Molecular basis of antibiotic resistance and β-lactamase inhibition by mechanism-based inactivators: Perspectives and future directions

FEMS Microbiology Reviews

Volumn 24, Issue 3, 2000, Pages 251-262

  Therrien, Christian ^a   Levesque, Roger C ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

Lactam; Lactamase; Antibiotic resistance

Indexed keywords

6 (1 METHYL 1,2,3 TRIAZOL 4 YLMETHYLENE)PENEM 3 CARBOXYLIC ACID; AMOXICILLIN PLUS CLAVULANIC ACID; BETA LACTAM; BETA LACTAMASE; BETA LACTAMASE INHIBITOR; CEFEPIME; CLAVULANIC ACID; IMIPENEM; MEZLOCILLIN; PEPTIDASE; PIPERACILLIN PLUS TAZOBACTAM; SULBACTAM; SYN 1012; TAZOBACTAM; TIMENTIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; DRUG MECHANISM; DRUG STRUCTURE; DRUG TARGETING; EVOLUTION; NONHUMAN; REVIEW;

ANTI-BACTERIAL AGENTS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; BETA-LACTAMS; ENZYME INHIBITORS; GRAM-NEGATIVE BACTERIA; GRAM-NEGATIVE BACTERIAL INFECTIONS; HUMANS;

EID: 0034035284     PISSN: 01686445     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-6445(99)00039-X     Document Type: Review

References (81)

