Hidden alternative structures of proline isomerase essential for catalysis

Nature

Volumn 462, Issue 7273, 2009, Pages 669-673

  Fraser, James S ^a   Clarkson, Michael W ^b   Degnan, Sheena C ^a   Erion, Renske ^a   Kern, Dorothee ^b   Alber, Tom ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHILIN A; ISOMERASE; PROLINE;

CATALYSIS; CRYSTALLOGRAPHY; ELECTRON DENSITY; ENZYME ACTIVITY; MUTATION; NUCLEAR MAGNETIC RESONANCE; PHASE EQUILIBRIUM; PROTEIN; SUBSTRATE; X-RAY;

ARTICLE; CATALYSIS; CHEMICAL REACTION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ELECTRON; ENVIRONMENTAL TEMPERATURE; ENZYME ACTIVE SITE; MUTATION; NUCLEAR ENERGY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; TURNOVER TIME; X RAY CRYSTALLOGRAPHY;

CATALYSIS; CRYSTALLOGRAPHY, X-RAY; CYCLOPHILIN A; HUMANS; MODELS, MOLECULAR; MUTATION; PROTEIN STRUCTURE, TERTIARY; TEMPERATURE;

EID: 71449103005     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature08615     Document Type: Article

References (45)

1. Henzler-Wildman, K. & Kern, D. Dynamic personalities of proteins. Nature 450, 964-972 (2007).
2. Mittermaier, A. & Kay, L. E. Review-new tools provide new insights in NMR studies of protein dynamics. Science 312, 224-228 (2006).
3. Boehr, D. D., McElheny, D., Dyson, H. J. & Wright, P. E. The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313, 1638-1642 (2006).
4. Eisenmesser, E. Z. et al. Intrinsic dynamics of an enzyme underlies catalysis. Nature 438, 117-121 (2005).
5. Hammes-Schiffer, S. & Benkovic, S. J. Relating protein motion to catalysis. Annu. Rev. Biochem. 75, 519-541 (2006).
6. Schramm, V. L. & Shi, W. Atomic motion in enzymatic reaction coordinates. Curr. Opin. Struct. Biol. 11, 657-665 (2001).
7. Agarwal, P. K. Cis/trans isomerization in HIV-1 capsid protein catalyzed by cyclophilin A: insights from computational and theoretical studies. Proteins 56, 449-463 (2004).
8. Hamelberg, D. & McCammon, A. Mechanistic insight into the role of transition-state stabilization in cyclophilin A. J. Am. Chem. Soc. 131, 147-152 (2009).
9. Li, G. H. & Cui, Q. What is so special about Arg 55 in the catalysis of cyclophilin A? Insights from hybrid QM/MM simulations. J. Am. Chem. Soc. 125, 15028-15038 (2003).
10. Trzesniak, D. & Van Gunsteren, W. F. Catalytic mechanism of cyclophilin as observed in molecular dynamics simulations: pathway prediction and reconciliation of X-ray crystallographic and NMR solution data. Protein Sci. 15, 2544-2551 (2006).
11. Howard, B. R., Vajdos, F. F., Li, S., Sundquist, W. I. & Hill, C. P. Structural insights into the catalytic mechanism of cyclophilin A. Nature Struct. Biol. 10, 475-481 (2003).
12. Ke, H. M. & Huai, Q. Crystal structures of cyclophilin and its partners. Front. Biosci. 9, 2285-2296 (2004).
13. Lang, P. T. et al. Automated electron-density sampling reveals widespread conformational polymorphism in proteins. Protein Sci. (submitted).
14. Eisenmesser, E. Z., Bosco, D. A., Akke, M. & Kern, D. Enzyme dynamics during catalysis. Science 295, 1520-1523 (2002).
15. Halle, B. Biomolecular cryocrystallography: structural changes during flash-cooling. Proc. Natl Acad. Sci. USA 101, 4793-4798 (2004).
16. Rasmussen, B. F., Stock, A. M., Ringe, D. & Petsko, G. A. Crystalline ribonuclease A loses function below the dynamical transition at 220 K. Nature 357, 423-424 (1992).
17. Loria, J. P., Rance, M. & Palmer, A. G. A TROSY CPMG sequence for characterizing chemical exchange in large proteins. J. Biomol. NMR 15, 151-155 (1999).
18. Millet, O., Loria, J. P., Kroenke, C. D., Pons, M. & Palmer, A. G. The static magnetic field dependence of chemical exchange linebroadening defines the NMR chemical shift time scale. J. Am. Chem. Soc. 122, 2867-2877 (2000).
