GB1 is not a two-state folder: Identification and characterization of an on-pathway intermediate

Biophysical Journal

Volumn 101, Issue 8, 2011, Pages 2053-2060

  Morrone, Angela ^a   Giri, Rajanish ^a   Toofanny, Rudesh D ^b   Travaglini Allocatelli, Carlo ^a   Brunori, Maurizio ^a   Daggett, Valerie ^b   Gianni, Stefano ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b University of Washington   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; IGG FC BINDING PROTEIN, STREPTOCOCCUS; IGG FC-BINDING PROTEIN, STREPTOCOCCUS;

ARTICLE; CHEMISTRY; KINETICS; MOLECULAR DYNAMICS; PH; PROTEIN CONFORMATION; PROTEIN FOLDING; THERMODYNAMICS;

BACTERIAL PROTEINS; HYDROGEN-ION CONCENTRATION; KINETICS; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; PROTEIN FOLDING; THERMODYNAMICS;

EID: 80054705419     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.09.013     Document Type: Article

References (44)

1. A.R. Fersht From the first protein structures to our current knowledge of protein folding: delights and scepticisms Nat. Rev. Mol. Cell Biol. 9 2008 650 654
2. L.S. Itzhaki, D.E. Otzen, and A.R. Fersht The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering methods: evidence for a nucleation-condensation mechanism for protein folding J. Mol. Biol. 254 1995 260 288
3. A.R. Fersht Optimization of rates of protein folding: the nucleation-condensation mechanism and its implications Proc. Natl. Acad. Sci. USA 92 1995 10869 10873
4. G.W. White, and S. Gianni V. Daggett Simulation and experiment conspire to reveal cryptic intermediates and a slide from the nucleation-condensation to framework mechanism of folding J. Mol. Biol. 350 2005 757 775 (Pubitemid 40848673)
5. S. Gianni, and N.R. Guydosh A.R. Fersht Unifying features in protein-folding mechanisms Proc. Natl. Acad. Sci. USA 100 2003 13286 13291 (Pubitemid 37444734)
6. J.D. Bryngelson, and J.N. Onuchic P.G. Wolynes Funnels, pathways, and the energy landscape of protein folding: a synthesis Proteins 21 1995 167 195
7. P. Alexander, J. Orban, and P. Bryan Kinetic analysis of folding and unfolding the 56 amino acid IgG-binding domain of streptococcal protein G Biochemistry 31 1992 7243 7248
8. H.S. Chung, J.M. Louis, and W.A. Eaton Distinguishing between protein dynamics and dye photophysics in single-molecule FRET experiments Biophys. J. 98 2010 696 706
9. K. Ding, J.M. Louis, and A.M. Gronenborn Insights into conformation and dynamics of protein GB1 during folding and unfolding by NMR J. Mol. Biol. 335 2004 1299 1307 (Pubitemid 38077247)
10. M.K. Frank, G.M. Clore, and A.M. Gronenborn Structural and dynamic characterization of the urea denatured state of the immunoglobulin binding domain of streptococcal protein G by multidimensional heteronuclear NMR spectroscopy Protein Sci. 4 1995 2605 2615
11. I.A. Hubner, J. Shimada, and E.I. Shakhnovich Commitment and nucleation in the protein G transition state J. Mol. Biol. 336 2004 745 761 (Pubitemid 38183026)
12. S.A. Islam, M. Karplus, and D.L. Weaver The role of sequence and structure in protein folding kinetics; the diffusion-collision model applied to proteins L and G Structure 12 2004 1833 1845 (Pubitemid 39298967)
13. B.A. Krantz, and L. Mayne T.R. Sosnick Fast and slow intermediate accumulation and the initial barrier mechanism in protein folding J. Mol. Biol. 324 2002 359 371 (Pubitemid 35379034)
14. E.L. McCallister, E. Alm, and D. Baker Critical role of beta-hairpin formation in protein G folding Nat. Struct. Biol. 7 2000 669 673 (Pubitemid 30636679)
15. S.H. Park, K.T. O'Neil, and H. Roder An early intermediate in the folding reaction of the B1 domain of protein G contains a native-like core Biochemistry 36 1997 14277 14283 (Pubitemid 27509919)
16. S.H. Park, M.C. Shastry, and H. Roder Folding dynamics of the B1 domain of protein G explored by ultrarapid mixing Nat. Struct. Biol. 6 1999 943 947 (Pubitemid 29463308)
17. F.B. Sheinerman, and C.L. Brooks 3rd A molecular dynamics simulation study of segment B1 of protein G Proteins 29 1997 193 202 (Pubitemid 27430934)
18. T. Shen, C. Zong, J.J. Portman, and P.G. Wolynes Variationally determined free energy profiles for structural models of proteins: characteristic temperatures for folding and trapping J. Phys. Chem. B 112 2008 6074 6082
19. J. Shimada, and E.I. Shakhnovich The ensemble folding kinetics of protein G from an all-atom Monte Carlo simulation Proc. Natl. Acad. Sci. USA 99 2002 11175 11180 (Pubitemid 34920898)
