Conformational sampling, catalysis, and evolution of the bacterial phosphotriesterase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 51, 2009, Pages 21631-21636

  Jackson, C J ^a   Foo, J L ^b   Tokuriki, N ^c,d   Afriat, L ^c   Carr, P D ^b   Kim, H K ^b   Schenk, G ^e   Tawfik, D S ^c   Ollis, D L ^b  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Conformational fluctuation; Dynamics; Enzyme catalysis; Evolution

Indexed keywords

PHOSPHOTRIESTERASE;

ARTICLE; BINDING SITE; CATALYSIS; CONFORMATIONAL TRANSITION; ENZYME CONFORMATION; ENZYME STRUCTURE; ESCHERICHIA COLI; HYDROLYSIS; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL;

BACTERIA; BIOCATALYSIS; EVOLUTION, MOLECULAR; KINETICS; MODELS, MOLECULAR; MUTATION; PHOSPHORIC TRIESTER HYDROLASES; PROTEIN CONFORMATION;

BACTERIA (MICROORGANISMS);

EID: 76049124264     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0907548106     Document Type: Article

References (47)

1. Radzicka A, Wolfenden R (1995) A proficient enzyme. Science 267(5194):90-93.
2. Hong SB, Raushel FM (1999) Stereochemical constraints on the substrate specificity of phosphotriesterase. Biochemistry 38(4):1159-1165.
3. Warshel A (1998) Electrostatic origin of the catalytic power of enzymes and the role of preorganized active sites. J Biol Chem 273(42):27035-27038.
4. Austin RH, et al. (1975) Dynamics of ligand binding to myoglobin. Biochemistry 14(24):5355-5373.
5. Frauenfelder H, Petsko GA, Tsernoglou D (1979) Temperature-dependent X-ray diffraction as a probe of protein structural dynamics. Nature 280(5723):558-563.
6. Frauenfelder H, Sligar SG, Wolynes PG (1991) The energy landscapes and motions of proteins. Science 254(5038):1598-1603.
7. Henzler-Wildman K, Kern D (2007) Dynamic personalities of proteins. Nature 450(7172):964-972.
8. Benkovic SJ, Hammes-Schiffer S (2003) A perspective on enzyme catalysis. Science 301(5637):1196-1202.
9. Boehr DD, et al. (2006) The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313(5793):1638-1642.
10. Eisenmesser EZ, et al. (2005) Intrinsic dynamics of an enzyme underlies catalysis. Nature 438(7064):117-121.
11. Henzler-Wildman KA, et al. (2007) Intrinsic motions along an enzymatic reaction trajectory. Nature 450(7171):838-844.
12. Tomita A, et al. (2009) Visualizing breathing motion of internal cavities in concert with ligand migration in myoglobin. Proc Natl Acad Sci USA 106(8):2612-2616.
13. Olsson MH, Parson WW, Warshel A (2006) Dynamical contributions to enzyme catalysis: Critical tests of a popular hypothesis. Chem Rev 106(5):1737-1756.
14. Horne I, et al. (2002) Identification of an opd (organophosphate degradation) gene in an Agrobacterium isolate. Appl Environ Microbiol 68(7):3371-3376.
15. Mulbry WW, Karns JS (1989) Parathion hydrolase specified by the Flavobacterium opd gene: Relationship between the gene and protein. J Bacteriol 171(12):6740-6746.
16. Caldwell SR, et al. (1991) Limits of diffusion in the hydrolysis of substrates by the phosphotriesterase from Pseudomonas diminuta. Biochemistry 30(30):7438-7444.
17. Caldwell SR, et al. (1991) Transition-state structures for enzymatic and alkaline phosphotriester hydrolysis. Biochemistry 30(30):7444-7450.
18. Jackson CJ, et al. (2006) Anomalous scattering analysis of Agrobacterium radiobacter phosphotriesterase: The prominent role of iron in the heterobinuclear active site. Biochem J 397(3):501-508.
19. Cho CM, Mulchandani A, Chen W (2004) Altering the substrate specificity of organo-phosphorus hydrolase for enhanced hydrolysis of chlorpyrifos. Appl Environ Microbiol 70(8):4681-4685.
20. Roodveldt C, Tawfik DS (2005) Directed evolution of phosphotriesterase from Pseudomonas diminuta for heterologous expression in Escherichia coli results in stabilization of the metal-free state. Protein Eng Des Sel 18(1):51-58.
21. Yang H, et al. (2003) Evolution of an organophosphate-degrading enzyme: A comparison of natural and directed evolution. Protein Eng 16(2):135-145.
