1887
banner image
No data available.
Please log in to see this content.
You have no subscription access to this content.
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.
The full text of this article is not currently available.
f
Structural fingerprints and their evolution during oligomeric vs. oligomer-free amyloid fibril growth
Rent:
Rent this article for
Access full text Article
/content/aip/journal/jcp/139/12/10.1063/1.4811343
1.
1. C. R. Berland, G. M. Thurston, M. Kondo, M. L. Broide, J. Pande, O. Ogun, and G. B. Benedek, Proc. Natl. Acad. Sci. U.S.A. 89, 1214 (1992);
http://dx.doi.org/10.1073/pnas.89.4.1214
1.M. Muschol and F. Rosenberger, J. Chem. Phys. 107 (6), 1953 (1997);
http://dx.doi.org/10.1063/1.474547
1.O. Galkin, K. Chen, R. L. Nagel, R. E. Hirsch, and P. G. Vekilov, Proc. Natl. Acad. Sci. U.S.A. 99(13), 8479 (2002);
http://dx.doi.org/10.1073/pnas.122055299
1.P. R. tenWolde and D. Frenkel, Science 277(5334), 1975 (1997);
http://dx.doi.org/10.1126/science.277.5334.1975
1.D. Rosenbaum, P. C. Zamora, and C. F. Zukoski, Phys. Rev. Lett. 76(1), 150 (1996);
http://dx.doi.org/10.1103/PhysRevLett.76.150
1.F. Sciortino, K. U. Prasad, D. W. Urry, and M. U. Palma, Chem. Phys. Lett. 153(6), 557 (1988);
http://dx.doi.org/10.1016/0009-2614(88)85260-6
1.F. Sciortino, D. W. Urry, M. U. Palma, and K. U. Prasad, Biopolymers 29(10–11), 1401 (1990);
http://dx.doi.org/10.1002/bip.360291007
1.S. M. Vaiana, M. B. Palma-Vittorelli, and M. U. Palma, Proteins: Struct., Funct., Bioinf. 51(1), 147 (2003).
http://dx.doi.org/10.1002/prot.10306
2.
2. P. Li, S. Banjade, H.-C. Cheng, S. Kim, B. Chen, L. Guo, M. Llaguno, J. V. Hollingsworth, D. S. King, S. F. Banani, P. S. Russo, Q.-X. Jiang, B. T. Nixon, and M. K. Rosen, Nature (London) 483(7389), 336 (2012).
http://dx.doi.org/10.1038/nature10879
3.
3. J. D. O’Connell, A. Zhao, A. D. Ellington, and E. M. Marcotte, Annu. Rev. Cell Dev. Biol. 28(1), 89 (2012).
http://dx.doi.org/10.1146/annurev-cellbio-101011-155841
4.
4. J. W. Kelly, Curr. Opin. Struct. Biol. 6(1), 11 (1996).
http://dx.doi.org/10.1016/S0959-440X(96)80089-3
5.
5. F. Chiti and C. M. Dobson, Annu. Rev. Biochem. 75(1), 333 (2006).
http://dx.doi.org/10.1146/annurev.biochem.75.101304.123901
6.
6. R. Halfmann, D. F. Jarosz, S. K. Jones, A. Chang, A. K. Lancaster, and S. Lindquist, Nature (London) 482(7385), 363 (2012).
http://dx.doi.org/10.1038/nature10875
7.
7. D. M. Fowler, A. V. Koulov, C. Alory-Jost, M. S. Marks, W. E. Balch, and J. W. Kelly, PLoS Biol. 4(1), e61 (2005);
http://dx.doi.org/10.1371/journal.pbio.0040006
7.D. Otzen, Prion 4(4), 256 (2010);
http://dx.doi.org/10.4161/pri.4.4.13676
7.S. K. Maji, M. H. Perrin, M. R. Sawaya, S. Jessberger, K. Vadodaria, R. A. Rissman, P. S. Singru, K. P. R. Nilsson, R. Simon, D. Schubert, D. Eisenberg, J. Rivier, P. Sawchenko, W. Vale, and R. Riek, Science 325(5938), 328 (2009).
http://dx.doi.org/10.1126/science.1173155
8.
8. T. R. Jahn, O. S. Makin, K. L. Morris, K. E. Marshall, P. Tian, P. Sikorski, and L. C. Serpell, J. Mol. Biol. 395(4), 717 (2010);
http://dx.doi.org/10.1016/j.jmb.2009.09.039
8.M. Sunde and C. C. F. Blake, Adv. Protein Chem. 50, 123 (1997);
http://dx.doi.org/10.1016/S0065-3233(08)60320-4
