Insights into the catalytic mechanism of cofactor-independent phosphoglycerate mutase from X-ray crystallography, simulated dynamics and molecular modeling

Journal of Molecular Biology

Volumn 328, Issue 4, 2003, Pages 909-920

  Rigden, Daniel J ^a   Lamani, Ejvis ^b   Mello, Luciane V ^a   Littlejohn, James E ^b   Jedrzejas, Mark J ^b  

^a National Centre of Genetic Resources and Biotechnology   (Brazil)

^b CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

Bacillus stearothermophilus; Catalysis; Catalytic mechanism; Glycolysis; Gram positive bacteria

Indexed keywords

2,3 DIPHOSPHOGLYCERIC ACID; ENZYME; GLYCERIC ACID; MANGANESE; MUTANT PROTEIN; PHOSPHOENZYME; PHOSPHOGLYCERATE MUTASE; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; WATER;

ARTICLE; BACTERIUM; CATALYSIS; CLINICAL STUDY; COENZYME; CRYSTAL STRUCTURE; ENZYME ANALYSIS; ENZYME SUBSTRATE; GEOBACILLUS STEAROTHERMOPHILUS; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOLECULE; NONHUMAN; ORIENTATION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; X RAY CRYSTALLOGRAPHY;

GEOBACILLUS STEAROTHERMOPHILUS; POSIBACTERIA;

EID: 0242418195     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00350-4     Document Type: Article

References (56)

