Crystal structure and activity studies of the Mycobacterium tuberculosis β-lactamase reveal its critical role in resistance to β-lactam antibiotics

Antimicrobial Agents and Chemotherapy

Volumn 50, Issue 8, 2006, Pages 2762-2771

  Wang, Feng ^a   Cassidy, Craig ^b   Sacchettini, James C ^a,b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMINO ACID; AMPICILLIN; ARGININE; ASPARAGINE; BACTERIAL ENZYME; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE; CARBAPENEM DERIVATIVE; CEFALOTIN; CEFALOTINASE; CEFOXITIN; CEFTAZIDIME; CEPHALOSPORIN DERIVATIVE; CLAVULANIC ACID; GLUTAMIC ACID; MEROPENEM; PENICILLIN DERIVATIVE; PENICILLINASE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL CHROMOSOME; BACTERIUM CULTURE; BLAC GENE; CRYSTAL STRUCTURE; CRYSTALLIZATION; CULTURE MEDIUM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; ENZYME SYNTHESIS; GENE DELETION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; BETA-LACTAMS; BINDING SITES; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; GENES, BACTERIAL; HYDROGEN BONDING; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM TUBERCULOSIS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, PROTEIN; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

EID: 33746878510     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.00320-06     Document Type: Article

References (59)

1. Abate, G., and H. Miorner. 1998. Susceptibility of multidrug-resistant strains of Mycobacterium tuberculosis to amoxycillin (sic) in combination with clavulanic acid and ethambutol. J. Antimicrob. Chemother. 42:735-740.
2. Ambler, R. P., A. F. Coulson, J. M. Frere, J. M. Ghuysen, B. Joris, M. Foreman, R. C. Levesque, G. Tiraby, and S. G. Waley. 1991. A standard numbering scheme for the class A beta-lactamases. Biochem. J. 276:269-270.
3. Anonymous. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D 50:760-763.
4. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: Signal? 3.0. J. Mol. Biol. 340:783-795.
5. Bentley, R. 2005. The development of penicillin: genesis of a famous antibiotic. Perspect. Biol. Med. 48:444-452.
6. Bush, K., G. A. Jacoby, and A. A. Medeiros. 1995. A functional classification scheme for beta-lactamases and its correlation with molecular structure. Antimicrob. Agents Chemother. 39:1211-1233.
7. Chambers, H. F., D. Moreau, D. Yajko, C. Miick, C. Wagner, C. Hackbarth, S. Kocagoz, E. Rosenberg, W. K. Hadley, and H. Nikaido. 1995. Can. penicillins and other beta-lactam antibiotics be used to treat tuberculosis? Antimicrob. Agents Chemother. 39:2620-2624.
8. Christopher, J. A. 1998. SPOCK: the Structural Properties Observation and Calculation Kit. Program manual. Center for Macromolecular Design, Texas A&M University, College Station, TX.
9. Davies, J. 1994. Inactivation of antibiotics and the dissemination of resistance genes. Science 264:375-382.
10. Dideberg, O., P. Charlier, J. P. Wery, P. Dehottay, J. Dusart, T. Erpicum, J. M. Frere, and J. M. Ghuysen. 1987. The crystal structure of the beta-lactamase of Streptomyces albus G at 0.3 nm resolution. Biochem. J. 245:911-913.
11. Dincer, I., A. Ergin, and T. Kocagoz, 2004. The in vitro efficacy of beta-lactam and beta-lactamase inhibitors against multidrug resistant clinical strains of Mycobacterium tuberculosis. Int. J. Antimicrob. Agents 23:408-411.
12. Edwards, J. R., and M. J. Betts. 2000. Carbapenems: the pinnacle of the beta-lactam antibiotics or room for improvement? J. Antimicrob. Chemother. 45:1-4.
13. Fisher, J. F., S. O. Meroueh, and S. Mobashery, 2005. Bacterial resistance to beta-lactam antibiotics: compelling opportunism, compelling opportunity. Chem. Rev. 105:395-424.
