The mechanism of folding of Im7 reveals competition between functional and kinetic evolutionary constraints

Nature Structural and Molecular Biology

Volumn 16, Issue 3, 2009, Pages 318-324

  Friel, Claire T ^a,d   Alastair Smith, D ^a,e   Vendruscolo, Michele ^b   Gsponer, Joerg ^c   Radford, Sheena E ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^d MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^e Avacta Group Plc   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HELIX LOOP HELIX PROTEIN; PROTEIN IM7; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL IMMUNITY; COMPLEX FORMATION; ENZYME KINETICS; GENETIC CONSERVATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; SIMULATION;

CARRIER PROTEINS; ESCHERICHIA COLI PROTEINS; KINETICS; MODELS, MOLECULAR; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY;

BACTERIA (MICROORGANISMS);

EID: 62049084565     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1562     Document Type: Article

References (41)

1. Roder, H., Maki, K. & Cheng, H. Early events in protein folding explored by rapid mixing methods. Chem. Rev. 106, 1836-1861 (2006).
2. Schuler, B. & Eaton, W.A. Protein folding studied by single-molecule FRET. Curr. Opin. Struct. Biol. 18, 16-26 (2008).
3. Dill, K.A. & Chan, H.S. From Levinthal to pathways to funnels. Nat. Struct. Biol. 4, 10-19 (1997).
4. Onuchic, J.N. & Wolynes, P.G. Theory of protein folding. Curr. Opin. Struct. Biol. 14, 70-75 (2004).
5. Bryngelson, J.D. & Wolynes, P.G. Spin glasses and the statistical mechanics of protein folding. Proc. Natl. Acad. Sci. USA 84, 7524-7528 (1987).
6. Hill, R.B. et al. De novo design of helical bundles as models for understanding protein folding and function. Acc. Chem. Res. 33, 745-754 (2000).
7. Sauer, R.T. Protein folding from a combinatorial perspective. Fold. Des. 1, R27-R30 (1996).
8. Watters, A.L. et al. The highly cooperative folding of small naturally occurring proteins is likely the result of natural selection. Cell 128, 613-624 (2007).
9. Monsellier, E. & Chiti, F. Prevention of amyloid-like aggregation as a driving force of protein evolution. EMBO Rep. 8, 737-742 (2007).
10. Mitraki, A. et al. Global suppression of protein folding defects and inclusion body formation. Science 253, 54-58 (1991).
11. Jahn, T.R. & Radford, S.E. Folding versus aggregation: polypeptide conformations on competing pathways. Arch. Biochem. Biophys. 469, 100-117 (2008).
12. Brockwell, D.J. & Radford, S.E. Intermediates: ubiquitous species on folding energy landscapes? Curr. Opin. Struct. Biol. 17, 30-37 (2007).
13. Dennis, C.A. et al. A structural comparison of the colicin immunity proteins Im7 and Im9 gives new insights into the molecular determinants of immunity-protein specificity. Biochem. J. 333, 183-191 (1998).
14. Capaldi, A.P., Kleanthous, C. & Radford, S.E. Im7 folding mechanism: misfolding on a path to the native state. Nat. Struct. Biol. 9, 209-216 (2002).
15. Capaldi, A.P. et al. Ultrarapid mixing experiments reveal that Im7 folds via an on-pathway intermediate. Nat. Struct. Biol. 8, 68-72 (2001).
16. Ferguson, N. et al. Rapid folding with and without populated intermediates in the homologous four-helix proteins Im7 and Im9. J. Mol. Biol. 286, 1597-1608 (1999).
17. Gorski, S.A. et al. Equilibrium hydrogen exchange reveals extensive hydrogen bonded secondary structure in the on-pathway intermediate of Im7. J. Mol. Biol. 337, 183-193 (2004).
18. Cranz-Mileva, S., Friel, C.T. & Radford, S.E. Helix stability and hydrophobicity in the folding mechanism of the bacterial immunity protein Im9. Protein Eng. Des. Sel. 18, 41-50 (2005).
19. Friel, C.T., Beddard, G.S. & Radford, S.E. Switching two-state to three-state kinetics in the helical protein Im9 via the optimisation of stabilising non-native interactions by design. J. Mol. Biol. 342, 261-273 (2004).
