Leapman, R. D., Guo, Z., Yau, W. -M., Mattson, M. P. and Tycko, R. (2005) Self-propagating, molecular-level polymorphism in Alzheimer's $\beta$-amyloid fibrils. Science 307, 262-265 https://doi.org/10.1126/science.1105850
  71. Wetzel, R., Shivaprasad, S. and Williams, A. D. (2007) Plasticity of amyloid fibrils. Biochemistry 46, 1-10 https://doi.org/10.1021/bi0620959
  72. Goldsbury, C., Frey, P., Olivieri, V., Aebi, U. and Muller, S. A. (2005) Multiple assembly pathways underlie amyloid-b fibril polymorphisms. J. Mol. Biol. 352, 282-298 https://doi.org/10.1016/j.jmb.2005.07.029
  73. Gosal, W. S., Morten, I. J., Hewitt, E. W., Smith, D. A., Thomson, N. H. and Radford, S. E. (2005) Competing pathways determine fibril morphology in the self-assembly of b2-microglobulin into amyloid. J. Mol. Biol. 351, 850-864 https://doi.org/10.1016/j.jmb.2005.06.040
  74. Griffith, J. S. (1967) Self-replication and scrapie. Nature 215, 1043-1044 https://doi.org/10.1038/2151043a0
  75. Nuvolone, M., Aguzzi, A. and Heikenwalder, M. (2009) Cells and prions: a license to replicate. FEBS Lett. 583, 2674-2684 https://doi.org/10.1016/j.febslet.2009.06.014
  76. Park, J. -W., Ahn, J. S., Lee, J. -H., Bhak, G., Jung, S. and Paik, S. R. (2008) Amyloid fibrillar meshwork formation of ion-induced oligomeric species of A$\beta$40 with phthalocyanine tetrasulfonate and its toxic consequences. Chem. Bio. Chem. 9, 2602-2605 https://doi.org/10.1002/cbic.200800343
  77. Kim, Y. -S., Lee, D., Lee, E. -K., Sung, J. Y., Chung, K. C., Kim, J. and Paik, S. R. (2001) Multiple ligand interaction of a-synuclein produced various forms of protein aggregates in the presence of A$\beta$25-35, copper, and eosin. Brain Res. 908, 93-98 https://doi.org/10.1016/S0006-8993(01)02575-6
  78. Paik, S. R., Lee, D., Cho, H. -J., Lee, E. -N. and Chang, C. -S. (2003) Oxidized glutathione stimulated the amyloid formation of a-synuclein. FEBS Lett. 537, 63-67 https://doi.org/10.1016/S0014-5793(03)00081-4
  79. Lee, D., Lee, E. -K., Lee, J. -H., Chang, C. -S. and Paik, S. R. (2001) Self-oligomerization and protein aggregation of a-synuclein in the presence of coomassie brilliant blue. Eur. J. Biochem. 268, 295-301 https://doi.org/10.1046/j.1432-1033.2001.01877.x
  80. McLaurin, J., Yang, D. -S., Yip, C. M. and Fraser, P. E. (2000) Review: modulating factors in amyloi-b fibril formation. J. Struct. Biol. 130, 259-270 https://doi.org/10.1006/jsbi.2000.4289
  81. Dong, J., Canfield, J. M., Mehta, A. K., Shokes, J. E., Tian, B., Childers, W. S., Simmons, J. A., Mao, Z., Scott, R. A., Warncke, K. and Lynn, D. G. (2007) Engineering metal ion coordination to regulate amyloid fibril assembly and toxicity. Proc. Natl. Acad. Sci. U.S.A. 104, 13313-13318 https://doi.org/10.1073/pnas.0702669104
  82. Koppaka, V. and Axelsen, P. H. (2000) Accelerated accumulation of amyloid b proteins on oxidatively damaged lipid membranes. Biochemistry 39, 10011-10016 https://doi.org/10.1021/bi000619d
  83. Naiki, H. and Gejyo, F. (1999) Kinetic analysis of amyloid fibril formation. Methods Enzymol. 309, 305-318 https://doi.org/10.1016/S0076-6879(99)09022-9
  84. Jarrett, J. T. and Lansbury, P. T. Jr. (1993) Seeding 'onedimensional crystallization' of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73, 1055-1058 https://doi.org/10.1016/0092-8674(93)90635-4
