Structural and mechanistic changes along an engineered path from metallo to nonmetallo 3-deoxy-D-manno-octulosonate 8-phosphate synthases

Biochemistry

Volumn 46, Issue 15, 2007, Pages 4532-4544

  Kona, Fathima ^a   Xu, Xingjue ^a   Martin, Philip ^a   Kuzmic, Petr ^a,b   Gatti, Domenico L ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BioKin Ltd   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; NONMETALLO SYNTHASES; WATER MOLECULES;

ESCHERICHIA COLI; MOLECULAR STRUCTURE; MUTAGENESIS; PHOSPHATES; THERMODYNAMIC STABILITY;

ENZYMES;

3 DEOXY DEXTRO MANNOOCTULOSONATE 8 PHOSPHATE SYNTHASE; BACTERIAL ENZYME; MUTANT PROTEIN; SYNTHETASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AQUIFEX AEOLICUS; ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; HYDROGEN BOND; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; THERMOSTABILITY; X RAY CRYSTALLOGRAPHY;

ALDEHYDE-LYASES; ASPARAGINE; BACTERIAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; ENZYME STABILITY; KINETICS; METALS; MODELS, CHEMICAL; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PHOSPHOENOLPYRUVATE; PROTEIN BINDING; SUBSTRATE SPECIFICITY;

AQUIFEX AEOLICUS; ESCHERICHIA COLI;

EID: 34247188488     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi6024879     Document Type: Article

References (44)