14. Flores, A. R., L. M. Parsons, and M. S. Pavelka, Jr. 2005. Characterization of novel Mycobacterium tuberculosis and Mycobacterium smegmatis mutants hypersusceptible to beta-lactam antibiotics. J. Bacteriol. 187:1892-1900.
15. Flores, A. R., L. M. Parsons, and M. S. Pavelka, Jr. 2005. Genetic analysis of the beta-lactamases of Mycobacterium tuberculosis and Mycobacterium smegmatis and susceptibility to beta-lactam antibiotics. Microbiology 151:521-532.
16. Fonze, E., M. Vanhove, G. Dive, E. Sauvage, J. M. Frere, and P, Charlier. 2002. Crystal structures of the Bacillus licheniformis BS3 class A beta-lactamase and of the acyl-enzyme adduct formed with cefoxitin. Biochemistry 41:1877-1885.
17. Frere, J. M. 1995. Beta-lactamases and bacterial resistance to antibiotics. Mol. Microbiol. 16:385-395.
18. Gattiker, A., E. Gasteiger, and A. Bairoch. 2002. ScanProsite: a reference implementation of a PROSITE scanning tool. Appl. Bioinformatics 1:107-108.
19. Guex, N, and M. C. Peitsch. 1997. SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modeling. Electrophoresis 18:2714-2723.
20. Hall, A., and J. R. Knowles. 1976. Directed selective pressure on a beta-lactamase to analyse molecular changes involved in development of enzyme function. Nature 264:803-804.
21. Herzberg, O., and J. Moult. 1987. Bacterial resistance to beta-lactam antibiotics: crystal structure of beta-lactamase from Staphylococcus aureus PC1 at 2.5 Å resolution. Science 236:694-701.
22. Holm, L., and C. Sander. 1995. Dali: a network tool for protein structure comparison. Trends Biochem. Sci. 20:478-480.
23. Ibuka, A., A. Taguchi, M. Ishiguro, S. Fushinobu, Y. Ishii, S. Kamitori, K. Okuyama, K. Yamaguchi, M. Konno, and H. Matsuzawa. 1999. Crystal structure of the E166A mutant of extended-spectrum beta-lactamase Toho-1 at 1.8 Å resolution. J. Mol. Biol. 285:2079-2087.
24. Ibuka, A. S., Y. Ishii, M. Galleni, M. Ishiguro, K. Yamaguchi, J. M. Frere, H. Matsuzawa, and H. Sakai. 2003. Crystal structure of extended-spectrum beta-lactamase Toho-1: insights into the molecular mechanism for catalytic reaction and substrate specificity expansion. Biochemistry 42:10634-10643.
25. Iland, C. N. 1946. The effect of penicillin on the tubercle bacillus: tubercle penicillinase. J. Pathol. Bacteriol. 58:495-500.
26. Imtiaz, U., E. Billings, J. R. Knox, E. K. Manavathu, S. A. Lerner, and S. Mobashery. 1993. Inactivation of class A beta-lactamases by clavulanic acid: the role of arginine-244 in a proposed nonconcerted sequence of events. J. Am. Chem. Soc. 115:4435-4442.
27. Imtiaz, U., E. K. Manavathu, S. A. Lerner, and S. Mobashery. 1993. Critical hydrogen bonding by serine 235 for cephalosporinase activity of TEM-1 beta-lactamase. Antimicrob. Agents Chemother. 37:2438-2442.
28. Jacob, F., B. Joris, S. Lepage, J. Dusart, and J. M. Frere. 1990. Role of the conserved amino acids of the 'SDN' loop (Ser130, Asp131 and Asn132) in a class A beta-lactamase studied by site-directed mutagenesis. Biochem. J. 271:399-406.
29. Jarlier, V., L. Gutmann, and H. Nikaido. 1991. Interplay of cell wall barrier and beta-lactamase activity determines high resistance to beta-lactam antibiotics in Mycobacterium chelonae. Antimicrob. Agents Chemother. 35:1937-1939.
