Design of β-sheet systems for understanding the thermodynamics and kinetics of protein folding

Current Opinion in Structural Biology

Volumn 14, Issue 4, 2004, Pages 458-464

  Searle, Mark S ^a   Ciani, Barbara ^b  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DISULFIDE; DITHIOL DERIVATIVE; GLUTAMIC ACID; LYSINE; PEPTIDE; PROTEIN; TRYPTOPHAN; UBIQUITIN;

AMINO TERMINAL SEQUENCE; AQUEOUS SOLUTION; BETA SHEET; BINDING SITE; CHEMICAL INTERACTION; CIRCULAR DICHROISM; CONFORMATION; COVALENT BOND; ENTHALPY; HYDROGEN BOND; KINETICS; METAL BINDING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; SPECTROSCOPY; TEMPERATURE DEPENDENCE; THERMODYNAMICS;

KINETICS; MODELS, MOLECULAR; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS; UBIQUITIN;

EID: 4143070403     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2004.06.001     Document Type: Review

References (48)

1. S.H. Gellman Minimal model systems for β-sheet secondary structure in proteins Curr Opin Chem Biol 2 1998 717 725
2. M. Ramirez-Alvarado, T. Kortemme, F.J. Blanco, and S. Serrano β-hairpin and β-sheet formation in designed linear peptides Bioorg Med Chem 7 1999 93 103
3. M.S. Searle Peptide models of protein β-sheets: design, folding and insights into stabilising weak interactions J Chem Soc Perkin Trans I 2 2001 1011 1020
4. S. Penel, R.G. Morrison, P.D. Dobson, R.J. Mortishire-Smith, and A.J. Doig Length preferences and periodicity in β-strands. Anti-parallel edge β-sheets are more likely to finish in non-hydrogen bonded rings Protein Eng 16 2003 957 961
5. J.F. Espinosa, F.A. Syud, and S.H. Gellman Analysis of the factors that stabilise a designed two-stranded anti-parallel β-sheet Protein Sci 11 2002 1492 1505
6. G. Colombo, G.M.S. De Mori, and D. Roccatano Interplay between hydrophobic cluster and loop propensity in β-hairpin formation Protein Sci 12 2003 538 550
7. H. Lei, and P.E. Smith The role of the unfolded state in hairpin stability Biophys J 85 2003 3513 3520
8. C.D. Tatko, and M.L. Waters Selective interactions in β-hairpin peptides J Am Chem Soc 124 2002 9372 9373 One of a series of papers describing quantitative studies of weak interactions. β-Hairpin model systems were used to dissect hydrophobic and specific electrostatic interactions between aromatic sidechains, using cyclohexylalanine as a non-aromatic substitute for phenylalanine.
9. C.D. Tatko, and M.L. Waters Comparison of C-H - π and hydrophobic interactions in a β-hairpin peptide: impact on stability and specificity J Am Chem 126 2004 2028 2034 A detailed analysis of the thermodynamics of the electrostatic interaction between phenylalanine or tryptophan and the polarised Cε of lysine to establish the origin of the stabilizing interaction.
10. C.D. Tatko, and M.L. Waters The geometry and efficacy of cation-π interactions in a diagonal position of a designed β-hairpin Protein Sci 12 2003 2443 2452
11. S.J. Russell, T. Blandl, N.J. Skelton, and A.G. Cochran Stability of cyclic β-hairpins: Asymmetric contributions from side chains of a hydrogen bonded cross-strand residue pair J Am Chem Soc 125 2003 388 395 This novel approach uses the equilibrium between dithiol and disulfide as a quantitative probe of stability to investigate context-dependent effects in β-hairpin folding.
12. T. Blandl, A.G. Cochran, and N.J. Skelton Turn stability in β-hairpin peptides: investigation of peptides containing 3:5 type I G1 bulge turns Protein Sci 12 2003 237 247
13. A.C. Gibbs, T.C. Bjorndahl, R.S. Hodges, and D.S. Wishart Probing the determinants of type II' β-turn formation in peptides and proteins J Am Chem Soc 124 2002 1203 1209
14. 1H NMR chemical shifts J Am Chem Soc 124 2002 14903 14909
15. M.T. Pastor, M. Lopez de la Paz, E. Lacroix, L. Serrano, and E. Perez-Paya Combinatorial approaches: a new tool to search for highly structured β-hairpin peptides Proc Natl Acad Sci USA 99 2002 614 619
16. N.J. Skelton, S. Russell, F. de Sauvage, and A.G. Cochran Amino acid determinants of β-hairpin conformation in erythropoeitin receptor agonist peptides derived from a phage display library J Mol Biol 316 2002 1111 1125