  85. Harper, J. D. and Lansbury, P. T. Jr. (1997) Models of amyloid seeding in Alzheimer's disease and scrapie: Mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu. Rev. Biochem. 66, 385-407 https://doi.org/10.1146/annurev.biochem.66.1.385
  86. Wood, S. J., Wypych, J., Steavenson, S., Louis, J. -C., Citron, M. and Biere, A. L. (1999) $\alpha$-Synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease. J. Biol. Chem. 274, 509-512
  87. Sandal, M., Valle, F., Tessari, I., Mammi, S., Bergantino, E., Musiani, F., Brucale, M., Bubacco, L. and Samori, B. (2008) Conformational equilibria in monomeric $\alpha$-synuclein at the single-molecule level. PLoS Biol. 6, e6 https://doi.org/10.1371/journal.pbio.0060006
  88. Uversky, V. N., Lee, H. -J., Li, J., Fink, A. L. and Lee, S. -J. (2001) Stabilization of partially folded conformation during a-synuclein oligomerization in both purified and cytosolic preparations. J. Biol. Chem. 276, 43495-43498 https://doi.org/10.1074/jbc.C100551200
  89. Bennett, M. J., Schlunegger, M. P. and Eisenberg, D. (1995) 3D domain swapping: a mechanism for oligomer assembly. Protein Sci. 4, 2455-2468 https://doi.org/10.1002/pro.5560041202
  90. Serio, T. R., Cashikar, A. G., Kowal, A. S., Sawicki, G. J., Moslehi, J. J., Serpell, L., Arnsdorf, M. F. and Lindquist, S. L. (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289, 1317-1321 https://doi.org/10.1126/science.289.5483.1317
  91. Li, J., Uversky, V. N. and Fink, A. L. (2001) Effect of familial Parkinson's disease point mutations A30P and A53T on the structural properties, aggregation, and fibrillation of human $\alpha$-synuclein. Biochemistry 40, 604-613
  92. Uversky, V. N., Li, J. and Fink, A. L. (2001) Evidence for a partially folded intermediate in $\alpha$-synuclein fibril formation. J. Biol. Chem. 276, 10737-10744 https://doi.org/10.1074/jbc.M010907200
  93. Uversky, V. N., Li, J. and Fink, A. L. (2001) Pesticides directly accelerate the rate of $\alpha$-synuclein fibril formation: a possible factor in Parkinson's disease. FEBS Lett. 500, 105-108 https://doi.org/10.1016/S0014-5793(01)02597-2
  94. Uversky, V. N., Li, J. and Fink, A. L. (2001) Metal-triggered structural transformations, aggregation, and fibrillation of human $\alpha$-synuclein. A possible molecular NK between Parkinson's disease and heavy metal exposure. J. Biol. Chem. 276, 44284-44296 https://doi.org/10.1074/jbc.M105343200
  95. Carulla, N., Caddy, G. L., Hall, D. R., Zurdo, J., Gairi, M., Feliz, M., Giralt, E., Robinson, C. V. and Dobson, C. M. (2005) Molecular recycling within amyloid fibrils. Nature 436, 554-558 https://doi.org/10.1038/nature03986
  96. Apetri, M. M., Maiti, N. C., Zagorski, M. G., Carey, P. R. and Anderson, V. E. (2006) Secondary structure of a-synuclein oligomers: characterization by Raman and atomic force microscopy. J. Mol. Biol. 355, 63-715 https://doi.org/10.1016/j.jmb.2005.10.071
  97. Conway, K. A., Lee, S. -J., Rochet, J. -C., Ding, T. T., Williamson, R. E. and Lansbury, P. T. Jr. (2000) Acceleration of oligomerization, not fibrillization, is a shared property of both a-synuclein mutations linked to early- onset Parkinson's disease: implications for pathogenesis and therapy. Proc. Natl. Acad. Sci. U.S.A. 97, 571-576 https://doi.org/10.1073/pnas.97.2.571
