Structure and mechanism of the genomically encoded fosfomycin resistance protein, FosX, from Listeria monocytogenes

Biochemistry

Volumn 46, Issue 27, 2007, Pages 8110-8120

  Fillgrove, Kerry L ^a,c   Pakhomova, Svetlana ^b   Schaab, Matthew R ^a   Newcomer, Marcia E ^b   Armstrong, Richard N ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

^c MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; FOSFOMYCIN RESISTANCE PROTEIN; LISTERIA MONOCYTOGENES; PATHOGENIC MICROORGANISMS;

AMINO ACIDS; ANTIBIOTICS; GENE ENCODING; MICROORGANISMS; MUTAGENESIS; PATHOGENS;

PROTEINS;

AMINO ACID; BACTERIAL PROTEIN; CARBOXYLIC ACID; EPOXYPROPYLPHOSPHONIC ACID; ETHYLENE OXIDE DERIVATIVE; FOSA PROTEIN; FOSFOMYCIN; FOSX PROTEIN; PHOSPHONIC ACID DERIVATIVE; UNCLASSIFIED DRUG; WATER;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; CARBOXY TERMINAL SEQUENCE; CATALYST; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; GENETIC CODE; HYDRATION; LISTERIA MONOCYTOGENES; METAL BINDING; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE;

BACTERIAL PROTEINS; BASE SEQUENCE; CRYSTALLOGRAPHY; DNA PRIMERS; DRUG RESISTANCE, MICROBIAL; FOSFOMYCIN; LISTERIA MONOCYTOGENES; MODELS, MOLECULAR; POINT MUTATION; PROTEIN CONFORMATION;

LISTERIA MONOCYTOGENES;

EID: 34447345970     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700625p     Document Type: Article

References (33)