1. Jedrzejas M.J. Structure, function, and evolution of phosphoglycerate mutases: comparison with fructose-2,6-bisphosphatase, acid phosphatase, and alkaline phosphatase. Prog. Biophys. Mol. Biol. 73:2000;263-287.
2. Fothergill-Gilmore L.A., Watson H.C. The phosphoglycerate mutases. Advan. Enzymol. Relat. Areas Mol. Biol. 62:1989;227-313.
3. 2+ and is pH sensitive. Can. J. Microbiol. 44:1998;759-767.
4. Chander M., Setlow P., Lamani E., Jedrzejas M.J. Structural studies on a 2,3-diphosphoglycerate independent phosphoglycerate mutase from Bacillus stearothermophilus. J. Struct. Biol. 126:1999;156-165.
5. Jedrzejas M.J., Chander M., Setlow P., Krishnasamy G. Mechanism of catalysis of the cofactor-independent phosphoglycerate mutase from Bacillus stearothermophilus. Crystal structure of the complex with 2-phosphoglycerate. J. Biol. Chem. 275:2000;23146-23153.
6. Jedrzejas M.J., Chander M., Setlow P., Krishnasamy G. Structure and mechanism of action of a novel phosphoglycerate mutase from Bacillus stearothermophilus. EMBO J. 19:2000;1419-1431.
7. Kim E.E., Wyckoff H.W. Reaction mechanism of alkaline phosphatase based on crystal structures. Two-metal ion catalysis. J. Mol. Biol. 218:1991;449-464.
8. Bond C.S., Clements P.R., Ashby S.J., Collyer C.A., Harrop S.J., Hopwood J.J., Guss J.M. Structure of a human lysosomal sulfatase. Structure. 5:1997;277-289.
9. Lukatela G., Krauss N., Theis K., Selmer T., Gieselmann V., von Figura K., Saenger W. Crystal structure of human arylsulfatase A: the aldehyde function and the metal ion at the active site suggest a novel mechanism for sulfate ester hydrolysis. Biochemistry. 37:1998;3654-3664.
10. Galperin M.Y., Jedrzejas M.J. Conserved core structure and active site residues in alkaline phosphatase superfamily enzymes. Proteins: Struct. Funct. Genet. 45:2001;318-324.
11. 18O-labeled substrate, investigations of the phosphatase and phosphoryl transfer activities, and evidence for a phosphoryl-enzyme intermediate. Biochemistry. 16:1977;3054-3060.
12. Gatehouse J.A., Knowles J.R. Phosphoglycerate mutase from wheat germ: studies with isotopically labeled 3-phospho-D-glycerates showing that the catalyzed reaction is intramolecular. Biochemistry. 16:1977;3045-3053.
13. Britton H.G., Carrerras J., Grisolia S. Mechanism of action of 2,3-diphosphoglycerate-independent phosphoglycerate mutase. Biochemistry. 10:1971;4522-4533.
14. Blättler A.W., Knowles J.R. Phosphoglycerate mutases: stereochemical course of the phosphoryl group transfers catalyzed by the cofactor-dependent enzyme from rabbit muscle and the cofactor-independent enzyme from wheat germ. Biochemistry. 19:1980;738-743.
15. Jedrzejas M.J., Setlow P. Comparison of the binuclear metalloenzymes diphosphoglycerate-independent phosphoglycerate mutase and alkaline phosphatase: their mechanism of catalysis via a phosphoserine intermediate. Chem. Rev. 101:2001;607-618.
16. Jedrzejas M.J. Three-dimensional structure and molecular mechanism of novel enzymes of spore-forming bacteria. Med. Sci. Monit. 8:2002;RA183-RA190.
17. Jedrzejas M.J. The structure and function of novel enzymes of Bacillus anthracis and other spore-forming bacteria: development of novel prophylactic and therapeutic agents. Crit. Rev. Biochem. Mol. Biol. 37:2002;339-373.
18. Collet J.F., Stroobant V., Van Schaftingen E. The 2,3-bisphosphoglycerate-independent phosphoglycerate mutase from Trypanosoma brucei: metal-ion dependency and phosphoenzyme formation. FEMS Microbiol. Letters. 204:2001;39-44.
19. Holtz K.M., Kantrowitz E.R. The mechanism of the alkaline phosphatase reaction: insights from NMR, crystallography and site-specific mutagenesis. FEBS Letters. 462:1999;7-11.
20. Galperin M.Y., Bairoch A., Koonin E.V. A superfamily of metalloenzymes unifies phosphopentomutase and cofactor-independent phosphoglycerate mutase with alkaline phosphatases and sulfatases. Protein Sci. 7:1998;1829-1835.
21. Rong S.B., Hu Y., Enyedy I., Powis G., Meuillet E.J., Wu X., et al. Molecular modeling studies of the Akt PH domain and its interaction with phosphoinositides. J. Med. Chem. 44:2001;898-908.
22. Likic V.A., Juranic N., Macura S., Prendergast F.G. A structural water molecule in the family of fatty acid binding proteins. Protein Sci. 9:2000;497-504.
23. Lee Y.H., Olson T.W., Ogata C.M., Levitt D.G., Banaszak L.J., Lange A.J. Crystal structure of a trapped phosphoenzyme during a catalytic reaction. Nature Struct. Biol. 4:1997;615-618.
24. Stec B., Hehir M.J., Brennan C., Nolte M., Kantrowitz E.R. Kinetic and X-ray structural studies of three mutant E. coli alkaline phosphatases: insights into the catalytic mechanism without the nucleophile Ser102. J. Mol. Biol. 277:1998;647-662.
25. Mizuguchi H., Cook P.F., Tai C.H., Hasemann C.A., Uyeda K. Reaction mechanism of fructose-2,6-bisphosphatase. A mutation of nucleophilic catalyst, histidine 256, induces an alteration in the reaction pathway. J. Biol. Chem. 274:1999;2166-2175.