  98. Ding, T. T., Lee, S. -J., Rochet, J. -C. and Lansbury, P. T. Jr. (2002) Annular a-synuclein protofibrils are produced when spherical protofibrils are incubated in solution of bound to brain-derived membranes. Biochemistry 41, 10209-10217 https://doi.org/10.1021/bi020139h
  99. Hoyer, W., Cherny, D., Subramaniam, V. and Jovin, T. M. (2004) Rapid self-assembly of a-synuclein observed by in situ atomic force microscopy. J. Mol. Biol. 340, 127-139 https://doi.org/10.1016/j.jmb.2004.04.051
  100. Bitan, G., Kirkitadze, M. D., Lomakin, A., Vollers, S. S., Benedek, G. B. and Teplow, D. B. (2003) Amyloid b-protein (Ab) assembly: Ab40 and Ab42 oligomerize through distinct pathways. Proc. Natl. Acad. Sci. U.S.A. 100, 330-335 https://doi.org/10.1073/pnas.222681699
  101. Jain, S. and Udgaonkar, J. B. (2008) Evidence for stepwise formation of amyloid fibrils by the mouse prion protein. J. Mol. Biol. 382, 1228-1241 https://doi.org/10.1016/j.jmb.2008.07.052
  102. Eakin, C. M., Attenello, F. J., Morgan, C. J. and Miranker, A. D. (2004) Oligomeric assembly of native-like precursors precedes amyloid formation by $\beta$-2 microglobulin. Biochemistry 43, 7808-7815 https://doi.org/10.1021/bi049792q
  103. Modler, A. J., Gast, K., Lutsch, G. and Damaschun, G. (2003) Assembly of amyloid protofibrils via critical oligomers - A novel pathway of amyloid formation. J. Mol. Biol. 325, 135-148 https://doi.org/10.1016/S0022-2836(02)01175-0
  104. Leonil, J., Henry, G., Jouanneau, D., Delage, M. -M., Forge, V. and Putaux, J. -L. (2008) Kinetics of fibril formation of bovine k-casein indicate a conformational rearrangement as a critical step in the process. J. Mol. Biol. 381, 1267-1280 https://doi.org/10.1016/j.jmb.2008.06.064
  105. Cheon, M., Chang, I., Mohanty, S., Luheshi, L. M., Dobson, C. M., Vendruscolo, M. and Favrin, G. (2007) Structural reorganisation and potential toxicity of oligomeric species formed during the assembly of amyloid fibrils. PLoS Comput. Biol. 3, 1727-1738
  106. Bhak, G., Lee, J. -H., Hahn, J. -S. and Paik, S. R. (2009) Granular assembly of a-synuclein leading to the accelerated amyloid fibril formation with shear stress. PLoS ONE 4, e4177 https://doi.org/10.1371/journal.pone.0004177
  107. Lee, J. -H., Bhak, G., Lee, S. -G. and Paik, S. R. (2008) Instantaneous amyloid fibril formation of a-synuclein from the oligomeric granular structures in the presence of hexane. Biophys. J. 95, L16-L18 https://doi.org/10.1529/biophysj.108.135186
  108. Vestergaard, B., Groenning, M., Roessle, M., Kastrup, J. S., Weert, M., Flink, J. M., Frokjaer, S., Gajhede, M. and Svergun, D. I. (2007) A helical structural nucleus is the primary elongating unit of insulin amyloid fibrils. PLoS Biol. 5, e134 https://doi.org/10.1371/journal.pbio.0050134
  109. Bates, G. (2003) Huntingtin aggregation and toxicity in Huntington's disease. Lancet 361, 1642-1644 https://doi.org/10.1016/S0140-6736(03)13304-1
  110. Morozova-Roche, L. A., Zamotin, V., Malisauskas, M., Ohman, A., Chertkova, R., Lavrikova, M. A., Kostanyan, I. A., Dolgikh, D. A. and Kirpichnikov, M. P. (2004) Fibrillation of carrier protein albebetin and its biologically active constructs. Multiple oligomeric intermediates and pathways. Biochemistry 43, 9610-9619 https://doi.org/10.1021/bi0494121
