Aromatic Cross-Strand Ladders Control the Structure and Stability of β-Rich Peptide Self-Assembly Mimics

Journal of Molecular Biology

Volumn 383, Issue 1, 2008, Pages 205-213

  Biancalana, Matthew ^a   Makabe, Koki ^a   Koide, Akiko ^a   Koide, Shohei ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

fibril; protein engineering; protein nanomaterial; tyrosine; sheet

Indexed keywords

BETA RICH PROTEIN; PEPTIDE; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; CONTROLLED STUDY; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; WILD TYPE;

EID: 52049088746     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.08.031     Document Type: Article

References (32)

1. Dobson C.M. Protein folding and misfolding. Nature 426 (2003) 884-890
2. Xing Y., and Higuchi K. Amyloid fibril proteins. Mech. Ageing Dev. 123 (2002) 1625-1636
3. Scheibel T., Parthasarathy R., Sawicki G., Lin X.M., Jaeger H., and Lindquist S.L. Conducting nanowires built by controlled self-assembly of amyloid fibers and selective metal deposition. Proc. Natl Acad. Sci. USA 100 (2003) 4527-4532
4. Woolfson D.N., and Ryadnov M.G. Peptide-based fibrous biomaterials: some things old, new and borrowed. Curr. Opin. Chem. Biol. 10 (2006) 559-567
5. Nelson R., and Eisenberg D. Recent atomic models of amyloid fibril structure. Curr. Opin. Struct. Biol. 16 (2006) 260-265
6. Tycko R. Molecular structure of amyloid fibrils: insights from solid-state NMR. Q. Rev. Biophys. 39 (2006) 1-55
7. Nelson R., Sawaya M.R., Balbirnie M., Madsen A.O., Riekel C., Grothe R., and Eisenberg D. Structure of the cross-beta spine of amyloid-like fibrils. Nature 435 (2005) 773-778
8. Sawaya M.R., Sambashivan S., Nelson R., Ivanova M.I., Sievers S.A., Apostol M.I., et al. Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447 (2007) 453-457
9. Makin O.S., Atkins E., Sikorski P., Johansson J., and Serpell L.C. Molecular basis for amyloid fibril formation and stability. Proc. Natl Acad. Sci. USA 102 (2005) 315-320
10. Tsai H.H., Gunasekaran K., and Nussinov R. Sequence and structure analysis of parallel beta helices: implication for constructing amyloid structural models. Structure 14 (2006) 1059-1072
11. Betts S., Haase-Pettingell C., Cook K., and King J. Buried hydrophobic side-chains essential for the folding of the parallel beta-helix domains of the P22 tailspike. Protein Sci. 13 (2004) 2291-2303
12. Makabe K., McElheny D., Tereshko V., Hilyard A., Gawlak G., Yan S., et al. Atomic structures of peptide self-assembly mimics. Proc. Natl Acad. Sci. USA 103 (2006) 17753-17758
13. Gazit E. A possible role for pi-stacking in the self-assembly of amyloid fibrils. FASEB J. 16 (2002) 77-83
14. Gazit E. Mechanisms of amyloid fibril self-assembly and inhibition. Model short peptides as a key research tool. FEBS J. 272 (2005) 5971-5978
15. 19F NMR spectroscopy. J. Am. Chem. Soc. 128 (2006) 8098-8099
16. Tartaglia G.G., Cavalli A., Pellarin R., and Caflisch A. The role of aromaticity, exposed surface, and dipole moment in determining protein aggregation rates. Protein Sci. 13 (2004) 1939-1941
17. Wu C., Lei H., and Duan Y. The role of Phe in the formation of well-ordered oligomers of amyloidogenic hexapeptide (NFGAIL) observed in molecular dynamics simulations with explicit solvent. Biophys. J. 88 (2005) 2897-2906
18. Bemporad F., Taddei N., Stefani M., and Chiti F. Assessing the role of aromatic residues in the amyloid aggregation of human muscle acylphosphatase. Protein Sci. 15 (2006) 862-870
19. Yan S., Gawlak G., Smith J., Silver L., Koide A., and Koide S. Conformational heterogeneity of an equilibrium folding intermediate quantified and mapped by scanning mutagenesis. J. Mol. Biol. 338 (2004) 811-825
20. Pawley N.H., Koide S., and Nicholson L.K. Backbone dynamics and thermodynamics of Borrelia outer surface protein A. J. Mol. Biol. 324 (2002) 991-1002
21. Word J.M., Lovell S.C., LaBean T.H., Taylor H.C., Zalis M.E., Presley B.K., et al. Visualizing and quantifying molecular goodness-of-fit: small-probe contact dots with explicit hydrogen atoms. J. Mol. Biol. 285 (1999) 1711-1733
22. Yan S., Gawlak G., Makabe K., Tereshko V., Koide A., and Koide S. Hydrophobic surface burial is the major stability determinant of a flat, single-layer beta-sheet. J. Mol. Biol. 368 (2007) 230-243
23. Makabe K., Tereshko V., Gawlak G., Yan S., and Koide S. Atomic-resolution crystal structure of Borrelia burgdorferi outer surface protein A via surface engineering. Protein Sci. 15 (2006) 1907-1914
24. Marek P., Abedini A., Song B., Kanungo M., Johnson M.E., Gupta R., et al. Aromatic interactions are not required for amyloid fibril formation by islet amyloid polypeptide but do influence the rate of fibril formation and fibril morphology. Biochemistry 46 (2007) 3255-3261
25. Haspel N., Zanuy D., Ma B., Wolfson H., and Nussinov R. A comparative study of amyloid fibril formation by residues 15-19 of the human calcitonin hormone: a single beta-sheet model with a small hydrophobic core. J. Mol. Biol. 345 (2005) 1213-1227
26. Tsai H.H., Reches M., Tsai C.J., Gunasekaran K., Gazit E., and Nussinov R. Energy landscape of amyloidogenic peptide oligomerization by parallel-tempering molecular dynamics simulation: significant role of Asn ladder. Proc. Natl Acad. Sci. USA 102 (2005) 8174-8179
27. Ishii Y., Markus M.A., and Tycko R. Controlling residual dipolar couplings in high-resolution NMR of proteins by strain induced alignment in a gel. J. Biomol. NMR 21 (2001) 141-151
28. Chou J.J., Gaemers S., Howder B., Louis J.M., and Bax A. A simple apparatus for generating stretched polyacrylamide gels, yielding uniform alignment of proteins and detergent micelles. J. Biomol. NMR 21 (2001) 377-382
29. Weigelt J. Single scan, sensitivity- and gradient-enhanced TROSY for multidimensional NMR experiments. J. Am. Chem. Soc. 120 (1998) 10778-10779
30. Pham T.-N., and Koide S. NMR studies of Borrelia burgdorferi OspA, a 28 kDa protein containing a single-layer β-sheet. J. Biomol. NMR 11 (1998) 407-414
31. Koide S., Huang X., Link K., Koide A., Bu Z., and Engelman D.M. Design of single-layer beta-sheets without a hydrophobic core. Nature 403 (2000) 456-460
32. Collaborative-Computational-Project. The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 (1994) 760-763