Ion mobilityg-mass spectrometry reveals a conformational conversion from random assembly to β-sheet in amyloid fibril formation

Nature Chemistry

Volumn 3, Issue 2, 2011, Pages 172-177

  Bleiholder, Christian ^a   Dupuis, Nicholas F ^a   Wyttenbach, Thomas ^a   Bowers, Michael T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; PEPTIDE;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; MASS SPECTROMETRY; METHODOLOGY; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; AMYLOID; HUMANS; MASS SPECTROMETRY; MODELS, MOLECULAR; PEPTIDES; PROTEIN STRUCTURE, SECONDARY;

EID: 79251631002     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.945     Document Type: Article

References (41)

1. Gleiter, R., Werz, D. B. & Rausch, B. J. A world beyond hydrogen bonds? Chalcogen-chalcogen interactions yielding tubular structures. Chem. Eur. J. 9, 2676-2683 (2003).
2. Bong, D. T., Clark, T. D., Granja, J. R. & Ghadiri, M. R. Self-assembling organic nanotubes. Angew. Chem. Int. Ed. 40, 988-1011 (2001).
3. Hamley, I. W. Peptide fibrillization. Angew. Chem. Int. Ed. 46, 8128-8147 (2007).
4. Couet, J., Samuel, J. D., Kopyshev, A., Santer, S. & Biesalski, M. Peptide-polymer hybrid nanotubes. Angew. Chem. Int. Ed. 44, 3297-3301 (2005).
5. Unwin, N. Acetylcholine receptor channel imaged in the open state. Nature 373, 37-43 (1995).
6. Ghadiri, M. R., Granja, J. R., Milligan, R. A., McRee, D. E. & Khazanovich, N. Self-assembling organic nanotubes based on a cyclic peptide architecture. Nature 366, 324-327 (1993).
7. Lear, J. D., Wasserman, Z. R. & DeGrado, W. F. Synthetic amphiphilic peptide models for protein ion channels. Science 240, 1177-1181 (1988).
8. Fowler, D. M., Koulov, A. V., Balch, W. E. & Kelly, J. W. Functional amyloid - from bacteria to humans. Trends Biochem. Sci. 32, 217-224 (2007).
9. Sawaya, M. R. et al. Atomic structures of amyloid cross-b spines reveal varied steric zippers. Nature 447, 453-457 (2007).
10. Nelson, R. et al. Structure of the cross-b spine of amyloid-like fibrils. Nature 435, 773-778 (2005).
11. Hartgerink, J. D., Clark, T. D. & Ghadiri, M. R. Peptide nanotubes and beyond. Chem. Eur. J. 4, 1367-1372 (1998).
12. Sipe, J. D. & Cohen, A. S. Review: history of the amyloid fibril. J. Struct. Biol. 130, 88-98 (2000).
13. Chiti, F. & Dobson, C. M. Amyloid formation by globular proteins under native conditions. Nat. Chem. Biol. 5, 15-21 (2008).
14. Nelson, R. & Eisenberg, D. Recent atomic models of amyloid fibril structure. Curr. Opin. Struct. Biol. 16, 260-265 (2006).
15. Luhrs, T. et al. 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc. Natl Acad. Sci. USA 102, 17342-17347 (2005).
16. Morris, A. M., Watzky, M. A. & Finke, R. G. Protein aggregation kinetics, mechanism, and curve-fitting: a review of the literature. Biochim. Biophys. Acta 1794, 375-397 (2009).
17. Eisenberg, D. et al. The structural biology of protein aggregation diseases: fundamental questions and some answers. Acc. Chem. Res. 39, 568-575 (2006).
18. Haass, C. & Selkoe, D. J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid b-peptide. Nat. Rev. Mol. Cell Biol. 8, 101-112 (2007).
19. Ehrnhoefer, D. E. et al. EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat. Struct. Biol. 15, 558-566 (2008).
20. Kodali, R. & Wetzel, R. Polymorphism in the intermediates and products of amyloid assembly. Curr. Opin. Struct. Biol. 17, 48-57 (2007).
