Evolution of metallo-β-lactamases: Trends revealed by natural diversity and in vitro evolution

Antibiotics

Volumn 3, Issue 3, 2014, Pages 285-316

  Meini, María Rocío ^a   Llarrull, Leticia I ^a   Vila, Alejandro J ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

Evolution; Metallo lactamases; Resistance

Indexed keywords

AMPICILLIN; BETA LACTAM ANTIBIOTIC; CARBAPENEM; CEFALORIDINE; CEFALOTIN; CEFOTAXIME; CEFOXITIN; CEFTAZIDIME; CEPHALOSPORIN; DORIPENEM; HYDROXYACYLGLUTATHIONE HYDROLASE; IMIPENEM; LACTOYLGLUTATHIONE LYASE; MACROLIDE; MEROPENEM; METALLO BETA LACTAMASE; PENICILLIN BINDING PROTEIN; PENICILLIN DERIVATIVE; PENICILLIN G; RIFAMPICIN; SULFAMETHOXAZOLE;

ANTIBIOTIC RESISTANCE; BACTERIAL INFECTION; BIODIVERSITY; CATALYSIS; CELL MEMBRANE; CHEMICAL ANALYSIS; CHEMICAL INTERACTION; CRYSTAL STRUCTURE; DNA LIBRARY; DRUG DESIGN; EVALUATION STUDY; EVOLUTION; FLUORINE NUCLEAR MAGNETIC RESONANCE; FOOD AND DRUG ADMINISTRATION; GENE MUTATION; GENETIC VARIABILITY; HYDROGEN BOND; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVIEW; STATIC ELECTRICITY;

EID: 84935850844     PISSN: None     EISSN: 20796382     Source Type: Journal    
DOI: 10.3390/antibiotics3030285     Document Type: Review

References (110)

1. Fisher, J.F.; Meroueh, S.O.; Mobashery, S. Bacterial resistance to beta-lactam antibiotics: Compelling opportunism, compelling opportunity. Chem. Rev. 2005, 105, 395-424.
2. Llarrull, L.I.; Testero, S.A.; Fisher, J.F.; Mobashery, S. The future of the β-lactams. Curr. Opin. Microbiol. 2010, 13, 551-557.
3. Bebrone, C. Metallo-beta-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily. Biochem. Pharmacol. 2007, 74, 1686-1701.
4. Paterson, D.L.; Bonomo, R.A. Extended-spectrum beta-lactamases: A clinical update. Clin. Microbiol. Rev. 2005, 18, 657-686.
5. Nordmann, P.; Naas, T.; Poirel, L. Global Spread of Carbapenemase-producing Enterobacteriaceae. Emerg. Infect. Dis. 2011, 17, 1791-1798.
6. Crowder, M.W.; Spencer, J.; Vila, A.J. Metallo-beta-lactamases: Novel weaponry for antibiotic resistance in bacteria. Acc. Chem. Res. 2006, 39, 721-728.
7. Llarrull, L.I.; Tioni, M.F.; Vila, A.J. Metal content and localization during turnover in B. cereus metallo-beta-lactamase. J. Am. Chem. Soc. 2008, 130, 15842-15851.
8. Tioni, M.F.; Llarrull, L.I.; Poeylaut-Palena, A.A.; Martí, M.A.; Saggu, M.; Periyannan, G.R.; Mata, E.G.; Bennett, B.; Murgida, D.H.; Vila, A.J. Trapping and characterization of a reaction intermediate in carbapenem hydrolysis by B. cereus metallo-beta-lactamase. J. Am. Chem. Soc. 2008, 130, 15852-15863.
9. Lim, H.M.; Pène, J.J.; Shaw, R.W. Cloning, nucleotide sequence, and expression of the Bacillus cereus 5/B/6 beta-lactamase II structural gene. J. Bacteriol. 1988, 170, 2873-2878.
10. Bellais, S.; Aubert, D.; Naas, T.; Nordmann, P. Molecular and biochemical heterogeneity of class B carbapenem-hydrolyzing beta-lactamases in Chryseobacterium meningosepticum. Antimicrob. Agents Chemother. 2000, 44, 1878-1886.
11. Walsh, T.R.; Hall, L.; Assinder, S.J.; Nichols, W.W.; Cartwright, S.J.; MacGowan, A.P.; Bennett, P.M. Sequence analysis of the L1 metallo-beta-lactamase from Xanthomonas maltophilia. Biochim. Biophys. Acta 1994, 1218, 199-201.