8.M. Fändrich, Cell. Mol. Life Sci. 64(16), 2066 (2007).
http://dx.doi.org/10.1007/s00018-007-7110-2
9.
9. E. H. Koo, P. T. Lansbury, and J. W. Kelly, Proc. Natl. Acad. Sci. U.S.A. 96, 9989 (1999).
http://dx.doi.org/10.1073/pnas.96.18.9989
10.
10. C. M. Dobson, Trends Biochem. Sci. 24, 329 (1999).
http://dx.doi.org/10.1016/S0968-0004(99)01445-0
11.
11. V. N. Uversky, A. Fernandez, and A. L. Fink, in Protein Misfolding, Aggregation and Conformational Diseases. Part A: Protein Aggregation and Conformational Diseases, edited by N. U. Vladimir and A. L. Fink (Springer, New York, 2006);
11.V. N. Uversky and A. L. Fink, Biochim. Biophys. Acta 1698, 131 (2004).
http://dx.doi.org/10.1016/j.bbapap.2003.12.008
12.
12. T. R. Jahn, G. A. Tennent, and S. E. Radford, J. Biol. Chem. 283(25), 17279 (2008).
http://dx.doi.org/10.1074/jbc.M710351200
13.
13. W. S. Gosal, I. J. Morten, E. W. Hewitt, D. A. Smith, N. H. Thompson, and S. E. Radford, J. Mol. Biol. 351, 850 (2005).
http://dx.doi.org/10.1016/j.jmb.2005.06.040
14.
14. C. Goldsbury, P. Frey, V. Olivieri, U. Aebi, and S. A. Müller, J. Mol. Biol. 352(2), 282 (2005);
http://dx.doi.org/10.1016/j.jmb.2005.07.029
14.S. Hess, S. Lindquist, and T. Scheibel, EMBO Rep. 8, 1196 (2007).
http://dx.doi.org/10.1038/sj.embor.7401096
15.
15. S. E. Hill, T. Miti, T. Richmond, and M. Muschol, PLoS ONE 6(4), e181711 (2011).
http://dx.doi.org/10.1371/journal.pone.0018171
16.
16. M. N. N. Vieira, L. Forny-Germano, L. M. Saraiva, A. Sebollela, A. M. B. Martinez, J.-C. Houzel, F. G. De Felice, and S. T. Ferreira, J. Neurochem. 103(2), 736 (2007);
http://dx.doi.org/10.1111/j.1471-4159.2007.04809.x
16.R. Kayed, E. Head, F. Sarsoza, T. Saing, C. Cotman, M. Necula, L. Margol, J. Wu, L. Breydo, J. Thompson, S. Rasool, T. Gurlo, P. Butler, and C. Glabe, Mol. Neurodegeneration 2(1), 18 (2007);
http://dx.doi.org/10.1186/1750-1326-2-18
16.J. P. Cleary, D. M. Walsh, J. J. Hofmeister, G. M. Shankar, M. A. Kuskowski, D. J. Selkoe, and K. H. Ashe, Nat. Neurosci. 8, 79 (2005);
http://dx.doi.org/10.1038/nn1372
16.R. Kayed, Y. Sokolov, B. Edmonds, T. M. McIntire, S. C. Milton, J. E. Hall, and C. G. Glabe, J. Biol. Chem. 279(45), 46363 (2004);
http://dx.doi.org/10.1074/jbc.C400260200
16.R. Kayed, E. Head, J. L. Thompson, T. M. McIntire, S. C. Milton, C. W. Cotman, and C. G. Glabe, Science 300, 486 (2003);
http://dx.doi.org/10.1126/science.1079469
16.D. M. Walsh, I. Klyubin, J. V. Fadeeva, W. K. Cullen, R. Anwyl, M. S. Wolfe, M. J. Rowan, and D. J. Selkoe, Nature (London) 416(6880), 535 (2002).
http://dx.doi.org/10.1038/416535a
17.
17. R. Kodali and R. Wetzel, Curr. Opin. Struct. Biol. 17(1), 48 (2007).
http://dx.doi.org/10.1016/j.sbi.2007.01.007
18.
18. G. Zandomeneghi, M. R. H. Krebs, M. G. McCammon, and M. Fändrich, Protein Sci. 13(12), 3314 (2004).
http://dx.doi.org/10.1110/ps.041024904
19.
19. A. S. Parmar, P. E. Gottschall, and M. Muschol, Biophys. Chem. 129, 224 (2007).
http://dx.doi.org/10.1016/j.bpc.2007.06.002
20.
20. D. R. Booth, M. Sunde, V. Bellotti, C. V. Robinson, W. L. Hutchinson, P. E. Fraser, P. N. Hawkins, C. M. Dobson, S. E. Radford, C. F. F. Blake, and M. B. Pepys, Nature (London) 385, 787 (1997);
http://dx.doi.org/10.1038/385787a0
