Characterization of the β-lactam antibiotic sensor domain of the MecR1 signal sensor/transducer protein from methicillin-resistant Staphylococcus aureus

Biochemistry

Volumn 46, Issue 26, 2007, Pages 7822-7831

  Cha, Jooyoung ^a   Vakulenko, Sergei B ^a   Mobashery, Shahriar ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS (MRSA); PENICILLIN;

ACYLATION; ANTIBIOTICS; BACTERIA; PROTEINS; SIGNAL TRANSDUCTION;

BIOSENSORS;

AMINO ACID; AMPICILLIN; ANTIBIOTIC AGENT; BACTERIAL PROTEIN; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE; BLAI PROTEIN; BLAR1 PROTEIN; CARBAPENEM; CARBON DIOXIDE; CEFEPIME; CEFTAZIDIME; CEPHALOSPORIN; GENOMIC DNA; IMIPENEM; KANAMYCIN A; LYSINE; MECI PROTEIN; MECR1 PROTEIN; METICILLIN; NITROCEFIN; OXACILLIN; PENICILLIN BINDING PROTEIN 2A; PENICILLIN DERIVATIVE; UNCLASSIFIED DRUG;

ACYLATION; ARTICLE; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIUM CULTURE; BLAI GENE; BLAZ GENE; CARBON NUCLEAR MAGNETIC RESONANCE; CARBOXYLATION; CIRCULAR DICHROISM; DISSOCIATION CONSTANT; ESCHERICHIA COLI; GENETIC TRANSCRIPTION; KINETICS; MECA GENE; MECI GENE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULAR CLONING; MULTIDRUG RESISTANCE; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SENSOR; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS INFECTION; TRANSCRIPTION REGULATION; ULTRAVIOLET SPECTROPHOTOMETRY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BETA-LACTAMS; BINDING SITES; CARRIER PROTEINS; CIRCULAR DICHROISM; CLONING, MOLECULAR; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; KINETICS; LYSINE; MUTAGENESIS, SITE-DIRECTED; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PENICILLIN-BINDING PROTEINS; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS;

EID: 34347349122     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7005459     Document Type: Article

References (49)