12. Lauretti, L.; Riccio, M.L.; Mazzariol, A.; Cornaglia, G.; Amicosante, G.; Fontana, R.; Rossolini, G.M. Cloning and characterization of blaVIM, a new integron-borne metallo-beta-lactamase gene from a Pseudomonas aeruginosa clinical isolate. Antimicrob. Agents Chemother. 1999, 43, 1584-1590.
13. Laraki, N.; Franceschini, N.; Rossolini, G.M.; Santucci, P.; Meunier, C.; de Pauw, E.; Amicosante, G.; Frere, J.M.; Galleni, M. Biochemical characterization of the Pseudomonas aeruginosa 101/1477 metallo-β-lactamase IMP-1 produced by Escherichia coli. Antimicrob. Agents Chemother. 1999, 43, 902-906.
14. Yong, D.; Toleman, M.A.; Giske, C.G.; Cho, H.S.; Sundman, K.; Lee, K.; Walsh, T.R. Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob. Agents Chemother. 2009, 53, 5046-5054.
15. King, D.T.; Strynadka, N.C.J. Targeting metallo-β-lactamase enzymes in antibiotic resistance. Future Med. Chem. 2013, 5, 1243-1263.
16. Poeylaut-Palena, A.A.; Tomatis, P.E.; Karsisiotis, A.I.; Damblon, C.; Mata, E.G.; Vila, A.J. A minimalistic approach to identify substrate binding features in B1 metallo-beta-lactamases. Bioorg. Med. Chem. Lett. 2007, 17, 5171-5174.
17. Charan, J.; Mulla, S.; Ryavanki, S.; Kantharia, N. New Delhi Metallo-beta lactamase-1 containing enterobacteriaceae: Origin, diagnosis, treatment and public health concern. Pan Afr. Med. J. 2012, 11, e22.
18. McKenna, M. Antibiotic resistance: The last resort. Nature 2013, 499, 394-396.
19. Smith, R.; Coast, J. The true cost of antimicrobial resistance. Br. Med. J. 2013, 346, f1493.
20. Walsh, C. Molecular mechanisms that confer antibacterial drug resistance. Nature 2000, 406, 775-781.
21. β-Lactamase classification and amino acid sequences for TEM, SHV and OXA extended-spectrum and inhibitor resistant enzymes. Available online: http://www.lahey.org/Studies/ (accessed on 9 April 2014).
22. Bush, K.; Jacoby, G.A. Updated functional classification of beta-lactamases. Antimicrob. Agents Chemother. 2010, 54, 969-976.
23. Orencia, M.C.; Yoon, J.S.; Ness, J.E.; Stemmer, W.P.; Stevens, R.C. Predicting the emergence of antibiotic resistance by directed evolution and structural analysis. Nat. Struct. Biol. 2001, 8, 238-242.
24. Stemmer, W.P. Rapid evolution of a protein in vitro by DNA shuffling. Nature 1994, 370, 389-391.
25. Zaccolo, M.; Gherardi, E. The effect of high-frequency random mutagenesis on in vitro protein evolution: A study on TEM-1 beta-lactamase. J. Mol. Biol. 1999, 285, 775-783.
26. Salverda, M.L.M.; De Visser, J.A.; Barlow, M. Natural evolution of TEM-1 β-lactamase: Experimental reconstruction and clinical relevance. FEMS Microbiol. Rev. 2010, 34, 1015-1036.
27. Iyobe, S.; Kusadokoro, H.; Ozaki, J.; Matsumura, N.; Minami, S.; Haruta, S.; Sawai, T.; O'Hara, K. Amino acid substitutions in a variant of IMP-1 metallo-beta-lactamase. Antimicrob. Agents Chemother. 2000, 44, 2023-2027.
28. Tomatis, P.E.; Rasia, R.M.; Segovia, L.; Vila, A.J. Mimicking natural evolution in metallo-beta-lactamases through second-shell ligand mutations. Proc. Natl. Acad. Sci. USA 2005, 102, 13761-13766.
29. Tomatis, P.E.; Fabiane, S.M.; Simona, F.; Carloni, P.; Sutton, B.J.; Vila, A.J. Adaptive protein evolution grants organismal fitness by improving catalysis and flexibility. Proc. Natl. Acad. Sci. USA 2008, 105, 20605-20610.
