Refolding the engrailed homeodomain: Structural basis for the accumulation of a folding intermediate

Biophysical Journal

Volumn 99, Issue 5, 2010, Pages 1628-1636

  McCully, Michelle E ^a   Beck, David A C ^b   Fersht, Alan R ^c   Daggett, Valerie ^a  

^a University of Washington   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77956567928     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.06.040     Document Type: Article

References (35)

1. Mayor, U., J. G. Grossmann., A. R. Fersht. 2003. The denatured state of engrailed homeodomain under denaturing and native conditions. J. Mol. Biol. 333:977-991.
2. Mayor, U., N. R. Guydosh., A. R. Fersht. 2003. The complete folding pathway of a protein from nanoseconds to microseconds. Nature. 421:863-867.
3. Religa, T. L., J. S. Markson., A. R. Fersht. 2005. Solution structure of a protein denatured state and folding intermediate. Nature. 437:1053-1056.
4. Mayor, U., C. M. Johnson., A. R. Fersht. 2000. Protein folding and unfolding in microseconds to nanoseconds by experiment and simulation. Proc. Natl. Acad. Sci. USA. 97:13518-13522.
5. DeMarco, M. L., D. O. V. Alonso, and V. Daggett. 2004. Diffusing and colliding: the atomic level folding/unfolding pathway of a small helical protein. J. Mol. Biol. 341:1109-1124.
6. Gianni, S., N. R. Guydosh., A. R. Fersht. 2003. Unifying features in protein-folding mechanisms. Proc. Natl. Acad. Sci. USA. 100:13286-13291.
7. Religa, T. L., C. M. Johnson., A. R. Fersht. 2007. The helix-turnhelix motif as an ultrafast independently folding domain: the pathway of folding of engrailed homeodomain. Proc. Natl. Acad. Sci. USA. 104:9272-9277.
8. Hubner, I. A., E. J. Deeds, and E. I. Shakhnovich. 2006. Understanding ensemble protein folding at atomic detail. Proc. Natl. Acad. Sci. USA. 103:17747-17752.
9. Li, D. W., H. Yang., S. Huo. 2008. Predicting the folding pathway of engrailed homeodomain with a probabilistic roadmap enhanced reaction-path algorithm. Biophys. J. 94:1622-1629.
10. Zhang, M., C. Chen., Y. Xiao. 2005. Improvement on a simplified model for protein folding simulation. Phys. Rev. E. 72:051919.
11. Englander, S. W., L. Mayne, and M. M. Krishna. 2007. Protein folding and misfolding: mechanism and principles. Q. Rev. Biophys. 40:287-326.
12. Fersht, A. R. 2002. On the simulation of protein folding by short time scale molecular dynamics and distributed computing. Proc. Natl. Acad. Sci. USA. 99:14122-14125.
13. McCully, M. E., D. A. C. Beck, and V. Daggett. 2008. Microscopic reversibility of protein folding in molecular dynamics simulations of the engrailed homeodomain. Biochemistry. 47:7079-7089.
14. Clarke, N. D., C. R. Kissinger., C. O. Pabo. 1994. Structural studies of the engrailed homeodomain. Protein Sci. 3:1779-1787.
15. Beck, D. A. C., D. O. V. Alonso, and V. Daggett. 2000-2010. In lucem molecular mechanics (ilmm). University of Washington, Seattle, WA.
16. Levitt, M., M. Hirshberg., V. Daggett. 1995. Potential energy function and parameters for simulations of the molecular-dynamics of proteins and nucleic acids in solution. Comput. Phys. Commun. 91:215-231.
17. Levitt, M., M. Hirshberg., V. Daggett. 1997. Calibration and testing of a water model for simulation of the molecular dynamics of proteins and nucleic acids in solution. J. Phys. Chem. B. 101:5051-5061.
18. Kell, G. S. 1967. Precise representation of volume properties of water at one atmosphere. J. Chem. Eng. Data. 12:66-69.
19. Beck, D. A. C., and V. Daggett. 2004. Methods for molecular dynamics simulations of protein folding/unfolding in solution. Methods. 34:112-120.
20. Beck, D. A. C., R. S. Armen, and V. Daggett. 2005. Cutoff size need not strongly influence molecular dynamics results for solvated polypeptides. Biochemistry. 44:609-616.
21. Lee, B., and F. M. Richards. 1971. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55:379-400.
22. Kabsch, W., and C. Sander. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:2577-2637.
23. Religa, T. L. 2008. Comparison of multiple crystal structures with NMR data for engrailed homeodomain. J. Biomol. NMR. 40:189-202.
24. Beck, D. A. C., and V. Daggett. 2007. A one-dimensional reaction coordinate for identification of transition states from explicit solvent P (fold)-like calculations. Biophys. J. 93:3382-3391.
25. Kazmirski, S. L., A. Li, and V. Daggett. 1999. Analysis methods for comparison of multiple molecular dynamics trajectories: applications to protein unfolding pathways and denatured ensembles. J. Mol. Biol. 290:283-304.
26. Toofanny, R. D., A. L. Jonsson, and V. Daggett. 2010. A comprehensive multidimensional-embedded, one-dimensional reaction coordinate for protein unfolding/folding. Biophys. J. 98:2671-2681.
27. Team, R. C. 2004. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
28. Li, A., and V. Daggett. 1994. Characterization of the transition state of protein unfolding by use of molecular dynamics: chymotrypsin inhibitor 2. Proc. Natl. Acad. Sci. USA. 91:10430-10434.
29. Li, A., and V. Daggett. 1996. Identification and characterization of the unfolding transition state of chymotrypsin inhibitor 2 by molecular dynamics simulations. J. Mol. Biol. 257:412-429.
30. Daggett, V., A. Li., A. R. Fersht. 1996. Structure of the transition state for folding of a protein derived from experiment and simulation. J. Mol. Biol. 257:430-440.
31. Noyes, M. B., R. G. Christensen., S. A. Wolfe. 2008. Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell. 133:1277-1289.
32. Zhu, Y., D. O. Alonso., F. Gai. 2003. Ultrafast folding of α3D: a de novo designed three-helix bundle protein. Proc. Natl. Acad. Sci. USA. 100:15486-15491.
33. Wensley, B. G., S. Batey., J. Clarke. 2010. Experimental evidence for a frustrated energy landscape in a three-helix-bundle protein family. Nature. 463:685-688.
34. Day, R., and V. Daggett. 2007. Direct observation of microscopic reversibility in single-molecule protein folding. J. Mol. Biol. 366:677-686.
35. Pettersen, E. F., T. D. Goddard., T. E. Ferrin. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.