30. Kuzin, A. P., M. Nukaga, Y. Nukaga, A. Hujer, R. A. Bonomo, and J. R. Knox. 2001. Inhibition of the SHV-1 beta-lactamase by sulfones: crystallographic observation of two reaction intermediates with tazobactam. Biochemistry 40:1861-1866.
31. Lim, D., F. Sanschagrin, L. Passmore, L. De Castro, R. C. Levesque, and N. C. Strynadka. 2001. Insights into the molecular basis for the carbenicillinase activity of PSE-4 beta-lactamase from crystallographic and kinetic studies. Biochemistry 40:395-402.
32. Maveyraud, L., L. Mourey, L. P. Kotra, J. Pedelacq, V. Guillet, S. Mobashery, and J. Samama. 1998. Structure basis for clinical longevity of carbapenem antibiotics in the face of challenge by the common class A beta-lactamases from the antibiotic-resistant bacteria. J. Am. Chem. Soc. 120:9748-9752.
33. McPherson, A. 1982. Preparation and analysis of protein crystals. Waverly, Baltimore, Md.
34. McRee, D. E. 1999. XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125:156-165.
35. Medeiros, A. A. 1997. Evolution and dissemination of beta-lactamases accelerated by generations of beta-lactam antibiotics. Clin. Infect. Dis. 24(Suppl. 1): S19-S45.
36. Meroueh, S. O., J. F. Fisher, H. B. Schlegel, and S. Mobashery. 2005. Ab initio QM/MM study of class A beta-lactamase acylation: dual participation of Glu166 and Lys73 in a concerted base promotion of Ser70. J. Am. Chem. Soc. 127:15397-15407.
37. Minasov, G., X. Wang, and B. K. Shoichet. 2002. An ultrahigh resolution structure of TEM-1 beta-lactamase suggests a role for Glu166 as the general base in acylation. J. Am. Chem. Soc. 124:5333-5340.
38. Mourey, L., K. Miyashita, P. Swaren, A. Bulychev, J. Samama, and S. Mobashery. 1998. Inhibition of the NMC-A beta-lactamase by a penicillanic acid derivative and the structural bases for the increase in substrate profile of this antibiotic resistance enzyme. J. Am. Chem. Soc. 120:9382-9383.
39. Nielsen, J. B., and J. O. Lampen. 1982. Glyceride-cysteine lipoproteins and secretion by gram-positive bacteria. J. Bacteriol. 152:315-322.
40. Nukaga, M., K. Mayama, G. V. Crichlow, and J. R. Knox. 2002. Structure of an extended-spectrum class A beta-lactamase from Proteus vulgaris K1. J. Mol. Biol. 317:109-117.
41. Nukaga, M., K. Mayama, A. M. Hujer, R. A. Bonomo, and J. R. Knox. 2003. Ultrahigh resolution structure of a class A beta-lactamase: on the mechanism and specificity of the extended-spectrum SHV-2 enzyme. J. Mol. Biol. 328:289-301.
42. Otwinowski, Z., and W. Minor. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
43. Padayatti, P. S., M. S. Helfand, M. A. Totir, M. P. Carey, A. M. Hujer, P. R. Carey, R. A. Bonomo, and F. van den Akker. 2004. Tazobactam forms a stoichiometric trans-enamine intermediate in the E166A variant of SHV-1 beta-lactamase: 1.63 Å crystal structure. Biochemistry 43:843-848.
44. Perez-Llarena, F., J. F. Martin, M. Galleni, J. J. Coque, J. L. Fuente, J. M. Frere, and P. Liras. 1997. The bla gene of the cephamycin cluster of Streptomyces clavuligerus encodes a class A beta-lactamase of low enzymatic activity. J. Bacteriol. 179:6035-6040.