30. Yano, H.; Kuga, A.; Okamoto, R; Kitasato, H.; Kobayashi, T.; Inoue, M. Plasmid-encoded metallo-beta-lactamase (IMP-6) conferring resistance to carbapenems, especially meropenem. Antimicrob. Agents Chemother. 2001, 45, 1343-1348.
31. Morán-Barrio, J.; Limansky, A.S.; Viale, A.M. Secretion of GOB metallo-beta-lactamase in Escherichia coli depends strictly on the cooperation between the cytoplasmic DnaK chaperone system and the Sec machinery: Completion of folding and Zn(II) ion acquisition occur in the bacterial periplasm. Antimicrob. Agents Chemother. 2009, 53, 2908-2917.
32. González, J.M.; Meini, M.-R.; Tomatis, P.E.; Medrano Martín, F.J.; Cricco, J.A.; Vila, A.J. Metallo-β-lactamases withstand low Zn(II) conditions by tuning metal-ligand interactions. Nat. Chem. Biol. 2012, 8, 698-700.
33. Meini, M.-R.; González, L.J.; Vila, A.J. Antibiotic resistance in Zn(II)-deficient environments: Metallo-β-lactamase activation in the periplasm. Future Microbiol. 2013, 8, 947-979.
34. Oelschlaeger, P. Outsmarting metallo-beta-lactamases by mimicking their natural evolution. J. Inorg Biochem. 2008, 102, 2043-2051.
35. Pal, A.; Tripathi, A. An in silico approach for understanding the molecular evolution of clinically important metallo-beta-lactamases. Infect. Genet. Evol. 2013, 20, 39-47.
36. Widmann, M.; Pleiss, J.; Oelschlaeger, P. Systematic analysis of metallo-β-lactamases using an automated database. Antimicrob. Agents Chemother. 2012, 56, 3481-3491.
37. Ho, P.L.; Ho, A.Y.; Chow, K.H.; Lai, E.L.; Ching, P.; Seto, W.H. Epidemiology and clonality of multidrug-resistant Acinetobacter baumannii from a healthcare region in Hong Kong. J. Hosp. Infect. 2010, 74, 358-364.
38. Hocquet, D.; Plesiat, P.; Dehecq, B.; Mariotte, P.; Talon, D.; Bertrand, X. Nationwide investigation of extended-spectrum β-lactamases, metallo-β-lactamases, and extended-spectrum oxacillinases produced by ceftazidime-resistant Pseudomonas aeruginosa strains in France. Antimicrob. Agents Chemother. 2010, 54, 3512-3515.
39. Galleni, M.; Lamotte-Brasseur, J.; Rossolini, G.M.; Spencer, J.; Dideberg, O.; Frère, J.M.; Metallo-beta-lactamases Working Group Standard numbering scheme for class B beta-lactamases. Antimicrob. Agents Chemother. 2001, 45, 660-663.
40. Garau, G.; García-Sáez, I.; Bebrone, C; Anne, C; Mercuri, P.; Galleni, M.; Frère, J.-M.; Dideberg, O. Update of the Standard Numbering Scheme for Class B β-Lactamases. Antimicrob. Agents Chemother. 2004, 48, 2347-2349.
41. Daiyasu, H.; Osaka, K.; Ishino, Y.; Toh, H. Expansion of the zinc metallo-hydrolase family of the beta-lactamase fold. FEBS Lett. 2001, 503, 1-6.
42. De Seny, D.; Prosperi-Meys, C; Bebrone, C; Rossolini, G.M.; Page, M.I.; Noel, P.; Frère, J.-M.; Galleni, M. Mutational analysis of the two zinc-binding sites of the Bacillus cereus 569/H/9 metallo-beta-lactamase. Biochem. J. 2002, 363, 687-696.
43. Abriata, L.A.; González, L.J.; Llarrull, L.I.; Tomatis, P.E.; Myers, W.K.; Costello, A.L.; Tierney, D.L.; Vila, A.J. Engineered mononuclear variants in Bacillus cereus metallo-beta-lactamase BcII are inactive. Biochemistry 2008, 47, 8590-8599.
44. Materon, I.C.; Palzkill, T. Identification of residues critical for metallo-beta-lactamase function by codon randomization and selection. Protein Sci. 2001, 10, 2556-2565.