1. Amyes, S.G.B. and Gemell, C.G. (1997) Antibiotic resistance. J. Med. Microbiol. 46, 436-470.
2. Medeiros, A.A. (1997) Evolution and dissemination of β-lactamases accelerated by generations of β-lactam antibiotics. Rev. Infect. Dis. 24, S19-S45.
3. Sanders, C.C. and Sanders Jr., W.E. (1992) β-Lactam resistance in Gram-negative bacteria: global trends and clinical impact. Clin. Infect. Dis. 15, 824-839.
4. Bush, K., Jacoby, G.A. and Medeiros, A.A. (1995) A functional classification scheme for β-lactamases and its correlation with molecular structure. Antimicrob. Agents Chemother. 39, 1211-1223.
5. French, G. and Ling, T. (1988) Amoxicillin/clavulanate resistant Escherichia coli. Lancet 1, 704.
6. Martinez, J.L., Cercenado, E., Rodriguez-Creixems, M., Vincente-Perez, M.F., Delgado-Iribarren, A. and Baquero, F. (1987) Resistance to β-lactam/clavulanate. Lancet 2, 473.
7. Sanders, C.C., Iaconis, J.P., Bodey, G.P. and Samonis, G. (1988) Resistance to ticarcillin-potassium clavulanate among clinical isolates of the familly Enterobacteriaceae: role of PSE-1 β-lactamase and high levels of TEM-1 and SHV-1 and problems with false susceptibility in disk diffusion tests. Antimicrob. Agents Chemother. 32, 1365-1369.
8. Seetulsingh, P.S., Hall, L.M. and Livermore, D.M. (1991) Activity of clavulanate combinations against TEM-1 β-lactamase-producing Escherichia coli isolates obtained in 1982 and 1989. J. Antimicrob. Chemother. 27, 749-759.
9. Shannon, K., King, H., Williams, A. and Phillips, I. (1990) Hyperproduction of TEM-1 β-lactamase in clinical isolates of Escherichia coli serotype O15. FEMS Microbiol. Lett. 55, 319-323.
10. Stapleton, P., Wu, P.J., King, A., Shannon, K., French, G. and Phillips, I. (1995) Incidence and mechanisms of resistance to the combination of amoxicillin and clavulanic acid in Escherichia coli. Antimicrob. Agents Chemother. 39, 2478-2483.
11. Thomson, K.S., Weber, D.A., Sanders, C.C. and Sanders Jr., W.E. (1990) β-Lactamase production in members of the family Enterobacteriaceae and resistance to β-lactam-enzyme inhibitor combinations. Antimicrob. Agents Chemother. 34, 622-627.
12. Wu, P.J., Shannon, K. and Phillips, I. (1994) Effect of hyperproduction of TEM-1 β-lactamase on in vitro susceptibility of Escherichia coli to β-lactam antibiotics. Antimicrob. Agents. Chemother. 38, 494-498.
13. Reguera, J.A., Baquero, F., Perez-Diaz, J.C. and Martinez, J.L. (1991) Factors determining resistance to β-lactams combined with β-lactamase inhibitors in Escherichia coli. J. Antimicrob. Chemother. 27, 569-575.
14. Belaaouaj, A., Lapoumeroulie, C., Caniáa, M.M., Vedel, G., Névot, P., Krishnamoorthy, R. and Paul, G. (1994) Nucleotide sequences of the genes coding for the TEM-like β-lactamases IRT-1 and IRT-2 (formaly called TRI-1 and TRI-2). FEMS Microbiol. Lett. 120, 75-80.
15. Blazquez, J., Baquero, M.R., Canton, R., Aglos, I. and Baquero, F. (1993) Characterization of a new TEM-type β-lactamase resistant to clavulanate, sulbactam and tazobactam in a clinical isolate of Escherichia coli. Antimicrob. Agents Chemother. 37, 2059-2063.
16. Bret, L., Chaibi, E.B., Chanal-Claris, C., Sirot, D., Labia, R. and Sirot, J. (1997) Inhibitor-resistant TEM (IRT) β-lactamases with different substitutions at position 244. Antimicrob. Agents Chemother. 41, 2547-2549.
17. Brun, T., Péduzzi, J., Caniáa, M.M., Paul, G., Névot, P., Barthélémy, M. and Labia, R. (1994) Characterization and amino acid sequence of IRT-4, a novel TEM-type enzyme with a decreased susceptibility to β-lactamase inhibitors. FEMS Microbiol. Lett. 120, 111-118.
18. Caniáa, M.M., Barthélémy, M., Gilly, L., Labia, R., Krishnamoorthy, R. and Paul, G. (1997) Properties of IRT-14 (TEM-45), a newly characterized mutant of TEM-type β-lactamase. Antimicrob. Agents Chemother. 41, 374-378.
19. Henquell, C., Chanal, C., Sirot, D., Labia, R. and Sirot, J. (1995) Molecular characterization of nine different types of mutants among 107 inhibitor-resistant TEM β-lactamases from clinical isolates of Escherichia coli. Antimicrob. Agents Chemother. 39, 421-430.