19. Kofron, J. L., Kuzmic, P., Kishore, V., Colonbonilla, E. & Rich, D. H. Determination of kinetic constants for peptidyl prolyl cis-trans isomerases by an improved spectrophotometric assay. Biochemistry 30, 6127-6134 (1991).
20. Farrow, N. A., Zhang, O. W., Forman-Kay, J. D. & Kay, L. E. A Heteronuclear correlation experiment for simultaneous determination of 15N longitudinal decay and chemical exchange rates of systems in slow equilibrium. J. Biomol. NMR 4, 727-734 (1994).
21. Zydowsky, L. D. et al. Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporine A binding and calcineurin inhibition. Protein Sci. 1, 1092-1099 (1992).
22. Frauenfelder, H. et al. Thermal expansion of a protein. Biochemistry 26, 254-261 (1987).
23. Frauenfelder, H., Petsko, G. A. & Tsernoglou, D. Temperature- dependent X-ray diffraction as a probe of protein structural dynamics. Nature 280, 558-563 (1979).
24. Tilton, R. F., Dewan, J. C. & Petsko, G. A. Effects of temperature on protein structure and dynamics: X-ray crystallographic studies of the protein ribonuclease-A at nine different temperatures from 98 to 320K. Biochemistry 31, 2469-2481 (1992).
25. Beach, H., Cole, R., Gill, M. L. & Loria, J. P. Conservation of ms-ms enzyme motions in the apo-and substrate-mimicked state. J. Am. Chem. Soc. 127, 9167-9176 (2005).
26. Tokuriki, N. & Tawfik, D. S. Protein dynamism and evolvability. Science 324, 203-207 (2009).
27. Lee, G. M. & Craik, C. S. Trapping moving targets with small molecules. Science 324, 213-215 (2009).
28. Kiefersauer, R. et al. A novel free-mounting system for protein crystals: transformation and improvement of diffraction power by accurately controlled humidity changes. J. Appl. Crystallogr. 33, 1223-1230 (2000).
29. Davis, D. G., Perlman, M. E. & London, R. E. Direct measurements of the dissociation-rate constant for inhibitor-enzyme complexes via the T1r and T2(CPMG) methods. J. Magn. Reson. Ser. B 104, 266-275 (1994).
30. Hu, J. S., Grzesiek, S. & Bax, A. Two-dimensional NMR methods for determining x1 angles of aromatic residues in proteins from three-bond JC'Cc and JNCc couplings. J. Am. Chem. Soc. 119, 1803-1804 (1997).
31. Southworth-Davies, R. J., Medina, M. A., Carmichael, I. & Garman, E. F. Observation of decreased radiation damage at higher dose rates in room temperature protein crystallography. Structure 15, 1531-1541 (2007).
32. Otwinowski, Z. & Minor, W. in Macromolecular Crystallography Part A, 307-326 (Methods in Enzymology, Vol. 276, Academic, 1997).
33. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
34. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948-1954 (2002).
35. Holton, J. & Alber, T. Automated protein crystal structure determination using ELVES. Proc. Natl Acad. Sci. USA 101, 1537-1542 (2004).
36. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800 (1993).
37. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
38. Davis, I. W. et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383 (2007).
39. Laskowski, R. A., Macarthur, M. W., Moss, D. S. & Thornton, J. M. Procheck-a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291 (1993).
40. Delano, W. L. The PyMOL Molecular Graphics System (DeLano Scientific, Palo Alto, 2008); Æhttp://www.pymol.orgæ.
41. Theobald, D. L. & Wuttke, D. S. THESEUS: maximum likelihood superpositioning and analysis of macromolecular structures. Bioinformatics 22, 2171-2172 (2006).
42. Mulder, F. A. A., Mittermaier, A., Hon, B., Dahlquist, F. W. & Kay, L. E. Studying excited states of proteins by NMR spectroscopy. Nature Struct. Biol. 8, 932-935 (2001).
43. Delaglio, F. et al. NMRPipe-a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
44. Johnson, B. A. & Blevins, R. A. NMR View-a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614 (1994).
45. Jeener, J., Meier, B. H., Bachmann, P. & Ernst, R. R. Investigation of exchange processes by 2-dimensional NMR-spectroscopy. J. Chem. Phys. 71, 4546-4553 (1979).