45. Fabiane, S.M.; Sohi, M.K.; Wan, T.; Payne, D.J.; Bateson, J.H.; Mitchell, T.; Sutton, B.J. Crystal structure of the zinc-dependent beta-lactamase from Bacillus cereus at 1.9 A resolution: Binuclear active site with features of a mononuclear enzyme. Biochemistry 1998, 37, 12404-12411.
46. Garcia-Saez, I.; Docquier, J.-D.; Rossolini, G.M.; Dideberg, O. The three-dimensional structure of VIM-2, a Zn-beta-lactamase from Pseudomonas aeruginosa in its reduced and oxidised form. J. Mol. Biol. 2008, 375, 604-611.
47. Concha, N.O.; Janson, C.A.; Rowling, P.; Pearson, S.; Cheever, C.A.; Clarke, B.P.; Lewis, C; Galleni, M.; Frère, J.M.; Payne, D.J. et al. Crystal structure of the IMP-1 metallo beta-lactamase from Pseudomonas aeruginosa and its complex with a mercaptocarboxylate inhibitor: Binding determinants of a potent, broad-spectrum inhibitor. Biochemistry 2000, 39, 4288-4298.
48. Docquier, J.-D.; Benvenuti, M.; Calderone, V.; Stoczko, M.; Menciassi, N.; Rossolini, G.M.; Mangani, S. High-resolution crystal structure of the subclass B3 metallo-beta-lactamase BJP-1: Rational basis for substrate specificity and interaction with sulfonamides. Antimicrob. Agents Chemother. 2010, 54, 4343-4351.
49. Bebrone, C; Delbrück, H.; Kupper, M.B.; Schlömer, P.; Willmann, C; Frère, J.-M.; Fischer, R.; Galleni, M.; Hoffmann, K.M.V. The Structure of the dizinc subclass B2 metallo-β-lactamase CphA reveals that the second inhibitory zinc ion binds in the histidine site. Antimicrob. Agents Chemother. 2009, 53, 4464-4471.
50. Oelschlaeger, P.; Schmid, R.D.; Pleiss, J. Insight into the mechanism of the IMP-1 metallo-beta-lactamase by molecular dynamics simulations. Protein Eng 2003, 16, 341-350.
51. Valdez, C.E.; Sparta, M.; Alexandrova, A.N. The role of the flexible L43-S54 protein loop in the CcrA metallo-β-lactamase in binding structurally dissimilar β-lactam antibiotics. J. Chem. Theory Comput. 2013, 9, 730-737.
52. Kim, Y.; Cunningham, M.A.; Mire, J.; Tesar, C; Sacchettini, J.; Joachimiak, A. NDM-1, the ultimate promiscuous enzyme: Substrate recognition and catalytic mechanism. FASEB J. 2013, 27, 1917-1927.
53. Brown, M.C.; Verma, D.; Russell, C; Jacobs, D.J.; Livesay, D.R. A case study comparing quantitative stability-flexibility relationships across five metallo-β-lactamases highlighting differences within NDM-1. Methods Mol. Biol. 2014, 1084, 227-238.
54. Scrofani, S.D.; Chung, J.; Huntley, J.J.; Benkovic, S.J.; Wright, P.E.; Dyson, H.J. NMR characterization of the metallo-beta-lactamase from Bacteroides fragilis and its interaction with a tight-binding inhibitor: Role of an active-site loop. Biochemistry 1999, 38, 14507-14514.
55. 19F-NMR spectroscopy. Angew. Chem. Int. Ed. 2014, 53, 3129-3133.
56. Murphy, T.A.; Catto, L.E.; Halford, S.E.; Hadfield, A.T.; Minor, W.; Walsh, T.R.; Spencer, J. Crystal structure of Pseudomonas aeruginosa SPM-1 provides insights into variable zinc affinity of metallo-beta-lactamases. J. Mol. Biol. 2006, 357, 890-903.
57. Poirel, L.; Naas, T.; Nicolas, D.; Collet, L.; Bellais, S.; Cavallo, J.D.; Nordmann, P. Characterization of VIM-2, a carbapenem-hydrolyzing metallo-beta-lactamase and its plasmid-and integron-borne gene from a Pseudomonas aeruginosa clinical isolate in France. Antimicrob. Agents Chemother. 2000, 44, 891-897.
58. Bush, K.; Fisher, J.F. Epidemiological expansion, structural studies, and clinical challenges of new β-lactamases from gram-negative bacteria. Annu. Rev. Microbiol. 2011, 65, 455-478.