20.J. D. Gillmore, D. R. Booth, S. Madhoo, M. B. Pepys, and P. N. Hawkins, Nephrol. Dial Transplant 14(11), 2639 (1999);
http://dx.doi.org/10.1093/ndt/14.11.2639
20.M. B. Pepys, P. N. Hawkins, D. R. Booth, D. M. Vigushin, G. A. Tennent, A. K. Soutar, N. Totty, O. Nguyen, C. C. F. Blake, C. J. Terry, T. G. Feest, A. M. Zalin, and J. J. Hsuan, Nature (London) 362(6420), 553 (1993).
http://dx.doi.org/10.1038/362553a0
21.
21. A. J. Trexler and M. R. Nilsson, Curr. Protein Pept. Sci. 8, 537 (2007).
http://dx.doi.org/10.2174/138920307783018659
22.
22. L. N. Arnaudov and R. de Vries, Biophys. J. 88(1), 515 (2005);
http://dx.doi.org/10.1529/biophysj.104.048819
22.S. E. Hill, J. Robinson, G. Matthews, and M. Muschol, Biophys. J. 96, 3781 (2009);
http://dx.doi.org/10.1016/j.bpj.2009.01.044
22.M. R. H. Krebs, D. K. Wilkins, E. W. Chung, M. C. Pitkeathly, A. K. Chamberlain, J. Zurdo, C. V. Robinson, and C. M. Dobson, J. Mol. Biol. 300(3), 541 (2000).
http://dx.doi.org/10.1006/jmbi.2000.3862
23.
23. E. Frare, P. Polverino de Laureto, J. Zurdo, C. M. Dobson, and A. Fontana, J. Mol. Biol. 340(5), 1153 (2004).
http://dx.doi.org/10.1016/j.jmb.2004.05.056
24.
24. R. Mishra, K. Sörgjerd, S. Nyström, A. Nordigården, Y.-C. Yu, and P. Hammarström, J. Mol. Biol. 366, 1029 (2007).
http://dx.doi.org/10.1016/j.jmb.2006.11.084
25.
25. M. Biancalana and S. Koide, Biochim. Biophys. Acta 1804(7), 1405 (2010);
http://dx.doi.org/10.1016/j.bbapap.2010.04.001
25.P. S. Vassar and C. F. Culling, Arch. Pathol. 68, 232 (1959).
26.
26. D. P. Smith, S. Jones, L. C. Serpell, M. Sunde, and S. E. Radford, J. Mol. Biol. 330(5), 943 (2003).
http://dx.doi.org/10.1016/S0022-2836(03)00687-9
27.
27. A. I. Sulatskaya, I. M. Kuznetsova, and K. K. Turoverov, J. Phys. Chem. B 115(39), 11519 (2011).
http://dx.doi.org/10.1021/jp207118x
28.
28. H. Z. Cummins, in Photon Correlation and Light Beating Spectroscopy, edited by H. Z. Cummins and E. R. Pike (Plenum Press, New York, 1973).
29.
29. M. Tanaka, S. R. Collins, B. H. Toyama, and J. S. Weissman, Nature (London) 442(7102), 585 (2006);
http://dx.doi.org/10.1038/nature04922
29.J. Masel, V. A. A. Jansen, and M. A. Nowak, Biophys. Chem. 77, 139 (1999);
http://dx.doi.org/10.1016/S0301-4622(99)00016-2
29.T. P. J. Knowles, C. A. Waudby, G. L. Devlin, S. I. A. Cohen, A. Aguzzi, M. Vendruscolo, E. M. Terentjev, M. E. Welland, and C. M. Dobson, Science 326, 1533 (2009).
http://dx.doi.org/10.1126/science.1178250
30.
30. T. R. Jahn and S. E. Radford, Arch. Biochem. Biophys. 469, 100 (2008).
http://dx.doi.org/10.1016/j.abb.2007.05.015
31.
31. M. Necula, R. Kayed, S. Milton, and C. G. Glabe, J. Biol. Chem. 282(14), 10311 (2007).
http://dx.doi.org/10.1074/jbc.M608207200
32.
32. W. Y. Yang, E. Larios, and M. Gruebele, J. Am. Chem. Soc. 125(52), 16220 (2003).
http://dx.doi.org/10.1021/ja0360081
33.
33. A. Laganowsky, C. Liu, M. R. Sawaya, J. P. Whitelegge, J. Park, M. Zhao, A. Pensalfini, A. B. Soriaga, M. Landau, P. K. Teng, D. Cascio, C. Glabe, and D. Eisenberg, Science 335(6073), 1228 (2012).
http://dx.doi.org/10.1126/science.1213151
http://aip.metastore.ingenta.com/content/aip/journal/jcp/139/12/10.1063/1.4811343
Loading
/content/aip/journal/jcp/139/12/10.1063/1.4811343
Loading