1. Raetz, C. R., and Whitfield, C. (2002) Lipopolysaccharide endotoxins, Annu. Rev. Biochem. 71, 635-700.
2. Raetz, C. R. (1990) Biochemistry of endotoxins, Annu. Rev. Biochem. 59, 129-170.
3. Levin, D. H., and Racker, E. (1959) Condensation of arabinose 5-phosphate and phosphorylenol pyruvate by 2-keto-3-deoxy-phosphooctonic acid synthetase, J. Biol. Chem. 234, 2532-2539.
4. Li, Z., Sau, A. K., Shen, S., Whitehouse, C., Baasov, T., and Anderson, K. S. (2003) A snapshot of enzyme catalysis using electrospray ionization mass spectrometry, J. Am. Chem. Soc. 125, 9938-9939.
5. Duewel, H. S., Radaev, S., Wang, J., Woodard, R. W., and Gatti, D. L. (2001) Substrate and metal complexes of 3-deoxy-D-manno- octulosonate 8-phosphate synthase from Aquifex aeolicus at 19 Å resolution: implications for the condensation mechanism, J. Biol. Chem. 276, 8393-8402.
6. Wang, J., Duewel, H. S., Woodard, R. W., and Gatti, D. L. (2001) Structures of Aquifex aeolicus KDO8P synthase in complex with R5P and PEP, and with a bisubstrate inhibitor: role of active site water in catalysis, Biochemistry 40, 15676-15683.
7. Kohen, A., Berkovich, R., Belakhov, V., and Baasov, T. (1993) Stereochemistry of KDO8P synthase. An efficient synthesis of the 3-fluoro analogs of KDO8P, Bioorg. Med. Chem. Lett. 3, 1577-1582.
8. Dotson, G. D., Dua, R. K., Clemens, J. C., Wooten, E. W., and Woodard, R. W. (1995) Overproduction and one-step purification of Escherichia coli 3-deoxy-D-manno-octulosonic acid 8-phosphate synthase and oxygen transfer studies during catalysis using isotopic-shifted heteronuclear NMR, J. Biol. Chem. 270, 13698-13705.
9. Dotson, G. D., Nanjappan, P., Reily, M. D., and Woodard, R. W. (1993) Stereochemistry of 3-deoxyoctulosonate 8-phosphate synthase, Biochemistry 32, 12392-12397.
10. Furdui, C., Zhou, L., Woodard, R. W., and Anderson, K. S. (2004) Insights into the mechanism of 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase (Phe) from Escherichia coli using a transient kinetic analysis, J. Biol. Chem. 279, 45618-45625.
11. Birck, M. R., and Woodard, R. W. (2001) Aquifex aeolicus 3-deoxy-D-manno-2-octulosonic acid 8-phosphate synthase: a new class of KDO 8-P synthase?, J. Mol. Evol. 52, 205-214.
12. Duewel, H. S., and Woodard, R. W. (2000) A metal bridge between two enzyme families. 3-deoxy-D-manno-octulosonate 8-phosphate synthase from Aquifex aeolicus requires a divalent metal for activity, J. Biol. Chem. 275, 22824-22831.
13. Radaev, S., Dastidar, P., Patel, M., Woodard, R. W., and Gatti, D. L. (2000) Structure and mechanism of 3-deoxy-D-manno-octulosonate 8-phosphate synthase, J. Biol. Chem. 275, 9476-9484.
14. Wagner, T., Kretsinger, R. H., Bauerle, R., and Tolbert, W. D. (2000) 3-Deoxy-D-manno-octulosonate-8-phosphate synthase from Escherichia coli. model of binding of phosphoenolpyruvate and D-arabinose-5- phosphate, J. Mol. Biol. 301, 233-238.
15. Vainer, R., Belakhov, V., Rabkin, E., Baasov, T., and Adir, N. (2005) Crystal structures of Escherichia coli KDO8P synthase complexes reveal the source of catalytic irreversibility, J. Mol. Biol. 351, 641-652.
16. Wang, J., Duewel, H. S., Stuckey, J. A., Woodard, R. W., and Gatti, D. L. (2002) Function of His185 in Aquifex aeolicus 3-deoxy-D- manno-octulosonate 8-phosphate synthase, J. Mol. Biol. 324, 205-214.
17. Xu, X., Kona, F., Wang, J., Lu, J., Stemmler, T., and Gatti, D. L. (2005) The catalytic and conformational cycle of Aquifex aeolicus KDO8P synthase: role of the L7 loop, Biochemistry 44, 12434-12444.
18. Asojo, O., Friedman, J., Adir, N., Belakhov, V., Shoham, Y., and Baasov, T. (2001) Crystal structures of KDOP synthase in its binary complexes with the substrate phosphoenolpyruvate and with a mechanism-based inhibitor, Biochemistry 40, 6326-6334.
19. Kaustov, L., Kababya, S., Du, S., Baasov, T., Gropper, S., Shoham, Y., and Schmidt, A. (2000) Structural and mechanistic investigation of 3-deoxy-D-manno-octulosonate-8-phosphate synthase by solid-state REDOR NMR, Biochemistry 39, 14865-14876.
20. Li, J., Wu, J., Fleischhacker, A. S., and Woodard, R. W. (2004) Conversion of Aquifex aeolicus 3-deoxy-D-manno- octulosonate 8-phosphate synthase, a metalloenzyme, into a nonmetalloenzyme, J. Am. Chem. Soc. 126, 7448-7449.
