An engineered disulfide bond between residues 69 and 238 in extended-spectrum β-lactamase toho-1 reduces its activity toward third-generation cephalosporins

Biochemistry

Volumn 43, Issue 50, 2004, Pages 15737-15745

  Shimizu Ibuka, Akiko ^a,c   Matsuzawa, Hiroshi ^b   Sakai, Hiroshi ^a  

^a UNIVERSITY OF SHIZUOKA   (Japan)

^b AOMORI UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CHEMICAL BONDS; ENZYMES; MUTAGENESIS; TITRATION;

CEPHALOSPORINS; GLYCINE; SUBSTRATE-BINDING SITE;

CRYSTALLOGRAPHY;

ASPARAGINE; BETA LACTAMASE; CEPHALOSPORIN; CYSTEINE; GLYCINE; MUTANT PROTEIN; PENICILLIN G; SERINE;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; DISULFIDE BOND; ENZYME ACTIVITY; KINETICS; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

AMINO ACID SEQUENCE; BETA-LACTAMASES; BINDING SITES; CEPHALOSPORINS; CRYSTALLOGRAPHY, X-RAY; DISULFIDES; DITHIONITROBENZOIC ACID; ESCHERICHIA COLI PROTEINS; MOLECULAR SEQUENCE DATA; POINT MUTATION; PROTEIN ENGINEERING; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

EID: 10844223675     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048488u     Document Type: Article

References (43)