20. H.S. Chung, J.M. Louis, and W.A. Eaton Experimental determination of upper bound for transition path times in protein folding from single-molecule photon-by-photon trajectories Proc. Natl. Acad. Sci. USA 106 2009 11837 11844
21. P.A. Alexander, and Y. He P.N. Bryan The design and characterization of two proteins with 88% sequence identity but different structure and function Proc. Natl. Acad. Sci. USA 104 2007 11963 11968 (Pubitemid 47185613)
22. M. Silow, and M. Oliveberg Transient aggregates in protein folding are easily mistaken for folding intermediates Proc. Natl. Acad. Sci. USA 94 1997 6084 6086 (Pubitemid 27270640)
23. M.M. Santoro, and D.W. Bolen Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants Biochemistry 27 1988 8063 8068
24. J. Kuszewski, A.M. Gronenborn, and G.M. Clore Improving the packing and accuracy of NMR structures with a pseudopotential for the radius of gyration J. Am. Chem. Soc. 121 1999 2337 2338 (Pubitemid 29152461)
25. D.A.C. Beck, D.O. Alonso, and V. Daggett in lucem Molecular Mechanics (ilmm) 2000-2011 University of Washington Seattle, WA
26. M. Levitt, and M. Hirshberg V. Daggett Potential-energy function and parameters for simulations of the molecular-dynamics of proteins and nucleic-acids in solution Comput. Phys. Commun. 91 1995 215 231
27. M. Levitt, and M. Hirshberg V. Daggett Calibration and testing of a water model for simulation of the molecular dynamics of proteins and nucleic acids in solution J. Phys. Chem. B 101 1997 5051 5061 (Pubitemid 127617309)
28. D.A.C. Beck, and V. Daggett Methods for molecular dynamics simulations of protein folding/unfolding in solution Methods 34 2004 112 120 (Pubitemid 38993212)
29. R.D. Toofanny, A.L. Jonsson, and V. Daggett A comprehensive multidimensional-embedded, one-dimensional reaction coordinate for protein unfolding/folding Biophys. J. 98 2010 2671 2681
30. B. Lee, and F.M. Richards The interpretation of protein structures: estimation of static accessibility J. Mol. Biol. 55 1971 379 400
31. S. Gianni, and Y. Ivarsson C. Travaglini-Allocatelli Identification and characterization of protein folding intermediates Biophys. Chem. 128 2007 105 113 (Pubitemid 46843445)
32. S.E. Jackson, and A.R. Fersht Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition Biochemistry 30 1991 10428 10435
33. M.J. Parker, J. Spencer, and A.R. Clarke An integrated kinetic analysis of intermediates and transition states in protein folding reactions J. Mol. Biol. 253 1995 771 786
34. G. Wildegger, and T. Kiefhaber Three-state model for lysozyme folding: triangular folding mechanism with an energetically trapped intermediate J. Mol. Biol. 270 1997 294 304 (Pubitemid 27296689)
35. A. Bachmann, and T. Kiefhaber Apparent two-state tendamistat folding is a sequential process along a defined route J. Mol. Biol. 306 2001 375 386 (Pubitemid 33032886)
36. I.E. Sánchez, and T. Kiefhaber Evidence for sequential barriers and obligatory intermediates in apparent two-state protein folding J. Mol. Biol. 325 2003 367 376 (Pubitemid 36062694)
37. J.M. Sauder, N.E. MacKenzie, and H. Roder Kinetic mechanism of folding and unfolding of Rhodobacter capsulatus cytochrome c2 Biochemistry 35 1996 16852 16862 (Pubitemid 27020531)
38. W.F. Walkenhorst, S.M. Green, and H. Roder Kinetic evidence for folding and unfolding intermediates in staphylococcal nuclease Biochemistry 36 1997 5795 5805 (Pubitemid 27214931)
39. S. Kmiecik, and A. Kolinski Folding pathway of the b1 domain of protein G explored by multiscale modeling Biophys. J. 94 2008 726 736 (Pubitemid 351162443)
40. M. Oliveberg Alternative explanations for multi-state kinetics in protein folding: transient aggregation and changing transition-state ensambles Acc. Chem. Res. 31 1998 765 772 (Pubitemid 128474543)
41. M. Oliveberg, and Y.J. Tan A.R. Fersht The changing nature of the protein folding transition state: implications for the shape of the free-energy profile for folding J. Mol. Biol. 277 1998 933 943 (Pubitemid 28195991)
42. S. Gianni, and M. Brunori M. Zhang Distinguishing between smooth and rough free energy barriers in protein folding Biochemistry 48 2009 11825 11830
43. S. Gianni, and N. Calosci C. Travaglini-Allocatelli Kinetic folding mechanism of PDZ2 from PTP-BL Protein Eng. Des. Sel. 18 2005 389 395 (Pubitemid 41187255)
44. J. Karanicolas, and C.L. Brooks 3rd The origins of asymmetry in the folding transition states of protein L and protein G Protein Sci. 11 2002 2351 2361