20. Li, W. et al. Highly discriminating protein-protein interaction specificities in the context of a conserved binding energy hotspot. J. Mol. Biol. 337, 743-759 (2004).
21. Goh, C.S. & Cohen, F.E. Co-evolutionary analysis reveals insights into protein-protein interactions. J. Mol. Biol. 324, 177-192 (2002).
22. Gsponer, J. et al. Determination of an ensemble of structures representing the intermediate state of the bacterial immunity protein Im7. Proc. Natl. Acad. Sci. USA 103, 99-104 (2006).
23. Whittaker, S.B. et al. NMR analysis of the conformational properties of the trapped onpathway folding intermediate of the bacterial immunity protein Im7. J. Mol. Biol. 366, 1001-1015 (2007).
24. Fersht, A.R. Nucleation mechanisms in protein folding. Curr. Opin. Struct. Biol. 7, 3-9 (1997).
25. Vendruscolo, M. et al. Three key residues form a critical contact network in a protein folding transition state. Nature 409, 641-645 (2001).
26. Lindorff-Larsen, K. et al. Calculation of mutational free energy changes in transition states for protein folding. Biophys. J. 85, 1207-1214 (2003).
27. Salvatella, X. et al. Determination of the folding transition states of barnase by using PhiI-value-restrained simulations validated by double mutant PhiIJ-values. Proc. Natl. Acad. Sci. USA 102, 12389-12394 (2005).
28. Guerois, R., Nielsen, J.E. & Serrano, L. Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J. Mol. Biol. 320, 369-387 (2002).
29. Munoz, V. & Serrano, L. Development of the multiple sequence approximation within the AGADIR model of a-helix formation: comparison with Zimm-Bragg and Lifson-Roig formalisms. Biopolymers 41, 495-509 (1997).
30. Rodriguez-Mendieta, I.R. et al. Ultraviolet resonance Raman studies reveal the environment of tryptophan and tyrosine residues in the native and partially folded states of the E. colicin-binding immunity protein Im7. Biochemistry 44, 3306-3315 (2005).
31. Dobson, C.M. Protein folding and misfolding. Nature 426, 884-890 (2003).
32. Jemth, P. et al. The structure of the major transition state for folding of an FF domain from experiment and simulation. J. Mol. Biol. 350, 363-378 (2005).
33. Sutto, L. et al. Consequences of localized frustration for the folding mechanism of the Im7 protein. Proc. Natl. Acad. Sci. USA 104, 19825-19830 (2007).
34. Keeble, A.H. & Kleanthous, C. The kinetic basis for dual recognition in colicin endonuclease-immunity protein complexes. J. Mol. Biol. 352, 656-671 (2005).
35. Kuhlmann, U.C. et al. Specificity in protein-protein interactions: the structural basis for dual recognition in endonuclease colicin-immunity protein complexes. J. Mol. Biol. 301, 1163-1178 (2000).
36. Di Nardo, A.A. et al. Dramatic acceleration of protein folding by stabilization of a nonnative backbone conformation. Proc. Natl. Acad. Sci. USA 101, 7954-7959 (2004).
37. Gosavi, S. et al. Extracting function from a b-trefoil folding motif. Proc. Natl. Acad. Sci. USA 105, 10384-10389 (2008).
38. Neudecker, P. et al. Phi-value analysis of a three-state protein folding pathway by NMR relaxation dispersion spectroscopy. Proc. Natl. Acad. Sci. USA 104, 15717-15722 (2007).
39. Friel, C.T., Capaldi, A.P. & Radford, S.E. Structural analysis of the rate-limiting transition states in the folding of lm7 and lm9: Similarities and differences in the folding of homologous proteins. J. Mol. Biol. 326, 293-305 (2003).
40. Masca, S.I. et al. Detailed evaluation of the performance of microfluidic T mixers using fluorescence and ultraviolet resonance Raman spectroscopy. Rev. Sci. Instrum. 77, 055105 (2006).
41. Brooks, B.R. et al. CHARMM - a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4, 187-217 (1983).