59. Docquier, J.-D.; Lamotte-Brasseur, J.; Galleni, M.; Amicosante, G.; Frère, J.-M.; Rossolini, G.M. On functional and structural heterogeneity of VIM-type metallo-β-lactamases. J. Antimicrob. Chemother. 2003, 51, 257-266.
60. Lassaux, P.; Traoré, D.A.K.; Loisel, E.; Favier, A.; Docquier, J.-D.; Sohier, J.S.; Laurent, C; Bebrone, C; Frère, J.-M.; Ferrer, J.-L. et al. Biochemical and structural characterization of the subclass B1 metallo-β-lactamase VIM-4. Antimicrob. Agents Chemother. 2011, 55, 1248-1255.
61. Samuelsen, Ø.; Castanheira, M.; Walsh, T.R.; Spencer, J. Kinetic characterization of VIM-7, a divergent member of the VIM metallo-beta-lactamase family. Antimicrob. Agents Chemother. 2008, 52, 2905-2908.
62. Marchiaro, P.; Tomatis, P.E.; Mussi, M.A.; Pasteran, F.; Viale, A.M.; Limansky, A.S.; Vila, A.J. Biochemical characterization of metallo-beta-lactamase VIM-11 from a Pseudomonas aeruginosa clinical strain. Antimicrob. Agents Chemother. 2008, 52, 2250-2252.
63. Merino, M.; Pérez-Llarena, F.J.; Kerff, F.; Poza, M.; Mallo, S.; Rumbo-Feal, S.; Beceiro, A.; Juan, C; Oliver, A.; Bou, G. Role of changes in the L3 loop of the active site in the evolution of enzymatic activity of VIM-type metallo-β-lactamases. J. Antimicrob. Chemother. 2010, 65, 1950-1954.
64. Rodriguez-Martinez, J.-M.; Nordmann, P.; Fortineau, N.; Poirel, L. VIM-19, a metallo-β-lactamase with increased carbapenemase activity from Escherichia coli and Klebsiella pneumoniae. Antimicrob. Agents Chemother. 2010, 54, 471-476.
65. Bogaerts, P.; Bebrone, C; Huang, T.-D.; Bouchahrouf, W.; DeGheldre, Y.; Deplano, A.; Hoffmann, K.; Glupczynski, Y. Detection and characterization of VIM-31, a new variant of VIM-2 with Tyr224His and His252Arg mutations, in a clinical isolate of Enterobacter cloacae. Antimicrob. Agents Chemother. 2012, 56, 3283-3287.
66. Yamaguchi, Y.; Jin, W.; Matsunaga, K.; Ikemizu, S.; Yamagata, Y.; Wachino, J.; Shibata, N.; Arakawa, Y.; Kurosaki, H. Crystallographic investigation of the inhibition mode of a VIM-2 metallo-beta-lactamase from Pseudomonas aeruginosa by a mercaptocarboxylate inhibitor. J. Med. Chem. 2007, 50, 6647-6653.
67. Borra, P.S.; Leiros, H.-K.S.; Ahmad, R.; Spencer, J.; Leiros, I.; Walsh, T.R.; Sundsfjord, A.; Samuelsen, O. Structural and computational investigations of VIM-7: Insights into the substrate specificity of VIM metallo-β-lactamases. J. Mol. Biol. 2011, 411, 174-189.
68. Rasia, R.M.; Vila, A.J. Structural determinants of substrate binding to Bacillus cereus metallo-beta-lactamase. J. Biol. Chem. 2004, 279, 26046-26051.
69. Crooks, G.E.; Hon, G.; Chandonia, J.-M.; Brenner, S.E. WebLogo: A Sequence Logo Generator. Genome Res. 2004, 14, 1188-1190.
70. Tamura, K.; Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993, 10, 512-526.
71. Tamura, K.; Stecher, G; Peterson, D.; Filipski, A.; Kumar, S. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013, 30, 2725-2729.
72. King, D.T.; Worrall, L.J.; Gruninger, R.; Strynadka, N.C.J. New Delhi metallo-β-lactamase: Structural insights into β-lactam recognition and inhibition. J. Am. Chem. Soc. 2012, 134, 11362-11365.