1. Ambler, R. P., Coulson, A. F., Frere, J.-M., Ghuysen, J.-M., Joris, B., Forsman, M., Levesque, R. C., Tiraby, G., and Waley, S. G. (1991) A standard numbering scheme for the class A β-lactamases, Biochem. J. 276, 269-270.
2. Helfand, M. S., and Bonomo, R. A. (2003) β-Lactamases: A survey of protein diversity, Curr. Drug Targets Infect. Disord. 3, 9-23.
3. Matagne, A., Lamotte-Brasseur, J., and Frere, J.-M. (1998) Catalytic properties of class A β-lactamases: Efficiency and diversity, Biochem. J. 330, 581-598.
4. Matagne, A., and Frere, J.-M. (1995) Contribution of mutant analysis to the understanding of enzyme catalysis: The case of class A β-lactamases, Biochim. Biophys. Acta 1246, 109-127.
5. Petrosino, J., Cantu, C., III, and Palzkill, T. (1998) β-Lactamases: Protein evolution in real time, Trends Microbiol. 6, 323-327.
6. Knox, J. R. (1995) Extended-spectrum and inhibitor-resistant TEM-type β-lactamases: Mutations, specificity, and three-dimensional structure, Antimicrob. Agents Chemother. 39, 2593-2601.
7. Tzouvelekis, L. S., Tzelepi, E., Tassios, P. T., and Legakis, N. J. (2000) CTX-M-type β-lactamases: An emerging group of extended-spectrum enzymes, Int. J. Antimicrob. Agents 14, 137-142.
8. Ibuka, A., Taguchi, A., Ishiguro, M., Fushinobu, S., Ishii, Y., Kamitori, S., Okuyama, K., Yamaguchi, K., Konno, M., and Matsuzawa, H. (1999) Crystal structure of the E166A mutant of extended-spectrum β-lactamase Toho-1 at 1.8 Å resolution, J. Mol. Biol. 285, 2079-2087.
9. Naas, T., Vandel, L., Sougakoff, W., Livermore, D. M., and Nordmann, P. (1994) Cloning and sequence analysis of the gene for a carbapenem-hydrolyzing class A β-lactamase, Sme-1, from Serratia marcescens S6, Antimicrob. Agents Chemother. 38, 1262-1270.
10. Nordmann, P., Mariotte, S., Naas, T., Labia, R., and Nicolas, M. H. (1993) Biochemical properties of a carbapenem-hydrolyzing β-lactamase from Enterobacter cloacae and cloning of the gene into Escherichia coli, Antimicrob. Agents Chemother. 37, 939-946.
11. Sougakoff, W., L'Hermite, G., Pernot, L., Naas, T., Guillet, V., Nordmann, P., Jarlier, V., and Delettre, J. (2002) Structure of the imipenem-hydrolyzing class A β-lactamase SME-1 from Serratia marcescens, Acta Crystallogr. D58, 267-274.
12. Swaren, P., Maveyraud, L., Raquet, X., Cabantous, S., Duez, C., Pedelacq, J. D., Mariotte-Boyer, S., Mourey, L., Labia, R., Nicolas-Chanoine, M. H., Nordmann, P., Frere, J.-M., and Samama, J. P. (1998) X-ray analysis of the NMC-A β-lactamase at 1.64-Å resolution, a class A carbapenemase with broad substrate specificity, J. Biol. Chem. 273, 26714-26721.
13. Raquet, X., Lamotte-Brasseur, J., Bouillenne, F., and Frere, J. M. (1997) A disulfide bridge near the active site of carbapenem-hydrolyzing class A β-lactamases might explain their unusual substrate profile, Proteins 27, 47-58.
14. Ishii, Y., Ohno, A., Taguchi, H., Imajo, S., Ishiguro, M., and Matsuzawa, H. (1995) Cloning and sequence of the gene encoding a cefotaxime-hydrolyzing class A β-lactamase isolated from Escherichia coli, Antimicrob. Agents Chemother. 39, 2269-2275.
15. Ibuka, A. S., Ishii, Y., Galleni, M., Ishiguro, M., Yamaguchi, K., Frere, J.-M., Matsuzawa, H., and Sakai H. (2003) Crystal structure of extended-spectrum β-lactamase Toho-1: Insights into the molecular mechanism for catalytic reaction and substrate specificity expansion, Biochemistry 42, 10634-10643.
16. Kunkel, T. A., Roberts, J. D., and Zakour, R. A. (1987) Rapid and efficient site-specific mutagenesis without phenotypic selection, Methods Enzymol. 154, 367-382.
17. Creighton, T. E. (1989) Disulphide bonds between cysteine residues, in Protein Structure: A Practical Approach (Creighton, T. E., Ed.) 1st ed., pp 155-157, IRL Press at Oxford University Press, New York.
18. De Meester, F., Joris, B., Reckinger, G., Bellefroid-Bourguignon, C., Frere, J.-M., and Waley, S.-G. (1987) Automated analysis of enzyme inactivation phenomena. Application to β-lactamases and DD-peptidases, Biochem. Pharmacol. 36, 2393-2403.
19. Steller, I., Bolotovsky, R., and Rossmann, M. G. (1997) An algorithm for automatic indexing of oscillation images using Fourier analysis, J. Appl. Crystallogr. 30, 1036-1040.