1. Berger-Bachi, B., and Rohrer, S. (2002) Factors influencing methicillin resistance in staphylococci, Arch. Microbiol. 178, 165-171.
2. Chang, S., Sievert, D. M., Hageman, J. C., Boulton, M. L., Tenover, F. C., Downes, F. P., Shah, S., Rudrik, J. T., Pupp, G. R., Brown, W. J., Cardo, D., and Fridkin, S. K. (2003) Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene, N. Engl. J. Med. 348, 1342-1347.
3. Gonzalez-Zorn, B., and Courvalin, P. (2003) vanA-mediated high level glycopeptide resistance in MRSA, Lancet Infect. Dis. 3, 67-68.
4. Severin, A., Tabei, K., Tenover, F., Chung, M., Clarke, N., and Tomasz, A. (2004) High level oxacillin and vancomycin resistance and altered cell wall composition in Staphylococcus aureus carrying the staphylococcal mecA and the enterococcal vanA gene complex, J. Biol. Chem. 279, 3398-3407.
5. Fuda, C., Suvorov, M., Vakulenko, S. B., and Mobashery, S. (2004) The basis for resistance to beta-lactam antibiotics by penicillin-binding protein 2a of methicillin-resistant Staphylococcus aureus, J. Biol. Chem. 279, 40802-40806.
6. Chambers, H. F. (1997) Methicillin resistance in staphylococci: Molecular and biochemical basis and clinical implications, Clin. Microbiol. Rev. 10, 781.
7. Katayama, Y., Zhang, H. Z., and Chambers, H. F. (2004) PBP 2a mutations producing very-high-level resistance to β-lactams, Antimicrob. Agents Chemother. 48, 453-459.
8. Pinho, M. G., de Lencastre, H., and Tomasz, A. (2001) An acquired and a native penicillin-binding protein cooperate in building the cell wall of drug-resistant staphylococci, Proc. Natl. Acad. Sci. U.S.A. 98, 10886-10891.
9. Zhu, Y. F., Curran, I. H. A., Joris, B., Ghuysen, J. M., and Lampen, J. O. (1990) Identification of blar, the signal transducer for β-lactamase production in Bacillus licheniformis, as a penicillin-binding protein with strong homology to the OXA-2 β-lactamase (class-D) of Salmonella typhimurium, J. Bacteriol. 172, 1137-1141.
10. Garcia-Castellanos, R., Mallorqui-Fernandez, G., Marrero, A., Potempa, J., Coll, M., and Gomis-Ruth, F. X. (2004) On the transcriptional regulation of methicillin resistance - MecI repressor in complex with its operator, J. Biol. Chem. 279, 17888-17896.
11. Van Melckebeke, H., Vreuls, C., Gans, P., Filee, P., Llabres, G., Joris, B., and Simorre, J. P. (2003) Solution structural study of BlaI: Implications for the repression of genes involved in β-lactam antibiotic resistance, J. Mol. Biol. 333, 711-720.
12. McKinney, T. K., Sharma, V. K., Craig, W. A., and Archer, G. L. (2001) Transcription of the gene mediating methicillin resistance in Staphylococcus aureus (mecA) is corepressed but not coinduced by cognate mecA and β-lactamase regulators, J. Bacteriol. 183, 6862-6868.
13. Golemi-Kotra, D., Cha, J. Y., Meroueh, S. O., Vakulenko, S. B., and Mobashery, S. (2003) Resistance to β-lactam antibiotics and its mediation by the sensor domain of the transmembrane BlaR signaling pathway in Staphylococcus aureus, J. Biol. Chem. 278, 18419-18425.
14. Thumanu, K., Cha, J., Fisher, J. F., Perrins, R., Mobashery, S., and Wharton, C. (2006) Discrete steps in sensing of β-lactam antibiotics by the BlaR1 protein of the methicillin-resistant Staphylococcus aureus bacterium, Proc. Natl. Acad. Sci. U.S.A. 103, 10630-10635.
15. Lewis, R. A., Curnock, S. P., and Dyke, K. G. H. (1999) Proteolytic cleavage of the repressor (BlaI) of β-lactamase synthesis in Staphylococcus aureus, FEMS Microbiol. Lett. 178, 271-275.
16. Zhang, H. Z., Hackbarth, C. J., Chansky, K. M., and Chambers, H. F. (2001) A proteolytic transmembrane signaling pathway and resistance to β-lactams in staphylococci, Science 291, 1962-1965.