73. Materon, I.C.; Beharry, Z.; Huang, W.; Perez, C; Palzkill, T. Analysis of the context dependent sequence requirements of active site residues in the metallo-beta-lactamase IMP-1. J. Mol. Biol. 2004, 344, 653-663.
74. Moali, C; Anne, C; Lamotte-Brasseur, J.; Groslambert, S.; Devreese, B.; van Beeumen, J.; Galleni, M.; Frère, J.-M. Analysis of the importance of the Metallo-β-lactamase active site loop in substrate binding and catalysis. Chem. Biol. 2003, 10, 319-329.
75. Huntley, J.J.A.; Fast, W.; Benkovic, S.J.; Wright, P.E.; Dyson, H.J. Role of a solvent-exposed tryptophan in the recognition and binding of antibiotic substrates for a metallo-beta-lactamase. Protein Sci. 2003, 12, 1368-1375.
76. Mollard, C; Moali, C; Papamicael, C; Damblon, C; Vessilier, S.; Amicosante, G; Schofield, C.J.; Galleni, M.; Frère, J.-M.; Roberts, G.C.K. Thiomandelic acid, a broad spectrum inhibitor of Zinc β-Lactamases kinetic and spectroscopic studies. J. Biol. Chem. 2001, 276, 45015-45023.
77. Karsisiotis, A.I.; Damblon, C.F.; Roberts, G.C.K. Solution structures of the Bacillus cereus metallo-β-lactamase BcII and its complex with the broad spectrum inhibitor R-thiomandelic acid. Biochem. J. 2013, 456, 397-407.
78. González, J.M.; Buschiazzo, A.; Vila, A.J. Evidence of adaptability in metal coordination geometry and active-site loop conformation among B1 metallo-beta-lactamases. Biochemistry 2010, 49, 7930-7938.
79. Borgianni, L.; Vandenameele, J.; Matagne, A.; Bini, L.; Bonomo, R.A.; Frere, J.-M.; Rossolini, G.M.; Docquier, J.-D. Mutational analysis of VIM-2 reveals an essential determinant for Metallo-β-lactamase stability and folding. Antimicrob. Agents Chemother. 2010, 54, 3197-3204.
80. Marciano, D.C.; Brown, N.G.; Palzkill, T. Analysis of the plasticity of location of the Arg244 positive charge within the active site of the TEM-1 beta-lactamase. Protein Sci. 2009, 18, 2080-2089.
81. Watanabe, M.; Iyobe, S.; Inoue, M.; Mitsuhashi, S. Transferable imipenem resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 1991, 35, 147-151.
82. Zhao, W.-H.; Hu, Z.-Q. IMP-type metallo-β-lactamases in Gram-negative bacilli: Distribution, phylogeny, and association with integrons. Crit. Rev. Microbiol. 2011, 37, 214-226.
83. Liu, E.M.; Pegg, K.M.; Oelschlaeger, P. The sequence-activity relationship between metallo-β-lactamases IMP-1, IMP-6, and IMP-25 suggests an evolutionary adaptation to meropenem exposure. Antimicrob. Agents Chemother. 2012, 56, 6403-6406.
84. Oelschlaeger, P.; Mayo, S.L.; Pleiss, J. Impact of remote mutations on metallo-beta-lactamase substrate specificity: Implications for the evolution of antibiotic resistance. Protein Sci. 2005, 14, 765-774.
85. Oelschlaeger, P.; Schmid, R.D.; Pleiss, J. Modeling domino effects in enzymes: Molecular basis of the substrate specificity of the bacterial metallo-beta-lactamases IMP-1 and IMP-6. Biochemistry 2003, 42, 8945-8956.
86. Haruta, S.; Yamamoto, E.T.; Eriguchi, Y.; Sawai, T. Characterization of the active-site residues asparagine 167 and lysine 161 of the IMP-1 metallo beta-lactamase. FEMS Microbiol. Lett. 2001, 197, 85-89.
87. Yanchak, M.P.; Taylor, R.A.; Crowder, M.W. Mutational analysis of metallo-beta-lactamase CcrA from Bacteroides fragilis. Biochemistry 2000, 39, 11330-11339.
88. Brown, N.G.; Horton, L.B.; Huang, W.; Vongpunsawad, S.; Palzkill, T. Analysis of the functional contributions of Asn233 in metallo-β-lactamase IMP-1. Antimicrob. Agents Chemother. 2011, 55, 5696-5702.