20. Bolotovsky, R., Steller, I., and Rossmann M. G. (1998) The use of partial reflections for scaling and averaging X-ray area-detector data, J. Appl. Crystallogr. 31, 708-717.
21. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
22. Jones, T. A., and Kjeldgaard, M. (1995) Manual for O version 5.10, Uppsala University, Uppsala, Sweden.
23. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
24. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography, Acta Crystallogr. D50, 760-763.
25. Herzberg, O. (1991) Refined crystal structure of β-lactamase from Staphylococcus aureus PC1 at 2.0 Å resolution, J. Mol. Biol. 217, 701-719.
26. Huletsky, A., Knox, J. R., and Levesque, R. C. (1993) Role of Ser-238 and Lys-240 in the hydrolysis of third-generation cephalosporins by SHV-type β-lactamases probed by site-directed mutagenesis and three-dimensional modeling, J. Biol. Chem. 268, 3690-3697.
27. Venkatachalam, K. V., Huang, W., LaRocco, M., and Palzkill, T. (1994) Characterization of TEM-1 β-lactamase mutants from positions 238 to 241 with increased catalytic efficiency for ceftazidime, J. Biol. Chem. 269, 23444-23450.
28. Taibi, P., and Mobashery, S. (1995) Mechanism of Turnover of Imipenem by TEM, J. Am. Chem. Soc. 117, 7600-7605.
29. Zawadzke, L. E., Smith, T. J., and Herzberg, O (1995) An engineered Staphylococcus aureus PC1 β-lactamase that hydrolyses third-generation cephalosporins, Protein Eng. 8, 1275-1285.
30. Cantu, C., III, Huang, W., and Palzkill, T. (1996) Selection and characterization of amino acid substitutions at residues 237-240 of TEM-1 β-lactamase with altered substrate specificity for aztreonam and ceftazidime, J. Biol. Chem. 271, 22538-22545.
31. Shimamura, T., Ibuka, A., Fushinobu, S., Wakagi, T., Ishiguro, M., Ishii, Y., and Matsuzawa, H. (2002) Acyl-intermediate structures of the extended-spectrum class A β-lactamase, Toho-1, in complex with cefotaxime, cephalothin, and benzylpenicillin, J. Biol. Chem. 277, 46601-46608.
32. Tranier, S., Bouthors, A. T., Maveyraud, L., Guillet, V., Sougakoff, W., and Samama, J. P. (2000) The high-resolution crystal structure for class A β-lactamase PER-1 reveals the bases for its increase in breadth of activity, J. Biol. Chem. 275, 28075-28082.
33. Knox, J. R., Moews, P. C., and Frere, J. M. (1996) Molecular evolution of bacterial β-lactam resistance, Chem. Biol. 3, 937-947.
34. Banerjee, S., Pieper, U., Kapadia, G., Pannell, L. K., and Herzberg, O. (1998) Role of the Ω-loop in the activity, substrate specificity, and structure of class A β-lactamase, Biochemistry 37, 3286-3296.
35. Tamaki, M., Nukaga, M., and Sawai, T. (1994) Replacement of serine 237 in class A β-lactamase of Proteus vulgaris modifies its unique substrate specificity, Biochemistry 33, 10200-10206.
36. Nukaga, M., Mayama, K., Crichlow, G. V., and Knox, J. R. (2002) Structure of an extended-spectrum class A β-lactamase from Proteus vulgaris K1, J. Mol. Biol. 317, 109-117.
37. Sougakoff, W., Naas, T., Nordmann, P., Collatz, E., and Jarlier, V. (1999) Role of Ser-237 in the substrate specificity of the carbapenem- hydrolyzing class A β-lactamase Sme-1, Biochim. Biophys. Acta 1433, 153-158.
38. Gazouli, M., Tzelepi, E., Sidorenko, S. V., and Tzouvelekis, L. S. (1998) Sequence of the gene encoding a plasmid-mediated cefotaxime-hydrolyzing class A β-lactamase (CTX-M-4): Involvement of serine 237 in cephalosporin hydrolysis, Antimicrob. Agents Chemother. 42, 1259-1262.
39. Majiduddin, F. K., and Palzkill, T. (2003) Amino acid sequence requirements at residues 69 and 238 for the SME-1 β-lactamase to confer resistance to β-lactam antibiotics, Antimicrob. Agents Chemother. 47, 1062-1067.
40. Kraulis, P. J. (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures, J. Appl. Crystallogr. 24, 946-950.
41. Esnouf, R. M. (1997) An extensively modified version of MolScript that includes greatly enhanced coloring capabilities, J. Mol. Graphics 15, 132-134.
42. Bacon, D. J., and Anderson, W. F. (1988) A fast algorithm for rendering space-filling molecule pictures, J. Mol. Graphics 6, 219-220.
43. Merritt, E. A., and Murphy, M. E. P. (1994) Raster3D version 2.0: A program for photorealistic molecular graphics, Acta Crystallogr. D50, 869-873.