26. Yuen M.H., Mizuguchi H., Lee Y.H., Cook P.F., Uyeda K., Hasemann C.A. Crystal structure of the H256A mutant of rat testis fructose-6-phosphate-2-kinase/fructose-2,6-bisphosphatase. Fructose 6-phosphate in the active site leads to mechanisms for both mutant and wild type bisphosphatase activities. J. Biol. Chem. 274:1999;2176-2184.
27. van Aalten D.M., de Groot B.L., Berendsen H.J., Findlay J.B. Conformational analysis of retinoids and restriction of their dynamics by retinoid-binding proteins. Biochem. J. 319:1996;543-550.
28. Hayward S., Berendsen H.J. Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins: Struct. Funct. Genet. 30:1998;144-154.
29. Mello L.V., van Aalten D.M., Findlay J.B. Dynamic properties of the guanine nucleotide binding protein alpha subunit and comparison of its guanosine triphosphate hydrolase domain with that of ras p21. Biochemistry. 37:1998;3137-3142.
30. Ledvina P.S., Yao N., Choudhary A., Quiocho F.A. Negative electrostatic surface potential of protein sites specific for anionic ligands. Proc. Natl Acad. Sci. USA. 93:1996;6786-6791.
31. Rigden D.J., Alexeev D., Phillips S.E., Fothergill-Gilmore L.A. The 2.3 Å X-ray crystal structure of S. cerevisiae phosphoglycerate mutase. J. Mol. Biol. 276:1998;449-459.
32. Bond C.S., White M.F., Hunter W.N. Mechanistic implications for Escherichia coli cofactor-dependent phosphoglycerate mutase based on the high-resolution crystal structure of a vanadate complex. J. Mol. Biol. 316:2002;1071-1081.
33. Bond C.S., White M.F., Hunter W.N. High resolution structure of the phosphohistidine-activated form of Escherichia coli cofactor-dependent phosphoglycerate mutase. J. Biol. Chem. 276:2001;3247-3253.
34. 6-tagging vectors allowing single-step purification of GroES and other polypeptides produced in Bacillus subtilis. Gene. 147:1994;91-94.
35. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1996;307-326.
36. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
37. Brunger A.T. The free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature. 355:1992;472-474.
38. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
39. Pannu N.S., Read R.J. Improved structure refinement through maximum likelihood. Acta Crystallog. sect. A. 52:1996;659-668.
40. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
41. 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. Crystallog. 26:1993;283-291.
42. Kleywegt G.J., Jones T.A. Efficient rebuilding of protein structures. Acta Crystallog. sect. D. 52:1996;829-832.
43. Kleywegt G.J. Experimental assessment of differences between related protein crystal structures. Acta Crystallog. sect. D. 55:1999;1878-1884.
44. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
45. Frishman D., Argos P. Knowledge-based secondary structure assignment. Proteins: Struct. Funct. Genet. 23:1995;566-579.
46. Nicholls A., Sharp K.A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
47. de Groot B.L., van Aalten D.M.F., Scheek R.M., Amadei A., Vriend G., Berendsen H.J.C. Prediction of protein conformational freedom from distance constraints. Proteins: Struct. Funct. Genet. 29:1997;240-251.
48. de Groot B.L., Vriend G., Berendsen H.J.C. Conformational changes in the chaperonin GroEL: new insights into the allosteric mechanism. J. Mol. Biol. 286:1999;1241-1249.
49. Labrou N.E., Mello L.V., Clonis Y.D. Functional and structural roles of the glutathione-binding residues in maize (Zea mays) glutathione S-transferase I. Biochem. J. 358:2001;101-110.
50. Mello L.V., de Groot B.L., Li S., Jedrzejas M.J. Mechanism of hyaluronan degradation by Streptococcus pneumoniae hyaluronate lyase. Structures of complexes with the substrate. J. Biol. Chem. 277:2002;36678-36688.
51. Amadei A., Linssen A.B.M., Berendsen H.J.C. Essential dynamics of proteins. Proteins: Struct. Funct. Genet. 17:1993;412-425.
52. Ichiye T., Karplus M. Collective motions in proteins: a covariance analysis of atomic fluctuations in molecular dynamics and normal mode simulations. Proteins: Struct. Funct. Genet. 11:1991;205-217.
53. van Aalten D.M.F., Amadei A., Vriend G., Linssen A.B.M., Venema G., Berendsen H.J.C., Eijsink V.G.H. The essential dynamics of thermolysin: confirmation of the hinge-bending motion and comparison of simulations in vacuum and water. Proteins: Struct. Funct. Genet. 22:1995;45-54.
54. Stec B., Holtz K.M., Kantrowitz E.R. A revised mechanism for the alkaline phosphatase reaction involving three metal ions. J. Mol. Biol. 299:2000;1303-1311.
55. Holtz K.M., Stec B., Kantrowitz E.R. A model of the transition state in the alkaline phosphatase reaction. J. Biol. Chem. 274:1999;8351-8354.
56. Murphy J.E., Stec B., Ma L., Kantrowitz E.R. Trapping and visualization of a covalent enzyme-phosphate intermediate. Nature Struct. Biol. 4:1997;618-622.