45. Quinting, B., J. M. Reyrat, D. Monnaie, G. Amicosante, V. Pelicic, B. Gicquel, J. M. Frere, and M. Galleni. 1997. Contribution of beta-lactamase production to the resistance of mycobacteria to beta-lactam antibiotics. FEBS Lett. 406:275-278.
46. Segura, C., M. Salvado, I. Collado, J. Chaves, and A. Coira. 1998. Contribution of beta-lactamases to beta-lactam susceptibilities of susceptible and multidrug-resistant Mycobacterium tuberculosis clinical isolates. Antimicrob. Agents Chemother. 42:1524-1526.
47. Shimamura, T., A. Ibuka, S. Fushinobu, T. Wakagi, M. Ishiguro, Y. Ishii, and H. Matsuzawa. 2002. Acyl-intermediate structures of the extended-spectrum class A beta-lactamase, Toho-1, in complex with cefotaxime, cephalothin, and benzylpenicillin. J. Biol. Chem. 277:46601-46608.
48. Sorg, T. B., and M. H. Cynamon. 1987. Comparison of four beta-lactamase inhibitors in combination with ampicillin against Mycobacterium tuberculosis. J. Antimicrob. Chemother. 19:59-64.
49. Strynadka, N. C., H. Adachi, S. E. Jensen, K. Johns, A. Sielecki, C. Betzel, K. Sutoh, and M. N. James. 1992. Molecular structure of the acyl-enzyme intermediate in beta-lactam hydrolysis at 1.7 Å resolution. Nature 359:700-705.
50. Sutcliffe, I. C., and R. R. Russell. 1995. Lipoproteins of gram-positive bacteria. J. Bacteriol. 177:1123-1128.
51. Swaren, P., L. Maveyraud, X. Raquet, S. Cabantous, C. Duez, J. D. Pedelacq, S. Mariotte-Boyer, L. Mourey, R. Labia, M. H. Nicolas-Chanoine, P. Nordmann, J. M. Frere, and J. P. Samama. 1998. X-ray analysis of the NMC-A beta-lactamase at 1.64-̊ resolution, a class A carbapenemase with broad substrate specificity. J. Biol. Chem. 273:26714-26721.
52. Therrien, C., and R. C. Levesque. 2000. Molecular basis of antibiotic resistance and beta-lactamase inhibition by mechanism-based inactivators: perspectives and future directions. FEMS Microbiol. Rev. 24:251-262.
53. Trias, J., V. Jarlier, and R. Benz. 1992. Porins in the cell wall of mycobacteria. Science 258:1479-1481.
54. Vakulenko, S. B., P. Taibi-Tronche, M. Toth, I. Massova, S. A. Lerner, and S. Mobashery. 1999. Effects on substrate profile by mutational substitutions at positions 164 and 179 of the class A TEM(pUC19) beta-lactamase from Escherichia coli. J. Biol. Chem. 274:23052-23060.
55. Voladri, R. K., D. L. Lakey, S. H. Hennigan, B. E. Menzies, K. M. Edwards, and D. S. Kernodle. 1998. Recombinant expression and characterization of the major beta-lactamase of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 42:1375-1381.
56. Wong, C. S., G. S. Palmer, and M. H. Cynamon. 1988. In-vitro susceptibility of Mycobacterium tuberculosis, Mycobacterium bovis and Mycobacterium kansasii to amoxycillin (sic) and ticarcillin in combination with clavulanic acid. J. Antimicrob. Chemother. 22:863-866.
57. Wong, J. T. 1985. Kinetics of enzyme mechanisms. Academic Press, New York, N.Y.
58. Yang, Y., B. A. Rasmussen, and D. M. Shlaes. 1999. Class A beta-lactamases-enzyme-inhibitor interactions and resistance. Pharmacol. Ther. 83:141-151.
59. Zhang, Y., V. A. Steingrube, and R. J. Wallace, Jr. 1992. Beta-lactamase inhibitors and the inducibility of the beta-lactamase of Mycobacterium tuberculosis. Am. Rev. Respir. Dis. 145:657-660.