1. Walsh, C. (2000) Molecular mechanisms that confer antibacterial drug resistance, Nature 406, 775-781.
2. Hendlin, D., Stapley, E. O., Jackson, M., Wallick, H., Miller, A. K., Wolf, F. J., Miller, T. W., Chaiet, L., Kahan, F. M., Flotz, E. L., Woodruff, H. B., Mata, J. M., Hernandez, S., and Mochales, S. (1969) Phosphonomycin, a new antibiotic produced by strains of Streptomyces, Science 166, 122-123.
3. Christensen, B. G., Leanza, W. J., Beattie, T. R., Patchett, A. A., Arison, B. H., Ormond, R. E., Kuehl, F. A., Albers-Schonberg, G., and Jardetzky, O. (1969) Phosphonomycin: Structure and synthesis, Science 166, 123-124.
4. Stapley, E. O., Hendlin, D., Mata, J. M., Jackson, M., Wallick, H., Hernandez, S., Mochales, S., Currie, S. A., and Miller, R. M. (1969) Phosphonomycin. I. Discovery and in vitro biological characterization, Antimicrob. Agents Chemother. 9, 284-290.
5. Kahan, F. M., Kahan, J. S., Cassidy, P. J., and Kroop, H. (1974) The mechanism of action of fosfomycin (phosphonomycin), Ann. N.Y. Acad. Sci. 235, 364-385.
6. Marquardt, J. L., Brown, E. D., Lane, W. S., Haley, T. M., Ichskawa, Y., Wong, C.-H., and Walsh, C. T. (1994) Kinetics, stoichiometry, and identification of the reactive thiolate in the inactivation of UDP-GlcNAc enolpyravoyl transferase by the antibiotic fosfomycin, Biochemistry 33, 10646-10651.
7. Skarzynski, T., Mistry, A., Wonacott, A., Hutchinson, S. E., Kelly, V. A., and Duncan, K. (1996) Structure of UDP-N-acetylglucosamine enolpyruvyl transferase, an enzyme essential for the synthesis of bacterial peptidoglycan, complexed with substrate UDP-N-acetylglucosamine and the drug fosfomycin, Structure 4, 1465-1474.
8. Kadner, R. J., and Winkler, H. H. (1975) Energy coupling for methionine transport in Escherichia coli, J. Bacteriol. 123, 985-991.
9. Tsuruoka, T., and Yamada, Y. (1975) Charactertization of spontaneous fosfomycin (phosphonomycin)-resistant cells of Escherichia coli B in vitro, J. Antibiot. 28, 906-911.
10. Venkateswaran, P. S., and Wu, H. C. (1972) Isolation and characterization of a phosphonomycin-resistant mutant of Escherichia coli K-12, J. Bacteriol. 110, 935-944.
11. Garcia-Lobo, J. M., and Ortiz, J. M. (1982) Tn2921, a transposon encoding fosfomycin resistance, J. Bacteriol. 151, 477-479.
12. Arca, P., Rico, M., Brana, A. F., Villar, C. J., Hardisson, C., and Suarez, J. E. (1988) Formation of an adduct between fosfomycin and glutathione: A new mechanism of antibiotic resistance in bacteria, Antimicrob. Agents Chemother. 32, 1552-1556.
13. Arca, P., Hardisson, C., and Suarez, J. E. (1990) Purification of a glutathione S-transferase that mediates fosfomycin resistance in bacteria, Antimicrob. Agents Chemother. 34, 844-848.
14. Bernat, B. A., Laughlin, L. T., and Armstrong, R. N. (1997) Fosfomycin resistance protein (FosA) is a manganese metalloglutathione transferase related to glyoxalase I and the extradiol dioxygenases, Biochemistry 36, 3050-3055.
15. Bernat, B. A., Laughlin, L. T., and Armstrong, R. N. (1999) Elucidation of a Monovalent Cation Dependence and Characterization of the Divalent Cation Binding Site of the Fosfomycin Resistance Protein, FosA, Biochemistry 38, 7462-7469.
16. Cao, M., Bernat, B. A., Wang, Z., Armstrong, R. N., and Helmann, J. D. (2001) FosB, a cysteine-dependent fosfomycin resistance protein under the control of σW, an extracytoplasmic function σ factor in Bacillus subtilis, J. Bacteriol. 183, 2380-2383.
17. Fillgrove, K. L., Pakhomova, S., Newcomer, M. E., and Armstrong, R. N. (2003) Mechanistic diversity of fosfomycin resistance in pathogenic microorganisms, J. Am. Chem. Soc. 125, 15730-15731.
18. +, J. Am. Chem. Soc. 124, 11001-11003.
19. 11B NMR study of p-carboxybenzeneboronic acid ions for complex formation with some monosaccharides, Anal. Sci. 19, 455-460.
20. Rigsby, R. E., Fillgrove, K. L., Beihoffer, L., and Armstrong, R. N. (2005) Fosfomycin Resistance Proteins: A Nexus of Glutathione Transferases and Epoxide Hydrolases in a Metalloenzyme Superfamily, Methods Enzymol. 401, 367-379.
21. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
22. Collaborative Computatonal Project, Number 4 (1994) The CCP4 suite: Program for protein crystallography, Acta Crystallogr. D50, 760-763.
23. Adams, D. P., Pannu, N. S., Read, R. J., and Branger, A. T. (1997) Cross-validated maximum likelihood enhances crystallographic simulated annealing refinement, Proc. Natl. Acad. Sci. U.S.A. 94, 5018-5023.
24. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A47, 110-119.
25. Glaser, P., Frangeul, L., Buchrieser, C., Rusniok, C., Amend, A., Baquero, F., Berche, P., Bloecker, H., Brandt, P., Chakraborty, T., Charbit, A., Chetouani, F., Couve, E., de Daruvar, A., Dehoux, P., Domann, E., Dominguez-Bernal, G., Duchaud, E., Durant, L., Dussurget, O., Entian, K. D., Fsihi, H., Garcia-del Portillo, F., Garrido, P., Gautier, L., Goebel, W., Gomez-Lopez, N., Hain, T., Hauf, J., Jackson, D., Jones, L. M., Kaerst, U., Kreft, J., Kuhn, M., Kunst, F., Kurapkat, G., Madueno, E., Maitournam, A., Vicente, J. M., Ng, E., Nedjari, H., Nordsiek, G., Novella, S., de Pablos, B., Perez-Diaz, J. C., Purcell, R., Remmel, B., Rose, M., Schlueter, T., Simoes, N., Tierrez, A., Vazquez-Boland, J. A., Voss, H., Wehland, J., and Cossart, P. (2001) Comparative genomics of Listeria species, Science 294, 849-852.
26. Pakhomova, S., Rife, C. L., Armstrong, R. N., and Newcomer, M. E. (2004) Structure of fosfomycin resistance protein FosA from transposon Tn2921, Protein Sci. 13, 1260-1265.
27. Armstrong, R. N. (2000) Mechanistic Diversity in a Metalloenzyme Superfamily, Biochemistry 39, 13625-13632.
28. Bergdoll, M., Eltis, L. D., Cameron, A. D., Dumas, P., and Bolin, J. T. (1998) All in the family: Structural and evolutionary relationships among three modular proteins with diverse functions and variable assembly. Protein Sci. 7, 1661-1670.
29. DeLano, W. L. (2002) The PyMOL Molecular Graphics, DeLano Scientific, San Carlos, CA.
30. Lacourciere, G. M., and Armstrong, R. N. (1993) The catalytic mechanism of microsomal epoxide hydrolase involves an ester intermediate, J. Am. Chem. Soc. 115, 10466-10467.
31. Armstrong, R. N. (1999) Nucleophilic Epoxide Openings, in Comprehensive Natural Products Chemistry (Poulter, C. D., Ed.) Vol. 5, pp 51-70, Elsevier Science, Oxford, U.K.
32. Bernat, B. A., Laughlin, L. T., and Armstrong, R. N. (1998) Regiochemical and Stereochemical Course of the Reaction Catalyzed by the Fosfomycin Resistance Protein, FosA, J. Org. Chem. 63, 3778-3780.
33. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF chimera: A visualization system for exploratory research and analysis, J. Comput. Chem. 25, 1605-1612.