  111. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W. and Glabe, C. G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 https://doi.org/10.1126/science.1079469
  112. Kaylor, J., Bodner, N., Edridge, S., Yamin, G., Hong, D. -P. and Fink, A. L. (2005) Characterization of oligomeric intermediates in a-synuclein fibrillation: FRET studies of Y125W/Y133F/Y136F $\alpha$-synuclein. J. Mol. Biol. 353, 357-372 https://doi.org/10.1016/j.jmb.2005.08.046
  113. Kumar, S. and Udgaonkar, J. B. (2009) Conformational conversion may precede or follow aggregate elongation on alternative pathways of amyloid protofibril formation. J. Mol. Biol. 385, 1266-1276 https://doi.org/10.1016/j.jmb.2008.11.033
  114. Kayed, R., Sokolov, Y., Edmonds, B., McIntire, T. M., Milton, S. C., Hall, J. E. and Glabe, C. G. (2004) Permeabilization of lipid bilayers is a common conformationdependent activity of soluble amyloid oligomers in protein misfolding diseases. J. Biol. Chem. 279, 46363-46366 https://doi.org/10.1074/jbc.C400260200
  115. Souillac, P. O., Uversky, V. N. and Fink, A. L. (2003) Structural transformations of oligomeric intermediates in the fibrillation of the immunoglobulin light chain LEN. Biochemistry 42, 8094-8104 https://doi.org/10.1021/bi034652m
  116. Bader, R., Bamford, R., Zurdo, J., Luisi, B. F. and Dobson, C. M. (2006) Probing the mechanism of amyloidogenesis through a tandem repeat of the PI3-SH3 domain suggests a generic model for protein aggregation and fibril formation. J. Mol. Biol. 356, 189-208
  117. Quintas, A., Vaz, D. C., Cardoso, I., Saraiva, M. J. M. and Brito, R. M. M. (2001) Tetramer dissociation and monomer partial unfolding precedes protofibril formation in amyloidogenic transthyretin variants. J. Biol. Chem. 276, 27207-27213 https://doi.org/10.1074/jbc.M101024200

Cited by

  1. Exploring the binding sites and proton diffusion on insulin amyloid fibril surfaces by naphthol-based photoacid fluorescence and molecular simulations vol.7, pp.1, 2017, https://doi.org/10.1038/s41598-017-06030-4
  2. The Model of Amyloid Aggregation of Escherichia coli RNA Polymerase σ 70 Subunit Based on AFM Data and In Vitro Assays vol.66, pp.3, 2013, https://doi.org/10.1007/s12013-012-9507-2
  3. Misfolding and Amyloid Aggregation of Apomyoglobin vol.14, pp.7, 2013, https://doi.org/10.3390/ijms140714287
  4. Amyloidogenic Protein of α-Synuclein vol.33, pp.2, 2013, https://doi.org/10.7599/hmr.2013.33.2.123
  5. Controlling the aggregation and rate of release in order to improve insulin formulation: molecular dynamics study of full-length insulin amyloid oligomer models vol.18, pp.3, 2012, https://doi.org/10.1007/s00894-011-1123-3
  6. Self-assembly and sequence length dependence on nanofibrils of polyglutamine peptides vol.57, 2016, https://doi.org/10.1016/j.npep.2016.01.011
  7. Suppression of dynamin GTPase decreases α-synuclein uptake by neuronal and oligodendroglial cells: a potent therapeutic target for synucleinopathy vol.7, pp.1, 2012, https://doi.org/10.1186/1750-1326-7-38
  8. A Concise Review of Amyloidosis in Animals vol.2012, 2012, https://doi.org/10.1155/2012/427296
