Optimal salt bridge for Trp-cage stabilization

Biochemistry

Volumn 50, Issue 7, 2011, Pages 1143-1152

  Williams, D Victoria ^a   Byrne, Aimee ^a   Stewart, James ^a   Andersen, Niels H ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTATES; C-TERMINUS; CIRCULAR DICHROISM; COMPUTATIONAL DESIGN; COOPERATIVITY; EXPERIMENTAL STUDIES; HELICITIES; HELIX STABILITY; HIGHER TEMPERATURES; MELTING TEMPERATURES; MODEL SYSTEM; SALT BRIDGES; SIDE CHAINS;

DICHROISM; MAGNETIC RESONANCE; MELTING; STABILIZATION;

OPTIMIZATION;

AMINO ACID DERIVATIVE; ASPARTIC ACID; ASPARTYLALANYLTYROSYLALANYLGLUTAMINYLTRYPTOPHANYLLEUCYLLYSYLASPARTYLGLYCYLGLYCYLPROLYLSERYLSERYLGLYCYLARGINYLPROLYLPROLYLPROLYLSERINE; GLOBULAR PROTEIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ACIDIFICATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; MUTATION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; SALTS; TEMPERATURE; THERMODYNAMICS; TRYPTOPHAN;

EID: 79951621811     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101555y     Document Type: Article

References (64)

