Ligand binding to distinct states diverts aggregation of an amyloid-forming protein

Nature Chemical Biology

Volumn 7, Issue 10, 2011, Pages 730-739

  Woods, Lucy A ^a   Platt, Geoffrey W ^a   Hellewell, Andrew L ^a   Hewitt, Eric W ^a   Homans, Steve W ^a   Ashcroft, Alison E ^a   Radford, Sheena E ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; BETA 2 MICROGLOBULIN; OLIGOMER; RIFAMYCIN;

ARTICLE; BIOCHEMISTRY; ELECTROSPRAY MASS SPECTROMETRY; FIBRIN FORMATION; ION MOBILITY SPECTROMETRY; LIGAND BINDING; PRIORITY JOURNAL;

EID: 80052970179     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.635     Document Type: Article

References (50)

1. Sipe, J. D. et al. Amyloid fibril protein nomenclature: 2010 recommendations from the nomenclature committee of the International Society of Amyloidosis. Amyloid 17, 101-104 (2010).
2. Chiti, F. & Dobson, C. M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366 (2006). (Pubitemid 44118036)
3. Bernstein, S. L. et al. Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat. Chem. 1, 326-331 (2009).
4. Glabe, C. G. Structural classification of toxic amyloid oligomers. J. Biol. Chem. 283, 29639-29643 (2008).
5. Necula, M., Kayed, R., Milton, S. & Glabe, C. G. Small molecule inhibitors of aggregation indicate that Aβ oligomerization and fibrillization pathways are independent and distinct. J. Biol. Chem. 282, 10311-10324 (2007). (Pubitemid 47093410)
6. 2-microglobulin into amyloid. J. Mol. Biol. 351, 850-864 (2005). (Pubitemid 41111901)
7. Carrell, R. W. Cell toxicity and conformational disease. Trends Cell Biol. 15, 574-580 (2005). (Pubitemid 41619421)
8. Martins, I. C. et al. Lipids revert inert Aβ amyloid fibrils to neurotoxic protofibrils that affect learning in mice. EMBO J. 27, 224-233 (2008).
9. Lee, H. G. et al. Challenging the amyloid cascade hypothesis: Senile plaques and amyloid-β as protective adaptations to Alzheimer disease. Ann. NY Acad. Sci. 1019, 1-4 (2004).
10. Porat, Y., Abramowitz, A. & Gazit, E. Inhibition of amyloid fibril formation by polyphenols: Structural similarity and aromatic interactions as a common inhibition mechanism. Chem. Biol. Drug Des. 67, 27-37 (2006). (Pubitemid 43881385)
11. 2-microglobulin. ChemMedChem 5, 1015-1025 (2010).
12. Cohen, F. E. & Kelly, J. W. Therapeutic approaches to protein-misfolding diseases. Nature 426, 905-909 (2003). (Pubitemid 38056884)
13. Conway, K. A., Rochet, J. C., Bieganski, R. M. & Lansbury, P. T. Kinetic stabilization of the α-synuclein protofibril by a dopamine-α-synuclein adduct. Science 294, 1346-1349 (2001). (Pubitemid 33063102)
14. Feng, B. Y. et al. Small-molecule aggregates inhibit amyloid polymerization. Nat. Chem. Biol. 4, 197-199 (2008). (Pubitemid 351264126)
15. Lendel, C. et al. On the mechanism of non-specific inhibitors of protein aggregation: Dissecting the interactions of α-synuclein with Congo red and lacmoid. Biochemistry 48, 8322-8334 (2009).
16. McGovern, S. L., Caselli, E., Grigorieff, N. & Shoichet, B. K. A common mechanism underlying promiscuous inhibitors from virtual and highthroughput screening. J. Med. Chem. 45, 1712-1722 (2002). (Pubitemid 34293537)
17. Ladiwala, A. R., Dordick, J. S. & Tessier, P. M. Aromatic small molecules remodel toxic soluble oligomers of amyloid β through three independent pathways. J. Biol. Chem. 286, 3209-3218 (2011).
18. Armstrong, A. H., Chen, J., McKoy, A. F. & Hecht, M. H. Mutations that replace aromatic side chains promote aggregation of the Alzheimer's Aβ peptide. Biochemistry 50, 4058-4067 (2011).
19. 2-microglobulin important for nucleation and elongation of aggregation. J. Mol. Biol. 378, 251-263 (2008).
20. Routledge, K. E., Tartaglia, G. G., Platt, G. W., Vendruscolo, M. & Radford, S. E. Competition between intra-molecular and inter-molecular interactions in an amyloid forming protein. J. Mol. Biol. 389, 776-786 (2009).
21. Meng, F., Marek, P., Potter, K. J., Verchere, C. B. & Raleigh, D. P. Rifampicin does not prevent amyloid fibril formation by human islet amyloid polypeptide but does inhibit fibril thioflavin-T interactions: Implications for mechanistic studies of β-cell death. Biochemistry 47, 6016-6024 (2008). (Pubitemid 351770031)
22. Lieu, V. H., Wu, J. W., Wang, S. S. S. & Wu, C. H. Inhibition of amyloid fibrillization of hen egg-white lysozymes by rifampicin and p-benzoquinone. Biotechnol. Prog. 23, 698-706 (2007). (Pubitemid 46911197)
23. Li, J., Zhu, M., Rajamani, S., Uversky, V. N. & Fink, A. L. Rifampicin inhibits α-synuclein fibrillation and disaggregates fibrils. Chem. Biol. 11, 1513-1521 (2004). (Pubitemid 39527278)