  9. Mysterious oligomerization of the amyloidogenic proteins vol.277, pp.14, 2010, https://doi.org/10.1111/j.1742-4658.2010.07721.x
  10. Amyloid in skin and brain: What′s the link? vol.19, pp.11, 2010, https://doi.org/10.1111/j.1600-0625.2010.01166.x
  11. Auramine-O as a Fluorescence Marker for the Detection of Amyloid Fibrils vol.116, pp.45, 2012, https://doi.org/10.1021/jp310232b
  12. Macromolecular Crowding as a Suppressor of Human IAPP Fibril Formation and Cytotoxicity vol.8, pp.7, 2013, https://doi.org/10.1371/journal.pone.0069652
  13. Protein aggregation: Mechanisms and functional consequences vol.44, pp.9, 2012, https://doi.org/10.1016/j.biocel.2012.05.023
  14. Advances in electrochemical detection for study of neurodegenerative disorders vol.405, pp.17, 2013, https://doi.org/10.1007/s00216-013-6904-3
  15. The Physical Properties and Self-Assembly Potential of the RFFFR Peptide vol.17, pp.21, 2016, https://doi.org/10.1002/cbic.201600383
  16. Kinetics of Amyloid Aggregation: A Study of the GNNQQNY Prion Sequence vol.8, pp.11, 2012, https://doi.org/10.1371/journal.pcbi.1002782
  17. Fibril Film Formation of Pseudoenantiomeric Oxymethylenehelicene Oligomers at the Liquid-Solid Interface: Structural Changes, Aggregation, and Discontinuous Heterogeneous Nucleation vol.21, pp.49, 2015, https://doi.org/10.1002/chem.201503224
  18. A Novel In Vitro CypD-Mediated p53 Aggregation Assay Suggests a Model for Mitochondrial Permeability Transition by Chaperone Systems vol.428, pp.20, 2016, https://doi.org/10.1016/j.jmb.2016.08.001
  19. Curcumin Attenuates Amyloid-β Aggregate Toxicity and Modulates Amyloid-β Aggregation Pathway vol.7, pp.1, 2016, https://doi.org/10.1021/acschemneuro.5b00214
  20. Kutane Amyloidosen vol.62, pp.1, 2011, https://doi.org/10.1007/s00105-010-2073-x
  21. Protein-Based SERS Technology Monitoring the Chemical Reactivity on an α-Synuclein-Mediated Two-Dimensional Array of Gold Nanoparticles vol.27, pp.21, 2011, https://doi.org/10.1021/la203124e
  22. Assays for α-synuclein aggregation vol.53, pp.3, 2011, https://doi.org/10.1016/j.ymeth.2010.12.008
  23. Application and use of differential scanning calorimetry in studies of thermal fluctuation associated with amyloid fibril formation vol.5, pp.3, 2013, https://doi.org/10.1007/s12551-012-0098-3
  24. Characterization of β2-microglobulin conformational intermediates associated to different fibrillation conditions vol.46, pp.8, 2011, https://doi.org/10.1002/jms.1946
  25. Ubiquitous Amyloids vol.166, pp.7, 2012, https://doi.org/10.1007/s12010-012-9549-3
  26. A New Face for Old Antibiotics: Tetracyclines in Treatment of Amyloidoses vol.56, pp.15, 2013, https://doi.org/10.1021/jm400161p
  27. Fibrillation Mechanism of a Model Intrinsically Disordered Protein Revealed by 2D Correlation Deep UV Resonance Raman Spectroscopy vol.13, pp.5, 2012, https://doi.org/10.1021/bm300193f
  28. Role of oligomers in the amyloidogenesis of primary cutaneous amyloidosis vol.65, pp.5, 2011, https://doi.org/10.1016/j.jaad.2010.09.735
  29. Formation of low-dimensional crystalline nucleus region during insulin amyloidogenesis process vol.419, pp.2, 2012, https://doi.org/10.1016/j.bbrc.2012.01.153