20. Sirot, D., Chanal, C., Henquell, C., Labia, R., Sirot, J. and Cluzel, R. (1994) Clinical isolates of Escherichia coli producing multiple TEM mutants resistant to β-lactamase inhibitors. J. Antimicrob. Chemother. 33, 1117-1126.
21. Thomson, C.J. and Amyes, S.G.B. (1992) TRC-1: emergence of a clavulanic acid-resistant TEM β-lactamase in a clinical strain. FEMS Microbiol. Lett. 91, 113-118.
22. Vedel, G., Belaaouaj, L., Gilly, L., Labia, R., Philippon, A., Nevot, P. and Paul, G. (1992) Clinical isolates of Escherichia coli producing TRI β-lactamases: novel TEM-enzymes conferring resistance to β-lactamase inhibitors. J. Antimicrob. Chemother. 30, 449-462.
23. Zhou, X.Y., Bordon, F., Sirot, D., Kitzis, M.D. and Gutmann, L. (1994) Emergence of clinical isolates of Escherichia coli producing TEM-1 derivatives or an OXA-1 β-lactamase conferring resistance to β-lactamase inhibitors. Antimicrob. Agents Chemother. 38, 1085-1089.
24. Bret, L., Chanal, C., Sirot, D., Labia, R. and Sirot, J. (1996) Characterization of an inhibitor-resistant enzyme IRT-2 derived from TEM-2 β-lactamase produced by Proteus mirabilis strains. J. Antimicrob. Chemother. 38, 183-191.
25. Hunter, J.E., Corkill, J.E., McLennan, A.G., Fletcher, J.N. and Hart, C.A. (1993) Plasmid encoded β-lactamases resistant to inhibition by clavulanic acid produced by calf faecal coliforms. Res. Vet. Sci. 55, 367-370.
26. Lemozy, J., Chanal, C., Labia, H., Dabernat, H. and Sirot, J. (1995) First characterization of inhibitor-resistant TEM (IRT) β-lactamases in Klebsiella pneumoniae strains. Antimicrob. Agents Chemother. 33, 2580-2582.
27. Prinarakis, E.E., Miriagou, V., Tzelepi, E., Gazouli, M. and Tzoulevekis, L.S. (1998) Emergence of an inhibitor-resistant β-lactamase (SHV-10) derived from an SHV-5 variant. Antimicrob. Agents. Chemother. 41, 838-840.
28. Maiti, S.N., Philips, O.A., Micetich, R.G. and Livermore, D.M. (1998) Agents to overcome bacterial resistance. Curr. Med. Chem. 5, 441-456.
29. Matagne, A., Dubus, A., Galleni, M. and Frère, J.-M. (1999) The beta-lactamase cycle: a tale of selective pressure and bacterial ingenuity. Nat. Prod. Rep. 16, 1-19.
30. Chaibi, E.B., Sirot, D., Paul, G. and Labia, R. (1999) Inhibitor-resistant TEM β-lactamases: phenotypic, genetic and biochemical characteristics. J. Antimicrob. Chemother. 43, 447-4-58.
31. Rolinson, G.N. (1991) Evolution of β-lactamase inhibitors. Rev. Infect. Dis. 13, S727-S732.
32. Li, N., Rahil, J., Margaret, M.E. and Pratt, R.F. (1997) Structure-activity studies of the inhibition of serine β-lactamases by phosphonate monoesters. Bioorg. Med. Chem. 5, 1783-1788.
33. Martin, R. and Jones, B. (1995) Rational design and synthesis of a highly effective transition state inhibitor of the RTEM-1 β-lactamase. Tetrahedron Lett. 36, 8399-8402.
34. Lode, H.M. (1996) Clinical indications for β-lactamase inhibitors in comparison to other antibiotics. Int. J. Antimicrob. Agents 7, S3-S7.
35. Munoz, P., Garcia-Garrote, F. and Bouza, E. (1996) Broad-spectrum β-lactam antibiotics with β-lactamase inhibitors. Int. J. Antimicrob. Agents 7, S9-S14.
36. William, J.D. (1997) β-Lactamase inhibition and in vitro activity of sulbactam and sulbactam/cefoperazone. Clin. Infect. Dis. 24, 494-497.
37. Knowles, J.R. (1985) Penicillin resistance: the chemistry of β-lactamase inhibition. Acc. Chem. Res. 18, 97-104.
38. Bush, K., Macalintal, C., Rasmussen, B.A., Lee, V.J. and Yang, Y. (1993) Kinetic interactions of tazobactam with β-lactamases from all major structural classes. Antimicrob. Agents Chemother. 37, 851-858.
39. Imtiaz, U., Billings, E., Knox, J.R., Manavathu, E.K., Lerner, S.A. and Mobashery, S. (1993) Inactivation of class A β-lactamases by clavulanic acid: the role of arginine-244 in a proposed nonconcerted sequence of events. J. Am. Chem. Soc. 115, 4435-4442.
40. Imtiaz, U., Billings, E.M., Knox, J.R. and Mobashery, S. (1994) A structure-based analysis of the inhibition of class A β-lactamases by sulbactam. Biochemistry 33, 5728-5738.