21. Lambert, M. P. et al. Diffusible, nonfibrillar ligands derived from Ab1-42 are potent central nervous system neurotoxins. Proc. Natl Acad. Sci. USA 95, 6448-6453 (1998).
22. Kirkitadze, M. D., Bitan, G. & Teplow, D. B. Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies. J. Neurosci. Res. 69, 567-577 (2002).
23. Bernstein, S. L. et al. Amyloid-b protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nature Chem. 1, 326-331 (2009).
24. Kayed, R. et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 (2003).
25. Bucciantini, M. et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416, 507-511 (2002).
26. Glabe, C. G. Conformation-dependent antibodies target diseases of protein misfolding. Trends Biochem. Sci. 29, 542-547 (2004).
27. Dupuis, N. F., Wu, C., Shea, J. E. & Bowers, M. T. Human islet amyloid polypeptide monomers form ordered b-hairpins: a possible amyloidogenic conformation. J. Am. Chem. Soc. 131, 18283-18292 (2009).
28. Kayed, R. et al. Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol. Neurodegen. 2: (2007).
29. Larson, J. L., Ko, E. & Miranker, A. D. Direct measurement of islet amyloid polypeptide fibrillogenesis by mass spectrometry. Protein Sci. 9, 427-431 (2000).
30. Smith, R. D., Lightwahl, K. J., Winger, B. E. & Loo, J. A. Preservation of noncovalent associations in electrospray ionization mass-spectrometry - multiply charged polypeptide and protein dimers. Org. Mass Spectrom. 27, 811-821 (1992).
31. Lightwahl, K. J., Schwartz, B. L. & Smith, R. D. Observation of the noncovalent quaternary associations of proteins by electrospray-ionization massspectrometry. J. Am. Chem. Soc. 116, 5271-5278 (1994).
32. Smith, R. D. & Lightwahl, K. J. The observation of noncovalent interactions in solution by electrospray-ionization mass-spectrometry - promise, pitfalls and prognosis. Biol. Mass Spectrom. 22, 493-501 (1993).
33. Nettleton, E. J. et al. Characterization of the oligomeric states of insulin in selfassembly and amyloid formation by mass spectrometry. Biophys. J. 79, 1053-1065 (2000).
34. Caddy, G. L. & Robinson, C. V. Insights into amyloid fibril formation from mass spectrometry. Protein Pept. Lett. 13, 255-260 (2006).
35. Loo, J. A. Studying noncovalent protein complexes by electrospray ionization mass spectrometry. Mass Spectrom. Rev. 16, 1-23 (1997).
36. von Helden, G., Gotts, N. G. & Bowers, M. T. Experimental evidence for the formation of fullerenes by collisional heating of carbon rings in the gas phase. Nature 363, 60-63 (1993).
37. von Helden, G., Wyttenbach, T. & Bowers, M. T. Conformation of macromolecules in the gas phase: use of matrix-assisted laser desorption methods in ion chromatography. Science 267, 1483-1485 (1995).
38. Bowers, M. T., Kemper, P. R., von Helden, G. & van Koppen, P. A. M. Gas-phase ion chromatography - transition-metal state selection and carbon cluster formation. Science 260, 1446-1451 (1993).
39. Ruotolo, B. T. et al. Evidence for macromolecular protein rings in the absence of bulk water. Science 310, 1658-1661 (2005).
40. Smith, G. D. & Griffin, J. F. Conformation of [Leu5] enkephalin from X-ray diffraction: features important for recognition at opiate receptor. Science 199, 1214-1216 (1978).
41. Deschamps, J. R., George, C. & Flippen-Anderson, J. L. Structural studies of opioid peptides: a review of recent progress in X-ray diffraction studies. Biopolymers 40, 121-139 (1996).