17. Ryffel, C., Kayser, F. H., and Bergerbachi, B. (1992) Correlation between regulation of mecA transcription and expression of methicillin resistance in staphylococci, Antimicrob. Agents Chemother. 36, 25-31.
18. Graves-Woodward, K., and Pratt, R. F. (1998) Reaction of soluble penicillin-binding protein 2a of methicillin-resistant Staphylococcus aureus with beta-lactams and acyclic substrates: kinetics in homogeneous solution, Biochem. J. 332, 755-761.
19. Zhao, G. S., Meier, T. I., Kahl, S. D., Gee, K. R., and Blaszczak, L. C. (1999) BOCILLIN FL, a sensitive and commercially available reagent for detection of penicillin-binding proteins, Antimicrob. Agents Chemother. 43, 1124-1128.
20. Butter, N. J. (1982) Carbon Dioxide Equilibria and Their Applications, Addison-Wesley, Reading, MA.
21. 2+ by the fosfomycin resistace protein (FosA), Biochemistry 40, 12712-12718.
22. Olson, S. T., and Shore, J. D. (1981) Binding of high affinity heparin to antithrombin III. Characterization of the protein fluorescence enhancement, J. Biol. Chem. 256, 11065-11072.
23. Birck, C., Cha, J. Y., Cross, J., Schulze-Briese, C., Meroueh, S. O., Schlegel, H. B., Mobashery, S., and Samama, J. P. (2004) X-ray crystal structure of the acylated β-lactam sensor domain of BlaR1 from Staphylococcus aureus and the mechanism of receptor activation for signal transduction, J. Am. Chem. Soc. 126, 13945-13947.
24. Kerff, F., Charlier, P., Colombo, M. L., Sauvage, E., Brans, A., Frere, J. M., Joris, B., and Fonze, E. (2003) Crystal structure of the sensor domain of the BlaR penicillin receptor from Bacillus licheniformis, Biochemistry 42, 12835-12843.
25. Marrero, A., Mallorqui-Fernandez, G., Guevara, T., Garcia-Castellanos, R., and Gomis-Ruth, F. X. (2006) Unbound and acylated structures of the MecR1 extracellular antibiotic-sensor domain provide insights into the signal-transduction system that triggers methicillin resistance, J. Mol. Biol. 361, 506-521.
26. Wilke, M. S., Hills, T. L., Zhang, H. Z., Chambers, H. F., and Strynadka, N. C. J. (2004) Crystal structures of the apo and penicillin-acylated forms of the BlaR1 β-lactam sensor of Staphylococcus aureus, J. Biol. Chem. 279, 47278-47287.
27. Golemi, D., Maveyraud, L., Vakulenko, S. B., Samama, J. P., and Mobashery, S. (2001) Critical involvement of a carbamylated lysine in catalytic function of class D β-lactamases, Proc. Natl. Acad. Sci. U.S.A. 98, 14280-14285.
28. Maveyraud, L., Golemi, D., Kotra, L. P., Tranier, S., Vakulenko, S. B., Mobashery, S., and Samama, J. P. (2000) Insights into class D β-lactamases are revealed by the crystal structure of the OXA-10 enzyme from Pseudomonas aeruginosa, Structure 8, 1289-1298.
29. Maveyraud, L., Golemi-Kotra, D., Ishiwata, A., Meroueh, O., Mobashery, S., and Samama, J. P. (2002) High-resolution X-ray structure of an acyl-enzyme species for the class D OXA-10 β-lactamase, J. Am. Chem. Soc. 124, 2461-2465.
30. Paetzel, M., Danel, F., de Castro, L., Mosimann, S. C., Page, M. G. P., and Strynadka, N. C. J. (2000) Crystal structure of the class D beta-lactamase OXA-10, Nat. Struct. Biol. 7, 918-925.
31. Golemi, D., Maveyraud, L., Vakulenko, S., Tranier, S., Ishiwata, A., Kotra, L. P., Samama, J. P., and Mobashery, S. (2000) The first structural and mechanistic insights for class D β-lactamases: Evidence for a novel catalytic process for turnover of β-lactam antibiotics, J. Am. Chem. Soc. 122, 6132-6133.
32. Tien, M., Berlett, B. S., Levine, R. L., Chock, P. B., and Stadtman, E. R. (1999) Peroxynitrite-mediated modification of proteins at physiological carbon dioxide concentration: pH dependence of carbonyl formation, tyrosine nitration, and methionine oxidation, Proc. Natl. Acad. Sci. U.S.A. 96, 7809-7814.