41. Imtiaz, U., Manavathu, E.K., Mobashery, S. and Lerner, S.A. (1994) Reversal of clavulanate resistance conferred by Ser-244 mutant of TEM-1 β-lactamase as a result of a second mutation (Arg to Ser at position 164) that enhances activity against ceftazidime. Antimicrob. Agents Chemother. 38, 1134-1139.
42. Brenner, D.G. and Knowles, J.R. (1984) Penicillanic acid sulfone: nature of irreversible inactivation of RTEM β-lactamase from Escherichia coli. Biochemistry 23, 5833-5839.
43. Cartwright, S.J. and Coulson, A.F.W. (1979) A semi synthetic penicillinase inactivator. Nature 278, 360-361.
44. Chen, C.C.H. and Herzberg, O. (1992) Inhibition of β-lactamase by clavulanate trapped intermediates in cryocrystallographic studies. J. Mol. Biol. 224, 1103-1113.
45. Brown, R.P.A., Aplin, R.T., Frydrych, C.H. and Schofield, C.J. (1997) Mass spectrometric studies on the inhibition of TEM-2 β-lactamase by clavulanic acid derivatives. J. Antibiot. 50, 184-185.
46. Brown, R.P.A., Aplin, R.T. and Schofield, C.J. (1996) Inhibition of TEM-2 β-lactamase from Escherichia coli by clavulanic acid: observation of intermediates by electrospray ionisation mass spectrometry. Biochemistry 35, 12421-12432.
47. Herzberg, O. (1991) Refined crystal structure of β-lactamase from Staphylococcus aureus PC1 at 2.0 Å resolution. J. Mol. Biol. 217, 701-719.
48. Jelsh, C., Mourey, L., Masson, J.M. and Samama, J.P. (1993) Crystal structure of Escherichia coli TEM-1 β-lactamase at 1.8 Å resolution. Proteins Struct. Funct. Genet. 16, 364-383.
49. Moews, P.C., Knox, J.R., Didebergg, O., Charlier, P. and Frère, J.M. (1990) β-lactamase of Bacillus licheniformis 749/C at 2 Å resolution. Proteins Struct. Funct. Genet. 7, 156-171.
50. Zafaralla, G. and Mobashery, S. (1992) Facilitation of D2 D1 pyrroline tautomerization of carbapenem antibiotics by the highly conserved arginine-244 of class A β-lactamase during the course of turnover. J. Am. Chem. Soc. 114, 1505-1506.
51. Taibi, P. and Mobashery, S. (1995) Mechanism of turnover of imipenem by the TEM β-lactamase revisited. J. Am. Chem. Soc. 117, 7600-7605.
52. Maveyraud, L., Massova, I., Birck, C., Miyashita, K., Samana, J.P. and Mobashery, S. (1996) Crystal structure of 6a (hydroxymethyl)-penicillinate complexed to the TEM-1 β-lactamase from Escherichia coli: evidence on the mechanism of action of a novel inhibitor designed by a computer-aided process. J. Am. Chem. Soc. 118, 7435-7440.
53. Miyashita, K., Massova, I., Taibi, P. and Mobashery, S. (1995) Design, synthesis and evaluation of a potent mechanism-based inhibitor for the TEM β-lactamase with implications for the enzyme mechanism. J. Am. Chem. Soc. 117, 11055-11059.
54. Farmer, T.H., Page, J.W.J., Payne, D.J. and Knowles, J.C. (1994) Kinetic and physical studies of β-lactamase inhibition by a novel penem BRL 42715. Biochem. J. 303, 825-830.
55. Farzaneh, S., Chaibi, E.B., Peduzzi, J., Barthelemy, M., Labia, R., Blazquez, J. and Baquero, F. (1996) Implication of Ile-69 and Thr-182 residues in kinetic characteristics of IRT-3 (TEM-32) β-lactamase. Antimicrob. Agents Chemother. 40, 2434-2436.
56. Satake, S. and Nakae, T. (1995) Outer membrane permeability of β-lactamase inhibitors in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 129, 251-254.
57. Pratt, R.F. (1992) β-Lactamase: inhibition. In: The Chemistry of β-Lactams. (Page, M.I., Ed.), pp. 229-271. Blackie Academic and Professional, London.
58. Taibi-Tronche, P., Massova, I., Vakulenko, S.B., Lerner, S.A. and Mobashery, S. (1996) Evidence for structural elasticity of class A β-lactamases in the course of catalytic turnover of the novel cephalosporin cefepime. J. Am. Chem. Soc. 118, 7441-7448.
59. Du Bois, S.K., Marriott, M.S. and Amyes, S.G.B. (1995) TEM- and SHV-derived β-lactamases: relationship between selection, structure and function. J. Antimicrob. Chemother. 35, 7-22.
60. Knox, J.R. (1995) Extended-spectrum and inhibitor-resistant TEM-type β-lactamases: mutation, specificity, and three-dimensional structure. Antimicrob. Agents Chemother. 39, 2593-2601.
61. Bonomo, R.A., Dawes, C.G., Knox, J.R. and Shlaes, D.M. (1995) Complementary roles of mutations at position 69 and 242 in a class A β-lactamase. Biochim. Biophys. Acta 124, 113-120.