17. B. Ciani, M. Jourdan, and M.S. Searle Stabilisation of β-hairpin peptides by salt bridges: role of pre-organisation in the energetic contribution of weak interactions J Am Chem Soc 125 2003 9038 9047 The authors estimate the energetic contribution of Glu-Lys salt bridges to hairpin stability. They also demonstrate cooperative interactions that show that the energetics are dependent on intrinsic hairpin stability and hence the degree of pre-organization of the hairpin template.
18. ••], showing that the β4 hairpin, when inserted as an extension of the N-terminal hairpin sequence of ubiquitin, produces a quantifiable increase in stability and limiting chemical shift data for estimating the stability of autonomously folding hairpin peptides.
19. J. Tsai, and M. Levitt Evidence of turn and salt bridge contributions to β-hairpin stability: MD simulations of C-terminal fragment from the B1 domain of protein G Biophys Chem 101-102 2002 187 201 Multiple parallel molecular dynamics simulations of the protein G β-hairpin support turn nucleation and hydrophobic collapse, with salt bridges stabilizing the folded state by inhibiting unfolding rather than driving strand association.
20. S.E. Kiehna, and M.L. Waters Sequence dependence of β-hairpin structure: comparison of a salt bridge and an aromatic interaction Protein Sci 12 2003 2657 2667 The authors determine the relative contribution of a Phe-Phe aromatic interaction versus a Glu-Lys salt bridge to β-hairpin stability and the thermodynamics of the interactions.
21. N. Carulla, C. Woodward, and G. Barany Betacore, a designed water soluble four-stranded anti-parallel β-sheet protein Protein Sci 11 2002 1539 1551
22. J. Venkatraman, G.A.N. Gowda, and P. Balaram Design and construction of an open multi-stranded β-sheet polypeptide stabilised by a disulfide bridge J Am Chem Soc 124 2002 4987 4994
23. F.A. Syud, H.E. Stanger, H. Schenk Mortell, J.F. Espinosa, J.D. Fisk, C.G. Fry, and S.H. Gellman Influence of strand number on anti-parallel β-sheet stability in designed three and four-stranded β-sheets J Mol Biol 326 2003 553 568 A detailed analysis of how the stability of antiparallel β-sheets changes as the number of β-strands increases, using designed two-, three- and four-stranded models with cyclic hairpins and disulfide cross-links to define the fully folded reference states.
24. J.W. Neidigh, R.M. Fesinmeyer, and N. Anderson Designing a 20-residue protein Nat Struct Biol 9 2002 425 430 The Trp cage is a novel motif of 20 residues that forms a compact globular structure stabilized by a tryptophan sidechain sheathed in proline rings. This motif represents a paradigm for protein folding studies.
25. S. Deechongkit, and J.W. Kelly The effect of backbone cyclisation on the thermodynamics of β-sheet unfolding: stability optimisation of the PIN WW domain J Am Chem Soc 124 2002 4980 4986
26. H.-X. Zhou Effect of backbone cyclisation on protein folding stability: chain entropies of both the unfolded and folded states are restricted J Mol Biol 332 2003 257 264
27. J. Hilario, J. Kubelka, and T.A. Keiderling Optical spectroscopic investigations of model β-sheet hairpins in aqueous solution J Am Chem Soc 125 2003 7562 7574
28. S.V. Kuznetsov, J. Hilario, T.A. Keiderling, and A. Ansari Spectroscopic studies of structural changes in two β-sheet forming peptides show an ensemble of structures that unfold non-cooperatively Biochemistry 42 2003 4321 4332 Detailed analysis of the folding of two model three-stranded antiparallel β-sheet peptides using multiple spectroscopic probes reveals very broad unfolding transitions, suggesting an ensemble of conformations and non-cooperative folding.
29. A.G. Cochran, N.J. Skelton, and M.A. Starovasnik Tryptophan zippers: stable monomeric β-hairpins Proc Natl Acad Sci USA 98 2001 5578 5583
30. W.Y. Yang, J.W. Pitera, W.C. Swope, and M. Gruebele Heterogeneous folding of the trpzip hairpin: full atom simulation and experiment J Mol Biol 336 2004 241 251 Further analysis of the energy landscape of the trpzip β-hairpin, using spectroscopic analysis and simulation, reveals multiple melting transitions correlated with local minima corresponding to non-native associations between pairs of tryptophan residues.
31. V. Munoz, P.A. Thompson, J. Hofrichter, and W.A. Eaton Folding dynamics and mechanism of β-hairpin formation Nature 390 1997 196 199