33. Duval, V., Swinnen, M., Lepage, S., Brans, A., Granier, B., Franssen, C., Frere, J. M., and Joris, B. (2003) The kinetic properties of the carboxy terminal domain of the Bacillus licheniformis 749/I BlaR penicillin-receptor shed a new light on the derepression of β-lactamase synthesis, Mol. Microbiol. 48, 1553-1564.
34. Hanique, S., Colombo, M. L., Goormaghtigh, E., Soumillion, P., Frere, J. M., and Joris, B. (2004) Evidence of an intramolecular interaction between the two domains of the BlaR1 penicillin receptor during the signal transduction, J. Biol. Chem. 279, 14264-14272.
35. Jones, R. N. (1996) Impact of changing pathogens and antimicrobial susceptibility patterns in the treatment of serious infections in hospitalized patients, Am. J. Med. 100, 3S-12S.
36. Coates, A., Hu, Y. M., Bax, R., and Page, C. (2002) The future challenges facing the development of new antimicrobial drugs, Nat. Rev. Drug Discov. 1, 895-910.
37. Fuda, C. C., Fisher, J. F., and Mobashery, S. (2005) β-lactam resistance in Staphylococcus aureus: the adaptive resistance of a plastic genome, Cell Mol. Life Sci. 62, 2617-2633.
38. Hiramatsu, K., Cui, L., Kuroda, M., and Ito, T. (2001) The emergence and evolution of methicillin-resistant Staphylococcus aureus, Trends Microbiol. 9, 486-493.
39. Sievert, D. M., Boulton, M. L., Stoltman, G., Johnson, D., Stobierski, M. G., Downes, F. P., Somsel, P. A., Rudrik, J. T., Brown, W., Hafeez, W., Lundstrom, T., Flanagan, E., Johnson, R., and Mitchell, J. (2002) Staphyloccocus aureus resistant to vancomycin - United States 2002, Morbid. Mortal. Weekly Rep. 51, 565-567.
40. Kirby, W. M. M. (1944) Extraction of a highly potent penicillin inactivator from penicillin resistant staphylococci, Science 99, 452-453.
41. Canica, M. M. M., Lu, C. Y., Krishnamoorthy, R., and Paul, G. C. (1997) Molecular diversity and evolution of bla(TEM) genes encoding β-lactamases resistant to clavulanic acid in clinical E. coli, J. Mol. Evol. 44, 57-65.
42. 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.
43. Rasmussen, B. A., and Bush, K. (1997) Carbapenem-hydrolyzing β-lactamases, Antimicrob. Agents Chemother. 41, 223-232.
44. Yang, Y. J., Bhachech, N., Bradford, P. A., Jett, B. D., Sahm, D. F., and Bush, K. (1998) Ceftazidime-resistant Klebsiella pneumoniae and Escherichia coli isolates producing TEM-10 and TEM-43 beta-lactamases from St. Louis, Missouri, Antimicrob. Agents Chemother. 42, 1671-1676.
45. Soge, O. O., Adeniyi, B. A., and Roberts, M. C. (2006) New antibiotic resistance genes associated with CTX-M plasmids from uropathogenic Nigerian Klebsiella pneumoniae, J. Antimicrob. Chemother. 58, 1048-1053.
46. Bradford, P. A., Bratu, S., Urban, C., Visalli, M., Mariano, N., Landman, D., Rahal, J. J., Brooks, S., Cebular, S., and Quale, J. (2004) Emergence of carbapenem-resistant Klebsiella species possessing the class A carbapenem-hydrolyzing KPC-2 and inhibitor-resistant TEM-30 beta-lactamases in New York City, Clin. Infect. Dis. 39, 55-60.
47. Naas, T., Bogaerts, P., Bauraing, C., Degheldre, Y., Glupczynski, Y., and Nordmanni, P. (2006) Emergence of PER and VEB extended-spectrum β-lactamases in Acinetobacter baumannii in Belgium, J. Antimicrob. Chemother. 58, 178-182.
48. Oliveira, D. C., Tomasz, A., and de Lencastre, H. (2002) Secrets of success of a human pathogen: molecular evolution of pandemic clones of meticillin-resistant Staphylococcus aureus, Lancet Infect. Dis. 2, 180-189.
49. Jevons, M. P. (1961) "Celbenin"-resistant staphylococci, Br. Med. J. 1, 124-125.