1. Ramírez-Alvarado, M., Blanco, F. J., and Serrano, L. (2001) Elongation of the BH8 β-hairpin peptide: Electrostatic interactions in β-hairpin formation and stability Protein Sci. 10, 1381-1392
2. Fesinmeyer, R. M., Hudson, F. M., and Andersen, N. H. (2004) Enhanced Hairpin Stability through Loop Design: The Case of the Protein G B1 Hairpin J. Am. Chem. Soc. 126, 7238-7243
3. Huyghues-Despointes, B. M., Qu, X., Tsai, J., and Scholtz, J. M. (2006) Terminal Ion Pairs Stabilize the Second β-Hairpin of the B1 Domain of Protein G Proteins: Struct., Funct., Bioinf. 63, 1005-1017
4. Rose, G. D. and Wolfenden, R. (1993) Hydrogen Bonding, Hydrophobicity, Packing, and Protein Folding Annu. Rev. Biophys. Biomol. Struct. 22, 381-415
5. Fersht, A. R., Shi, J.-P., Knill-Jones, J., Lowe, D. M., Wilkinson, A. J., Blow, D. M., Brick, P., Carter, P., Waye, M. M. Y., and Winter, G. (1985) Hydrogen bonding and biological specificity analysed by protein engineering Nature 314, 235-238
6. Fersht, A. R. (1987) The hydrogen bond in molecular recognition Trends Biochem. Sci. 12, 301-304
7. Anderson, D. E., Becktel, W. J., and Dahlquist, F. W. (1990) pH-induced denaturation of proteins: A single salt bridge contributes 3-5 kcal/mol to the free energy of folding of T4 lysozyme Biochemistry 29, 2403-2408
8. Tissot, A. C., Vuilleumier, S., and Fersht, A. R. (1996) Importance of Two Buried Salt Bridges in the Stability and Folding Pathway of Barnase Biochemistry 35, 6786-6794
9. Waldburger, C. D., Schildbach, J. F., and Sauer, R. T. (1995) Are buried salt bridges important for protein stability and conformational specificity? Nat. Struct. Mol. Biol. 2, 122-128
10. Bang, D., Tereshko, V., Kossiakoff, A. A., and Kent, S. B. H. (2009) Role of a salt bridge in the model protein crambin explored by chemical protein synthesis: X-ray structure of a unique protein analogue, [V15A]crambin-α- carboxamide Mol. BioSyst. 5, 750-756
11. Dey, M., Cao, C., Sicheri, F., and Dever, T. E. (2007) Conserved Intermolecular Salt Bridge Required for Activation of Protein Kinases PKR, GCN2, and PERK J. Biol. Chem. 282, 6653-6660
12. Dong, F. and Zhou, H.-X. (2002) Electrostatic Contributions to T4 Lysozyme Stability: Solvent-Exposed Charges versus Semi-Buried Salt Bridges Biophys. J. 83, 1341-1347
13. Horovitz, A., Serrano, L., Avron, B., Bycroft, M., and Fersht, A. R. (1990) Strength and co-operativity of contributions of surface salt bridges to protein stability J. Mol. Biol. 216, 1031-1044
14. Sali, D., Bycroft, M., and Fersht, A. R. (1991) Surface electrostatic interactions contribute little to stability of barnase J. Mol. Biol. 220, 779-788
15. Makhatadze, G. I., Loladze, V. V., Ermolenko, D. N., Chen, X., and Thomas, S. T. (2003) Contribution of Surface Salt Bridges to Protein Stability: Guidelines for Protein Engineering J. Mol. Biol. 327, 1135-1148
16. Loladze, V. V., Ibarra-Molero, B., Sanxhez-Ruiz, J. M., and Makhatadze, G. I. (1999) Engineering a Thermostable Protein via Optimization of Charge-Charge Interactions on the Protein Surface Biochemistry 38, 16419-16423
17. Horng, J.-C., Moroz, V., Rigotti, D. J., Fairman, R., and Raleigh, D. P. (2002) Characterization of Large Peptide Fragments Derived from the N-Terminal Domain of the Ribosomal Protein L9: Definition of the Minimum Folding Motif and Characterization of Local Electrostatic Interactions Biochemistry 41, 13360-13369
18. Cho, J.-H. and Raleigh, D. P. (2005) Mutational analysis demonstrates that specific electrostatic interactions can play a key role in the denatured state ensemble of proteins J. Mol. Biol. 353, 174-185
19. Neidigh, J. W., Fesinmeyer, R. M., and Andersen, N. H. (2002) Designing a 20-residue protein Nat. Struct. Biol. 9, 425-430
20. 6 Insertion Dramatically Increases Helicity J. Am. Chem. Soc. 126, 13679-13684
21. Barua, B., Lin, J. C., Williams, D. V., Neidigh, J. W., Kummler, P., and Andersen, N. H. (2008) The Trp-cage: Optimizing the Stability of a Globular Miniprotein Protein Eng., Des. Sel. 21, 171-185
22. Simmerling, C. L., Strockbine, B., and Roitberg, A. E. (2002) All-atom structure prediction and folding simulation of a stable protein J. Am. Chem. Soc. 124, 11258-11259
23. Snow, C. D., Zagrovic, B., and Pande, V. S. (2002) The Trp Cage: Folding Kinetics and Unfolded State Topology via Molecular Dynamics Simulations J. Am. Chem. Soc. 124, 14548-14549
24. Chowdhury, S., Lee, M. C., Xiong, G., and Duan, Y. (2003) Ab initio Folding Simulation of the Trp-cage Mini-protein Approaches NMR Resolution J. Mol. Biol. 327, 711-717
25. Pitera, J. W. and Swope, W. (2003) Understanding folding and design: Replica-exchange simulation of "Trp-cage" miniproteins Proc. Natl. Acad. Sci. U.S.A. 100, 7587-7592
26. Schug, A., Herges, T., and Wenzel, W. (2003) Reproducible Protein Folding with the Stochastic Tunneling Method Phys. Rev. Lett. 91, 158102/1-158102/4
27. Zhou, R. (2003) Trp-cage: Folding free energy landscape in explicit water Proc. Natl. Acad. Sci. U.S.A. 100, 13280-13285 (Pubitemid 37444733)
28. Carnevali, P., Toth, G., Toubassi, G., and Siavash, N. (2003) Fast Protein Structure Prediction using Monte Carlo Simulations with Modal Moves J. Am. Chem. Soc. 125, 14244-14245
29. Ota, M., Ikeguchi, M., and Kidera, A. (2004) Phylogeny of protein-folding trajectories reveals a unique pathway to native structure Proc. Natl. Acad. Sci. U.S.A. 101, 17658-17663
30. Schug, A., Wenzel, W., and Hansmann, U. H. E. (2005) Energy landscape paving simulations of the trp-cage protein J. Chem. Phys. 122, 194711/1-194711/7
31. Ding, F., Buldyrev, S. V., and Dokholyan, N. V. (2005) Folding Trp-cage to NMR resolution native structure using a coarse-grained protein model Biophys. J. 88, 147-155