24. Tomiyama, T., Kaneko, H., Kataoka, K., Asano, S. & Endo, N. Rifampicin inhibits the toxicity of pre-aggregated amyloid peptides by binding to peptide fibrils and preventing amyloid-cell interaction. Biochem. J. 322, 859-865 (1997). (Pubitemid 27135636)
25. Carazzone, C. et al. Sulfonated molecules that bind a partially structured species of β2-microglobulin also influence refolding and fibrillogenesis. Electrophoresis 29, 1502-1510 (2008). (Pubitemid 351524361)
26. Smith, A. M., Jahn, T. R., Ashcroft, A. E. & Radford, S. E. Direct observation of oligomeric species formed in the early stages of amyloid fibril formation using electrospray ionisation mass spectrometry. J. Mol. Biol. 364, 9-19 (2006). (Pubitemid 44634528)
27. 2-microglobulin amyloid assembly revealed by ion mobility spectrometrymass spectrometry. Proc. Natl. Acad. Sci. USA 107, 6794-6798 (2010).
28. Armstrong, D. W., Schneiderheinze, J., Nair, U., Magid, L. J. & Butler, P. D. Self-association of rifamycin B: Possible effects on molecular recognition. J. Phys. Chem. B 103, 4338-4341 (1999). (Pubitemid 129702701)
29. Kayed, R. et al. Annular protofibrils are a structurally and functionally distinct type of amyloid oligomer. J. Biol. Chem. 284, 4230-4237 (2009).
30. O'Nuallain, B. & Wetzel, R. Conformational Abs recognizing a generic amyloid fibril epitope. Proc. Natl. Acad. Sci. USA 99, 1485-1490 (2002). (Pubitemid 34136519)
31. Xue, W. F. et al. Fibril fragmentation enhances amyloid cytotoxicity. J. Biol. Chem. 284, 34272-34282 (2009).
32. Smith, D. P. et al. Deciphering drift time measurements from travelling wave ion mobility spectrometry-mass spectrometry studies. Eur. J. Mass Spectrom. (Chichester, Eng.) 15, 113-130 (2009).
33. Smith, D. P., Giles, K., Bateman, R. H., Radford, S. E. & Ashcroft, A. E. Monitoring copopulated conformational states during protein folding events using electrospray ionization-ion mobility spectrometry-mass spectrometry. J. Am. Soc. Mass Spectrom. 18, 2180-2190 (2007). (Pubitemid 350161334)
34. 2- microglobulin studied by NMR. J. Mol. Biol. 346, 279-294 (2005). (Pubitemid 40128321)
35. Tomiyama, T. et al. Rifampicin prevents the aggregation and neurotoxicity of Aβ protein in vitro. Biochem. Biophys. Res. Commun. 204, 76-83 (1994). (Pubitemid 24335264)
36. 2-microglobulin uncovered quantitatively by electrospray ionisation mass spectroscopy. J. Biol. Chem. 279, 27069-27077 (2004). (Pubitemid 38812543)
37. 2-microglobulin amyloid formation. J. Mol. Biol. 330, 943-954 (2003). (Pubitemid 36818893)
38. Xue, W. F., Homans, S. W. & Radford, S. E. Systematic analysis of nucleationdependent polymerization reveals new insights into the mechanism of amyloid self-assembly. Proc. Natl. Acad. Sci. USA 105, 8926-8931 (2008).
39. Ladner, C. L. et al. Stacked sets of parallel, in-register beta-strands of β2-microglobulin in amyloid fibrils revealed by site-directed spin labeling and chemical labeling. J. Biol. Chem. 285, 17137-17147 (2010).
40. 2- microglobulin amyloid fibrils in two distinct morphologies. J. Am. Chem. Soc. 132, 10414-10423 (2010).
41. Gazit, E. A possible role for π-stacking in the self-assembly of amyloid fibrils. FASEB J. 16, 77-83 (2002). (Pubitemid 34027953)
42. Taniguchi, S. et al. Inhibition of heparin-induced tau filament formation by phenothiazines, polyphenols, and porphyrins. J. Biol. Chem. 280, 7614-7623 (2005). (Pubitemid 40349654)
43. Ehrnhoefer, D. E. et al. EGCG redirects amyloidogenic polypeptides into unstructured, of-pathway oligomers. Nat. Struct. Mol. Biol. 15, 558-566 (2008). (Pubitemid 351799141)
44. Bieschke, J. et al. EGCG remodels mature α-synuclein and amyloid-β fibrils and reduces cellular toxicity. Proc. Natl. Acad. Sci. USA 107, 7710-7715 (2010).
45. Ladiwala, A. R. A. et al. Resveratrol selectively remodels soluble oligomers and fibrils of amyloid Aβ of-pathway conformers. J. Biol. Chem. 285, 24228-24237 (2010).
46. Grabenauer, M., Wu, C., Soto, P., Shea, J. E. & Bowers, M. T. Oligomers of the prion protein fragment 106-126 are likely assembled from beta-hairpins in solution, and methionine oxidation inhibits assembly without altering the peptide's monomeric conformation. J. Am. Chem. Soc. 132, 532-539 (2010).
47. Dupuis, N. F., Wu, C., Shea, J. E. & Bowers, M. T. Human islet amyloid polypeptide monomers form ordered beta-hairpins: A possible direct amyloidogenic precursor. J. Am. Chem. Soc. 131, 18283-18292 (2009).
48. Ashcroft, A. E. Mass spectrometry and the amyloid problem-how far can we go in the gas phase? J. Am. Soc. Mass Spectrom. 21, 1087-1096 (2010).
49. Kayed, R. et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 (2003). (Pubitemid 36444329)
50. Laurén, J., Gimbel, D. A., Nygaard, H. B., Gilbert, J. W. & Strittmatter, S. M. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-β oligomers. Nature 457, 1128-1132 (2009).