Data & Media loading...

Loading

Article metrics loading...

/content/aip/journal/jcp/139/12/10.1063/1.4811343
2013-07-01
2014-10-21

Abstract

Deposits of fibrils formed by disease-specific proteins are the molecular hallmark of such diverse human disorders as Alzheimer's disease, type II diabetes, or rheumatoid arthritis. Amyloid fibril formation by structurally and functionally unrelated proteins exhibits many generic characteristics, most prominently the cross β-sheet structure of their mature fibrils. At the same time, amyloid formation tends to proceed along one of two separate assembly pathways yielding either stiff monomeric filaments or globular oligomers and curvilinear protofibrils. Given the focus on oligomers as major toxic species, the very existence of an oligomer-free assembly pathway is significant. Little is known, though, about the structure of the various intermediates emerging along different pathways and whether the pathways converge towards a common or distinct fibril structures. Using infrared spectroscopy we probed the structural evolution of intermediates and late-stage fibrils formed during lysozyme amyloid assembly along an oligomeric and oligomer-free pathway. Infrared spectroscopy confirmed that both pathways produced amyloid-specific β-sheet peaks, but at pathway-specific wavenumbers. We further found that the amyloid-specific dye thioflavin T responded to all intermediates along either pathway. The relative amplitudes of thioflavin T fluorescence responses displayed pathway-specific differences and could be utilized for monitoring the structural evolution of intermediates. Pathway-specific structural features obtained from infrared spectroscopy and Thioflavin T responses were identical for fibrils grown at highly acidic or at physiological pH values and showed no discernible effects of protein hydrolysis. Our results suggest that late-stage fibrils formed along either pathway are amyloidogenic in nature, but have distinguishable structural fingerprints. These pathway-specific fingerprints emerge during the earliest aggregation events and persist throughout the entire cascade of aggregation intermediates formed along each pathway.

Loading

Full text loading...

/deliver/fulltext/aip/journal/jcp/139/12/1.4811343.html;jsessionid=qamurknnj4dl.x-aip-live-06?itemId=/content/aip/journal/jcp/139/12/10.1063/1.4811343&mimeType=html&fmt=ahah&containerItemId=content/aip/journal/jcp
true
true
This is a required field
Please enter a valid email address
752b84549af89a08dbdd7fdb8b9568b5 journal.articlezxybnytfddd
Scitation: Structural fingerprints and their evolution during oligomeric vs. oligomer-free amyloid fibril growth
http://aip.metastore.ingenta.com/content/aip/journal/jcp/139/12/10.1063/1.4811343
10.1063/1.4811343
SEARCH_EXPAND_ITEM