21. Oliynyk, Z., Briseno-Roa, L., Janowitz, T., Sondergeld, P., and Fersht, A. R. (2004) Designing a metal-binding site in the scaffold of Escherichia coli KDO8PS, Protein Eng., Des. Sel. 17, 383-390.
22. Shulami, S., Furdui, C., Adir, N., Shoham, Y., Anderson, K. S., and Baasov, T. (2004) A reciprocal single mutation affects the metal requirement of 3-deoxy-D-manno-2-octulosonate-8-phos-phate (KDO8P) synthases from Aquifex pyrophilus and Escherichia coli, J. Biol. Chem. 279, 45110-45120.
23. Nozaki, Y. (1972) The preparation of guanidine hydrochloride, Methods Enzymol. 26 (Part C), 43-50.
24. Royer, C. A., Mann, C. J., and Matthews, C. R. (1993) Resolution of the fluorescence equilibrium unfolding profile of trp aporepressor using single tryptophan mutants, Protein Sci. 2, 1844-1852.
25. Fersht, A. (1999) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding, W. H. Freeman, New York.
26. Duggleby, R. G. (1995) Analysis of enzyme progress curves by nonlinear regression, Methods Enzymol. 249, 61-90.
27. Beechem, J. M. (1992) Global analysis of biochemical and biophysical data, Methods Enzymol. 210, 37-54.
28. Kuzmic, P. (1996) Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase, Anal. Biochem. 237, 260-273.
29. Bates, D. M., and Watts, D. G. (1998) Nonlinear Regression Analysis and its Applications, Wiley, New York.
30. Duewel, H. S., Sheflyan, G. Y., and Woodard, R, W. (1999) Functional and biochemical characterization of a recombinant 3-deoxy-D-manno- octulosonic acid 8-phosphate synthase from the hyperthermophilic bacterium Aquifex aeolicus, Biochem. Biophys. Res. Commun. 263, 346-351.
31. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
32. Adams, P. D., Pannu, N. S., Read, R. J., and Brunger, A. T. (1997) Cross-validated maximum likelihood enhances crystallographic simulated annealing refinement, Proc. Natl. Acad. Sci. U.S.A. 94, 5018-5023.
33. Goldenberg, D. P. (1992) Mutational analysis of protein folding and stability, in Protein Folding (Creighton, T. E., Ed.) pp 353-403, W. H. Freeman, New York.
34. Shortle, D., and Meeker, A. K. (1986) Mutant forms of staphylococcal nuclease with altered patterns of guanidine hydrochloride and urea denaturation, Proteins 1, 81-89.
35. Segel, I. (1975) Enzyme Kinetics. Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems, John Wiley & Sons, New York.
36. King, E. L., and Altman, C. (1956) A schematic method of deriving the rate laws for enzyme-catalyzed reactions, J. Phys. Chem. 60, 1375-1378.
37. Cornish-Bowden, A. (1995) Fundamentals of Enzyme Kinetics, revised ed., Portland Press, London.
38. Cleland, W. W. (1963) The kinetics of enzyme-catalyzed reactions with two or more substrates or products. III. Prediction of initial velocity and inhibition patterns by inspection, Biochim. Biophys. Acta 67, 188-196.
39. Bevington, P. R. (1969) Data Reduction and Error Analysis for the Physical Sciences, McGraw-Hill, New York.
40. Ray, P. H. (1980) Purification and characterization of 3-deoxy-D-manno-octulosonate 8-phosphate synthetase from Escherichia coli, J. Bacteriol. 141, 635-644.
41. Howe, D. L., Sundaram, A. K., Wu, J., Gatti, D. L., and Woodard, R. W. (2003) Mechanistic insight into 3-deoxy-D-manno-octulosonate-8- phosphate synthase and 3-deoxy-D-arabino-heptulosonate-7- phosphate synthase utilizing phosphorylated monosaccharide analogues, Biochemistry 42, 4843-4854.
42. Shumilin, I. A., Bauerle, R., and Kretsinger, R. H. (2003) The high-resolution structure of 3-deoxy-D-arabino-heptulosonate-7- phosphate synthase reveals a twist in the plane of bound phosphoenolpyruvate, Biochemistry 42, 3766-3776.
43. Shumilin, I. A., Bauerle, R., Wu, J., Woodard, R. W., and Kretsinger, R. H. (2004) Crystal structure of the reaction complex of 3-deoxy-D- arabino-heptulosonate-7-phosphate synthase from Thermotoga maritima refines the catalytic mechanism and indicates a new mechanism of allosteric regulation, J. Mol. Biol. 341, 455-466.
44. Jensen, R. A., Xie, G., Calhoun, D. H., and Bonner, C. A. (2002) The correct phylogenetic relationship of KdsA (3-deoxy-D-manno- octulosonate 8-phosphate synthase) with one of two independently evolved classes of AroA (3-deoxy-D-arabino-heptulosonate 7-phosphate synthase), J. Mol. Evol. 54, 416-423.