32. Linhananta, A., Boer, J., and MacKay, I. (2005) The equilibrium properties and folding kinetics of an all-atom Go model J. Chem. Phys. 122, 114901-114915
33. Chen, J., Im, W., and Brooks, C. L., III (2006) Balancing Solvation and Intramolecular Interactions: Toward a Consistent Generalized Born Force Field J. Am. Chem. Soc. 128, 3728-3736
34. Ulmschneider, J. P., Ulmschneider, M. B., and Di Nola, A. (2006) Monte Carlo vs Molecular Dynamics for All-Atom Polypeptide Folding Simulation J. Phys. Chem. B 110, 16733-16742
35. Juraszek, J. and Bolhuis, P. G. (2006) Sampling the multiple folding mechanisms of Trp-cage in explicit solvent Proc. Natl. Acad. Sci. U.S.A. 103, 15859-15864
36. Kentsis, A., Gindin, T., Mezei, M., and Osman, R. (2007) Calculation of the free energy and cooperativity of protein folding PLoS One 2, e446
37. Beck, D. A. C., White, G. W. N., and Daggett, V. (2007) Exploring the energy landscape of protein folding using replica-exchange and conventional molecular dynamics simulations J. Struct. Biol. 157, 514-523
38. Bendová-Biedermannová, L., Hobza, P., and Vondrášek, J. (2008) Identifying stabilizing key residues in proteins using interresidue interaction energy matrix Proteins: Struct., Funct., Bioinf. 72, 402-413
39. Hu, Z., Tang, Y., Wang, H., Zhang, X., and Lei, M. (2008) Dynamics and cooperativity of Trp-cage folding Arch. Biochem. Biophys. 475, 140-147
40. Searle, M. S. and Ciani, B. (2004) Design of β-sheet systems for understanding the thermodynamics of kinetics of protein folding Curr. Opin. Struct. Biol. 14, 1-7
41. Mok, K. H., Kuhn, L. T., Goez, M., Day, I. J., Lin, J. C., Andersen, N. H., and Hore, P. J. (2007) A pre-existing hydrophobic collapse in the unfolded state of an ultrafast folding protein Nature 447, 106-109
42. Naduthambi, D. and Zondlo, N. J. (2006) Stereoelectronic Tuning of the Structure and Stability of the Trp Cage Miniprotein J. Am. Chem. Soc. 128, 12430-12431
43. Juraszek, J. and Bolhuis, P. G. (2008) Rate Constant and Reaction Coordinate of Trp-Cage Folding in Explicit Water Biophys. J. 95, 4246-4257
44. Xu, W. and Mu, Y. (2008) Ab initio folding simulation of Trp cage by replica exchange with hybrid Hamiltonian Biophys. Chem. 137, 116-125
45. Cerný, J., Vondrásek, J., and Hobza, P. (2009) Loss of Dispersion Energy Changes the Stability and Folding/Unfolding Equilibrium of the Trp-Cage Protein J. Phys. Chem. B 113, 5657-5660
46. Marinelli, F., Pietrucci, F., Laio, A., and Piana, S. (2009) A Kinetic Model of Trp-Cage Folding from Multiple Biased Molecular Dynamics Simulations PLoS Comput. Biol. 5, e1000452
47. 2-Cage J. Phys. Chem. B 110, 3759-3763
48. Chatterjee, C. and Gerig, J. T. (2006) Interactions of Hexafluoro-2-propanol with the Trp-Cage Peptide Biochemistry 45, 14665-14674
49. Chatterjee, C. and Gerig, J. T. (2007) Interactions of trifluroethanol with the Trp-cage peptide Biopolymers 87, 115-123
50. Neuman, R. C. and Gerig, J. T. (2008) Solvent interactions with the Trp-cage peptide in 35% ethanol-water Biopolymers 89, 862-872
51. Wafer, L. N. R., Streicher, W. W., and Makhatadze, G. I. (2010) Thermodynamics of the Trp-cage miniprotein unfolding in urea Proteins: Struct., Funct., Bioinf. 78, 1376-1381
52. Andersen, N. H., Barua, B., Fesinmeyer, R. M., Hudson, F. M., Lin, J., Euser, A., and White, G. (2002) in Peptides 2002: Proceedings of the 27th European Peptide Symposium, pp 824 - 825, Edizioni Ziino, Napoli, Italy.
53. Williams, D. V., Barua, B., and Andersen, N. H. (2008) A Hyperstable Miniprotein: Additive Effects of d-and l -Ala Substitutions Org. Biomol. Chem. 6, 4287-4289
54. Streicher, W. W. and Makhatadze, G. I. (2007) Unfolding Thermodynamics of Trp-Cage, a 20 Residue Miniprotein, Studied by Differential Scanning Calorimetry and Circular Dichroism Spectroscopy Biochemistry 46, 2876-2880
55. Day, R., Paschek, D., and Garcia, A. E. (2010) Microsecond simulations of the folding/unfolding thermodynamics of the Trp-cage miniprotein Proteins: Struct., Funct., Bioinf. 78, 1889-1899
56. Hudaky, P., Straner, P., Farkas, V., Varadi, G., Toth, G., and Perczel, A. (2008) Cooperation between a Salt Bridge and the Hydrophobic Core Triggers Fold Stabilization in a Trp-Cage Miniprotein Biochemistry 47, 1007-1016
57. Barua, B. (2005) Design and Study of Trp-cage Miniproteins. Ph.D. Thesis, University of Washington, Seattle.
58. 13C Carbonyl labeled Residues to Develop and Refine Site-Specific NMR Secondary Structure Analysis Techniques. Ph.D. Thesis, University of Washington, Seattle.
59. Andersen, N. H. and Tong, H. (1997) Empirical parameterization of a model for predicting peptide helix/coil equilibrium populations Protein Sci. 6, 1920-1936
60. Song, K., Stewart, J. M., Fesinmeyer, R. M., Andersen, N. H., and Simmerling, C. (2008) Structural insights for designed alanine-rich helices: Comparing NMR helicity measures and conformational ensembles from molecular dynamics simulation Biopolymers 89, 747-760
61. Stewart, J. M., Lin, J. C., and Andersen, N. H. (2008) Lysine and arginine residues do not increase the helicity of alanine-rich helices Chem. Commun., 4765-4767
62. Fesinmeyer, R. M. (2005) Chemical Shifts Define the Structure and Folding Thermodynamics of Polypeptides. Ph.D. Thesis, University of Washington, Seattle.
63. Doig, A. J. and Baldwin, R. L. (1995) N- and C-capping preferences for all 20 amino acids in α-helical peptides Protein Sci. 4, 1325-1336
64. Huyghues-Despointes, B. M., Scholtz, J. M., and Baldwin, R. L. (1993) Effect of a single aspartate on helix stability at different positions in a neutral alanine-based peptide Protein Sci. 2, 1604-1611