  30. Amyloid fibrils compared to peptide nanotubes vol.1840, pp.9, 2014, https://doi.org/10.1016/j.bbagen.2014.05.019
  31. Synthesis and in vitro characterization of some benzothiazole- and benzofuranone-derivatives for quantification of fibrillar aggregates and inhibition of amyloid-mediated peroxidase activity vol.22, pp.1, 2013, https://doi.org/10.1007/s00044-012-0012-3
  32. Amyloid formation characteristics of GNNQQNY from yeast prion protein Sup35 and its seeding with heterogeneous polypeptides vol.149, 2017, https://doi.org/10.1016/j.colsurfb.2016.10.011
  33. Effects of pH on aggregation kinetics of the repeat domain of a functional amyloid, Pmel17 vol.107, pp.50, 2010, https://doi.org/10.1073/pnas.1006424107
  34. A computational study of the self-assembly of the RFFFR peptide vol.17, pp.44, 2015, https://doi.org/10.1039/C5CP01324K
  35. Mechanisms of amyloid fibril formation - focus on domain-swapping vol.278, pp.13, 2011, https://doi.org/10.1111/j.1742-4658.2011.08149.x
  36. Natural Biomolecules and Protein Aggregation: Emerging Strategies against Amyloidogenesis vol.13, pp.12, 2012, https://doi.org/10.3390/ijms131217121
  37. A Generic Crystallization-like Model That Describes the Kinetics of Amyloid Fibril Formation vol.287, pp.36, 2012, https://doi.org/10.1074/jbc.M112.375345
  38. Role of Metal Ions in the Self-assembly of the Alzheimer’s Amyloid-β Peptide vol.52, pp.21, 2013, https://doi.org/10.1021/ic4003059
  39. Photoconductivity of Pea-Pod-Type Chains of Gold Nanoparticles Encapsulated within Dielectric Amyloid Protein Nanofibrils of α-Synuclein vol.123, pp.6, 2011, https://doi.org/10.1002/ange.201004301
  40. Full length amylin oligomer aggregation: insights from molecular dynamics simulations and implications for design of aggregation inhibitors vol.32, pp.10, 2014, https://doi.org/10.1080/07391102.2013.832635
  41. Proteomic Screening for Amyloid Proteins vol.9, pp.12, 2014, https://doi.org/10.1371/journal.pone.0116003
  42. Heme binding site in apomyoglobin may be effectively targeted with small molecules to control aggregation vol.45, pp.2, 2013, https://doi.org/10.1016/j.biocel.2012.10.004
  43. Amyloid Fibril Formation by the Chain B Subunit of Monellin Occurs by a Nucleation-Dependent Polymerization Mechanism vol.53, pp.7, 2014, https://doi.org/10.1021/bi401467p
  44. Covalent Structural Changes in Unfolded GroES That Lead to Amyloid Fibril Formation Detected by NMR vol.286, pp.24, 2011, https://doi.org/10.1074/jbc.M111.228445
  45. Photoconductivity of Pea-Pod-Type Chains of Gold Nanoparticles Encapsulated within Dielectric Amyloid Protein Nanofibrils of α-Synuclein vol.50, pp.6, 2011, https://doi.org/10.1002/anie.201004301
  46. Interaction of polymers with amyloidogenic peptides vol.67, pp.1, 2017, https://doi.org/10.1002/pi.5483
  47. Morphological Evaluation of Meta-stable Oligomers of α-Synuclein with Small-Angle Neutron Scattering vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-32655-0
  48. Molecular and Clinical Aspects of Protein Aggregation Assays in Neurodegenerative Diseases vol.55, pp.9, 2018, https://doi.org/10.1007/s12035-018-0926-y
  49. Phase transformations of bovine serum albumin: Evidences from Rayleigh-Brillouin light scattering pp.03770486, 2019, https://doi.org/10.1002/jrs.5547