32. Y. Xu, R. Oyola, and F. Gai Infrared study of the stability and folding kinetics of a 15-residue β-hairpin J Am Chem Soc 125 2003 15388 15394 T-jump time-resolved IR reveals much faster β-hairpin folding kinetics than previously reported [31], which appears to correlate with a very loosely packed structure. By contrast, trpzip4 is a slow folder with well-defined sidechain interactions and a compact structure.
33. D.K. Klimov, and D. Thirumalai Stiffness of the distal loop restricts the structural heterogeneity of the transition state ensemble in SH3 domains J Mol Biol 317 2002 721 737
34. A. Cavalli, P. Ferrara, and A. Caflisch Weak temperature dependence of the free energy surface and folding pathway of structured peptides Proteins 47 2002 305 314
35. B. Ma, and R. Nussinov Energy landscape and dynamics of the β-hairpin G peptide and its isomers: topology and sequences Protein Sci 12 2003 1882 1893
36. X. Wu, S. Wang, and B.R. Brooks Direct observation of the folding and unfolding of a β-hairpin in explicit water through computer simulation J Am Chem Soc 124 2002 5282 5283
37. C.D. Snow, L. Qiu, D. Du, F. Gai, S.J. Hagen, and V.S. Pande Trp zipper folding kinetics by molecular dynamics and temperature-jump spectroscopy Proc Natl Acad Sci USA 101 2004 4077 4082 The authors used T-jump fluorescence and IR spectroscopy, coupled with atomistic molecular dynamics simulations, to generate large simulated folding ensembles of trpzip β-hairpins.
38. S.J. Maness, S. Franzen, A.C. Gibbs, T.P. Causgrove, and R.B. Dyer Nanosecond temperature jump relaxation dynamics of cyclic β-hairpin peptides Biophys J 84 2003 3874 3882
39. A.-R. Viguera, and L. Serrano Bergerac-SH3: "frustration" induced by stabilising the folding nucleus J Mol Biol 311 2001 357 371
40. A.-R. Viguera, and L. Serrano Hydrogen-exchange stability analysis of Bergerac-Src homology 3 variants allows the characterisation of a folding intermediate in equilibrium Proc Natl Acad Sci USA 100 2003 5730 5735 Detailed amide hydrogen/deuterium exchange studies of the Bergerac SH3 domain with a β-hairpin extension confirm that the observed shift from a two-state to a three-state folding mechanism arises from the consolidation of a pre-folded long β-hairpin intermediate state.
41. G.W. Platt, S.A. Simpson, R. Layfield, and M.S. Searle Stability and folding kinetics of a ubiquitin mutant with a strong propensity for non-native β-hairpin conformation in the unfolded state Biochemistry 42 2003 13762 13771 Mutations in the β-turn sequence of ubiquitin show that a non-native strand alignment is stabilized in model hairpin peptides. However, in the context of the native protein, the native strand alignment is enforced with significant effects on protein stability and a reduction in the rate of folding, suggesting intimate involvement of the β-hairpin in nucleating folding.
42. B.A. Krantz, R.S. Dothager, and T.R. Sosnick Discerning the structure and energy of multiple transition states in protein folding using ψ-analysis J Mol Biol 337 2004 463 475 A novel approach to probing protein folding pathways by stabilizing elements of secondary structure using engineered metal-binding sites (zinc/bis-histidine). The study reveals possible multiple folding pathways for ubiquitin based around the β-sheet core.
43. K.S. Rotondi, and L.M. Gierasch Local sequence information in cellular retinoic acid binding protein I: specific residue roles in β-turns Biopolymers 71 2003 638 651
44. J. Kim, S.R. Brych, J. Lee, T.M. Logan, and M. Blaber Identification of a key structural element for protein folding within β-hairpin turns J Mol Biol 328 2003 951 961
45. J. Karanicolas, and C.L. Brooks The structural basis for biphasic kinetics in the folding of the WW domain from a formin-binding protein: lessons for protein design? Proc Natl Acad Sci USA 100 2003 3954 3959
46. K.S. Rotondia, L.F. Rotondib, and L.M. Gierasch Native structural propensity in cellular retinoic acid-binding protein I 64-88: the role of locally encoded structure in the folding of a β-barrel protein Biophys Chem 100 2003 421 436
47. W.F. Walkenhurst, J.A. Edwards, J.L. Markly, and H. Roder Early formation of a β-hairpin during folding of staphylococcal nuclease H124L as detected by pulsed hydrogen exchange Protein Sci 11 2002 82 91
48. R. Koradi, M. Billeter, and K Wuthrich MOLMOL: a program for display and analysis of macromolecular structures J Mol Graph 14 1996 51 55