62. Chaibi, E.B., Péduzzi, J., Farzaneh, S., Barthélémy, M., Sirot, D. and Labia, R. (1998) Clinical inhibitor-resistant mutants of the β-lactamase TEM-1 at amino-acid position 69: kinetic analysis and molecular modeling. Biochim. Biophys. Acta 1382, 38-46.
63. Delaire, M., Labia, R., Samama, J.P. and Masson, J.M. (1992) Site-directed mutagenesis at the active site of Escherichia coli TEM-1 β-lactamase. J. Biol. Chem. 267, 20600-20606.
64. Saves, I., Burlet-Schiltz, O., Swaren, P., Lefèvre, F., Masson, J.M., Promé, J.C. and Samama, J.P. (1995) The asparagine to aspartic acid substitution at position 276 of TEM-35 and TEM-36 is involved in the β-lactamase resistance to clavulanic acid. J. Biol. Chem. 270, 18240-18245.
65. Henquell, C., Sirot, D., Chanal, C., De Champs, C., Chatron, P., Lafeuille, B., Texier, P., Sirot, J. and Cluzel, J. (1994) Frequency of inhibitor-resistant TEM β-lactamases in Escherichia coli isolates from urinary track infections in France. J. Antimicrob. Chemother. 34, 707-714.
66. Goussard, S. and Courvalin, P. (1999) Updated sequence information for TEM β-lactamase genes. Antimicrob. Agents Chemother. 43, 367-370.
67. Massova, I. and Mobashery, S. (1998) Kinship and diversification of bacterial penicillin-binding proteins and β-lactamases. Antimicrob. Agents Chemother. 42, 1-17.
68. Goffin, C. and Ghuysen, J.-M. (1999) Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 62, 1079-1093.
69. Chen, H.Y., Yuan, M. and Livermore, D.M. (1995) Mechanisms of resistance to β-lactam antibiotics amongst Pseudomonas aeruginosa isolates collected in the U.K. in 1993. J. Med. Microbiol. 43, 300-309.
70. imp among the clinically isolated strains of Serratia marcescens. Antimicrob. Agents Chemother. 39, 824-829.
71. MOX-1 gene encoding AmpC-type β-lactamase. Gene 139, 93-98.
72. Bradford, P.A., Urban, C., Mariano, N., Projan, S.J., Rahal, J. and Bush, K. (1997) Imipenem resistance in Klebsiella pneumoniae is associated with the combination of ACT-1, a plasmid-mediated AmpC β-lactamase, and the loss of an outer-membrane protein. Antimicrob. Agents Chemother. 41, 563-569.
73. Gazouli, M., Tzouvelekis, L.S., Vatopoulos, A.C. and Tzelepi, E. (1998) Transferable class C β-lactamases in Escherichia coli strains isolated in Greek hospitals and characterization of two enzyme variants (LAT-3 and LAT-4) closely related to Citrobacter freundii AmpC β-lactamases. J. Antimicrob. Chemother. 42, 419-425.
74. Panagiota, G., Tzelepi, E., Legakis, N.J. and Tzouvelekis, L. (1999) Aspartic acid for asparagine substitutions at positions 276 reduces susceptibility to mechanism-based inhibitors in SHV-1 and SHV-5 β-lactamases. J. Antimicrobial. Chemother. 43, 23-29.
75. Rasmussen, B. and Bush, K. (1997) Carbapenem-hydrolyzing β-lactamases. Antimicrob. Agents Chemother. 41, 223-232.
76. Payne, D.J., Bateson, J.H., Gasson, B.C., Proctor, D., Khushi, T., Farmer, T.H., Tolson, T.H., Bell, D., Skett, P.W., Marshall, A.C., Reid, R., Ghosez, L., Combret, Y. and Marchand-Brynaert, J. (1997) Inhibition of metallo-β-lactamase by a series of mercaptoacetic acid thiol ester derivatives. Antimicrob. Agents Chemother. 41, 135-140.
77. Strynadka, N., Jensen, S., Johns, K., Blanchard, H., Page, M., Matagne, A., Frère, J.-M. and James, M.N.G. (1994) Structural and kinetic characterization of a β-lactamase-inhibitor protein. Nature 368, 657-660.
78. Strynadka, N.C., Jensen, S.E., Alzari, P.M. and James, M.N.G. (1996) A potent new mode of β-lactamase inhibition revealed by the TEM-1/BLIP complex at 1.7 A resolution. Nat. Struct. Biol. 3, 290-297.
79. Rudgers, G.W. and Palzkill, T. (1999) Identification of residues in β-lactamase critical for binding β-lactamase inhibitory protein. J. Biol. Chem. 274, 6963-6971.
80. Albeck, S. and Schreiber, G. (1999) Biophysical characterization of the interaction of the β-lactamase TEM-1 with its protein inhibitor. Biochemistry 38, 11-21.
81. Erdmann, J. (1999) Bacteria resistant to drugs draw scrutiny of biofirms. Gen. Eng. News 19, 1-3.