Ligand binding to distinct states diverts aggregation of an amyloid-forming protein (original) (raw)

References

  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).
    Article CAS PubMed Google Scholar
  2. Chiti, F. & Dobson, C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333–366 (2006).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed PubMed Central Google Scholar
  4. Glabe, C.G. Structural classification of toxic amyloid oligomers. J. Biol. Chem. 283, 29639–29643 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  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).
    Article CAS PubMed Google Scholar
  6. Gosal, W.S. et al. Competing pathways determine fibril morphology in the self-assembly of β2-microglobulin into amyloid. J. Mol. Biol. 351, 850–864 (2005).
    Article CAS PubMed Google Scholar
  7. Carrell, R.W. Cell toxicity and conformational disease. Trends Cell Biol. 15, 574–580 (2005).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  11. Regazzoni, L. et al. A combined high-resolution mass spectrometric and in silico approach for the characterization of small ligands of β2-microglobulin. ChemMedChem 5, 1015–1025 (2010).
    Article CAS PubMed Google Scholar
  12. Cohen, F.E. & Kelly, J.W. Therapeutic approaches to protein-misfolding diseases. Nature 426, 905–909 (2003).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  14. Feng, B.Y. et al. Small-molecule aggregates inhibit amyloid polymerization. Nat. Chem. Biol. 4, 197–199 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  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).
    Article CAS PubMed Google Scholar
  16. McGovern, S.L., Caselli, E., Grigorieff, N. & Shoichet, B.K. A common mechanism underlying promiscuous inhibitors from virtual and high-throughput screening. J. Med. Chem. 45, 1712–1722 (2002).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed PubMed Central Google Scholar
  19. Platt, G.W., Routledge, K.E., Homans, S.W. & Radford, S.E. Fibril growth kinetics reveal a region of β2-microglobulin important for nucleation and elongation of aggregation. J. Mol. Biol. 378, 251–263 (2008).
    Article CAS PubMed PubMed Central Google Scholar
  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).
    Article CAS PubMed PubMed Central Google Scholar
  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).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed PubMed Central Google Scholar
  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).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  27. Smith, D.P., Radford, S.E. & Ashcroft, A.E. Elongated oligomers in β2-microglobulin amyloid assembly revealed by ion mobility spectrometry-mass spectrometry. Proc. Natl. Acad. Sci. USA 107, 6794–6798 (2010).
    Article CAS PubMed Google Scholar
  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).
    Article CAS Google Scholar
  29. Kayed, R. et al. Annular protofibrils are a structurally and functionally distinct type of amyloid oligomer. J. Biol. Chem. 284, 4230–4237 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  30. O'Nuallain, B. & Wetzel, R. Conformational Abs recognizing a generic amyloid fibril epitope. Proc. Natl. Acad. Sci. USA 99, 1485–1490 (2002).
    Article CAS PubMed Google Scholar
  31. Xue, W.F. et al. Fibril fragmentation enhances amyloid cytotoxicity. J. Biol. Chem. 284, 34272–34282 (2009).
    Article CAS PubMed PubMed Central Google Scholar
  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).
    Article CAS Google Scholar
  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).
    Article CAS PubMed PubMed Central Google Scholar
  34. Platt, G.W., McParland, V.J., Kalverda, A.P., Homans, S.W. & Radford, S.E. Dynamics in the unfolded state of β2-microglobulin studied by NMR. J. Mol. Biol. 346, 279–294 (2005).
    Article CAS PubMed Google Scholar
  35. Tomiyama, T. et al. Rifampicin prevents the aggregation and neurotoxicity of Aβ protein in vitro. Biochem. Biophys. Res. Commun. 204, 76–83 (1994).
    Article CAS PubMed Google Scholar
  36. Borysik, A.J., Radford, S.E. & Ashcroft, A.E. Co-populated conformational ensembles of β2-microglobulin uncovered quantitatively by electrospray ionisation mass spectroscopy. J. Biol. Chem. 279, 27069–27077 (2004).
    Article CAS PubMed Google Scholar
  37. Smith, D.P., Jones, S., Serpell, L.C., Sunde, M. & Radford, S.E. A systematic investigation into the effect of protein destabilization on β2-microglobulin amyloid formation. J. Mol. Biol. 330, 943–954 (2003).
    Article CAS PubMed Google Scholar
  38. Xue, W.F., Homans, S.W. & Radford, S.E. Systematic analysis of nucleation-dependent polymerization reveals new insights into the mechanism of amyloid self-assembly. Proc. Natl. Acad. Sci. USA 105, 8926–8931 (2008).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed PubMed Central Google Scholar
  40. Debelouchina, G.T., Platt, G.W., Bayro, M.J., Radford, S.E. & Griffin, R.G. Magic angle spinning NMR analysis of β2-microglobulin amyloid fibrils in two distinct morphologies. J. Am. Chem. Soc. 132, 10414–10423 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  41. Gazit, E. A possible role for π-stacking in the self-assembly of amyloid fibrils. FASEB J. 16, 77–83 (2002).
    Article CAS PubMed Google Scholar
  42. Taniguchi, S. et al. Inhibition of heparin-induced tau filament formation by phenothiazines, polyphenols, and porphyrins. J. Biol. Chem. 280, 7614–7623 (2005).
    Article CAS PubMed Google Scholar
  43. Ehrnhoefer, D.E. et al. EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat. Struct. Mol. Biol. 15, 558–566 (2008).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed Google Scholar
  45. Ladiwala, A.R.A. et al. Resveratrol selectively remodels soluble oligomers and fibrils of amyloid Aβ off-pathway conformers. J. Biol. Chem. 285, 24228–24237 (2010).
    Article CAS PubMed PubMed Central Google Scholar
  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).
    Article CAS PubMed Google Scholar
  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).
    Article CAS PubMed PubMed Central Google Scholar
  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).
    Article CAS PubMed Google Scholar
  49. Kayed, R. et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486–489 (2003).
    Article CAS PubMed Google Scholar
  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).
    Article PubMed PubMed Central Google Scholar

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