22. Jackson CJ, et al. (2008) In crystallo capture of a Michaelis complex and product-binding modes of a bacterial phosphotriesterase. J Mol Biol 375(5):1189-1196.
23. Grimsley JK, et al. (2005) Structural and mutational studies of organophosphorus hydrolase reveal a cryptic and functional allosteric-binding site. Arch Biochem Biophys 442(2):169-179.
24. Warshel A, Florian J (1998) Computer simulations of enzyme catalysis: Finding out what has been optimized by evolution. Proc Natl Acad Sci USA 95(11):5950-5955.
25. Benning MM, et al. (1994) Three-dimensional structure of phosphotriesterase: An enzyme capable of detoxifying organophosphate nerve agents. Biochemistry 33(50):15001-15007.
26. Jackson CJ, et al. (2005) The effects of substrate orientation on the mechanism of a phosphotriesterase. Org Biomol Chem 3(24):4343-4350.
27. Bahar I, Rader AJ (2005) Coarse-grained normal mode analysis in structural biology. Curr Opin Struct Biol 15(5):586-592.
28. Kong Y, et al. (2006) The allosteric mechanism of yeast chorismate mutase: A dynamic analysis. J Mol Biol 356(1):237-247.
29. Kondrashov DA, et al. (2007) Protein structural variation in computational models and crystallographic data. Structure 15(2):169-177.
30. Burgi HB (2000) Motion and disorder in crystal structure analysis: Measuring and distinguishing them. Annu Rev Phys Chem 51:275-296.
31. Wang X, Minasov G, Shoichet BK (2002) Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs. J Mol Biol 320(1):85-95.
32. McLoughlin SY, et al. (2005) Increased expression of a bacterial phosphotriesterase in Escherichia coli through directed evolution. Protein Expr Purif 41(2):433-440.
33. Chen-Goodspeed M, et al. (2001) Structural determinants of the substrate and stereochemical specificity of phosphotriesterase. Biochemistry 40(5):1325-1331.
34. Hong SB, Raushel FM (1996) Metal-substrate interactions facilitate the catalytic activity of the bacterial phosphotriesterase. Biochemistry 35(33):10904-10912.
35. diSioudi B, et al. (1999) Modification of near active site residues in organophosphorus hydrolase reduces metal stoichiometry and alters substrate specificity. Biochemistry 38(10):2866-2872.
36. Liu H, Warshel A (2007) The catalytic effect of dihydrofolate reductase and its mutants is determined by reorganization energies. Biochemistry 46(20):6011-6025.
37. Wolf-Watz M, et al. (2004) Linkage between dynamics and catalysis in a thermophilicmesophilic enzyme pair. Nat Struct Mol Biol 11(10):945-949.
38. Young L, Post CB (1996) Catalysis by entropic guidance from enzymes. Biochemistry 35(48):15129-15133.
39. Finkelstein IJ, Massari AM, Fayer MD (2007) Viscosity-dependent protein dynamics. Biophys J 92(10):3652-3662.
40. Neylon C, et al. (2000) Interaction of the Escherichia coli replication terminator protein (Tus) with DNA: A model derived from DNA-binding studies of mutant proteins by surface plasmon resonance. Biochemistry 39(39):11989-11999.
41. Leslie AGW (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography, No. 26.
42. Evans P (1993) Data reduction. Proceedings of CCP4 Study Weekend on Data Collection and Processing, eds Sawyer L, Isaacs N, Bailey S (SERC Daresbury Lab, Warrington, U.K.), pp 114-122.
43. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126-2132.
44. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53:240-255.
45. Potterton E, et al. (2003) A graphical user interface to the CCP4 program suite. Acta Crystallogr D Biol Crystallogr 59:1131-1137.
46. Suhre K, Sanejouand YH (2004) ElNemo: A normal mode web server for protein movement analysis and the generation of templates for molecular replacement. Nucleic Acids Res 32:W610-W614.
47. Pisliakov AV, Cao J, Kamerlin SC, Warshel A (2009) Enzyme millisecond conformational dynamics do not catalyze the chemical step. Proc Natl Acad Sci USA 106:17359-17364.