89. Pegg, K.M.; Liu, E.M.; Lacuran, A.E.; Oelschlaeger, P. Biochemical characterization of IMP-30, a metallo-β-lactamase with enhanced activity toward ceftazidime. Antimicrob. Agents Chemother. 2013, 57, 5122-5126.
90. Murphy, T.A.; Simm, A.M.; Toleman, M.A.; Jones, R.N.; Walsh, T.R. Biochemical characterization of the acquired metallo-beta-lactamase SPM-1 from Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2003, 47, 582-587.
91. Johnson, A.P.; Woodford, N. Global spread of antibiotic resistance: The example of New Delhi metallo-β-lactamase (NDM)-mediated carbapenem resistance. J. Med. Microbiol. 2013, 62, 499-513.
92. Maya, J.J.; Ruiz, S.J.; Blanco, V.M.; Gotuzzo, E.; Guzman-Blanco, M.; Labarca, J.; Salles, M.; Quinn, J.P.; Villegas, M.V. Current status of carbapenemases in Latin America. Expert Rev. Anti Infect. Ther. 2013, 11, 657-667.
93. Kumarasamy, K.K.; Toleman, M.A.; Walsh, T.R.; Bagaria, J.; Butt, F.; Balakrishnan, R.; Chaudhary, U.; Doumith, M.; Giske, C.G.; Irfan, S. et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: A molecular, biological, and epidemiological study. Lancet Infect. Dis. 2010, 10, 597-602.
94. Nordmann, P.; Poirel, L.; Walsh, T.R.; Livermore, D.M. The emerging NDM carbapenemases. Trends Microbiol. 2011, 19, 588-595.
95. Walsh, T.R.; Weeks, J.; Livermore, D.M.; Toleman, M.A. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: An environmental point prevalence study. Lancet Infect. Dis. 2011, 11, 355-362.
96. Livermore, D.M.; Walsh, T.R.; Toleman, M.; Woodford, N. Balkan NDM-1: Escape or transplant? Lancet Infect. Dis. 2011, 11, 164.
97. Jovcic, B.; Lepsanovic, Z.; Suljagic, V.; Rackov, G.; Begovic, J.; Topisirovic, L.; Kojic, M. Emergence of NDM-1 Metallo-β-Lactamase in Pseudomonas aeruginosa clinical isolates from Serbia. Antimicrob. Agents Chemother. 2011, 55, 3929-3931.
98. Nordmann, P.; Boulanger, A.E.; Poirel, L. NDM-4 metallo-β-lactamase with increased carbapenemase activity from Escherichia coli. Antimicrob. Agents Chemother. 2012, 56, 2184-2186.
99. Hornsey, M.; Phee, L.; Wareham, D.W. A novel variant, NDM-5, of the New Delhi metallo-β-lactamase in a multidrug-resistant Escherichia coli ST648 isolate recovered from a patient in the United Kingdom. Antimicrob. Agents Chemother. 2011, 55, 5952-5954.
100. Cuzon, G; Bonnin, R.A.; Nordmann, P. First identification of novel NDM carbapenemase, NDM-7, in Escherichia coli in France. PLoS One 2013, 8, e61322.
101. Tada, T.; Miyoshi-Akiyama, T.; Dahal, R.K.; Sah, M.K.; Ohara, H.; Kirikae, T.; Pokhrel, B.M. NDM-8 metallo-β-lactamase in a multidrug-resistant Escherichia coli strain isolated in Nepal. Antimicrob. Agents Chemother. 2013, 57, 2394-2396.
102. Hall, B.G. In vitro evolution predicts that the IMP-1 metallo-beta-lactamase does not have the potential to evolve increased activity against imipenem. Antimicrob. Agents Chemother. 2004, 48, 1032-1033.
103. Matsumura, N.; Minami, S.; Watanabe, Y.; Iyobe, S.; Mitsuhashi, S. Role of permeability in the activities of β-Lactams against gram-negative bacteria which produce a group 3 β-Lactamase. Antimicrob. Agents Chemother. 1999, 43, 2084-2086.
104. Heinisch, T.; Ward, T.R. Design strategies for the creation of artificial metalloenzymes. Curr. Opin. Chem. Biol. 2010, 14, 184-199.
105. Brustad, E.M.; Arnold, F.H. Optimizing non-natural protein function with directed evolution. Curr. Opin. Chem. Biol. 2011, 15, 201-210.
106. Park, H.-S.; Nam, S.-H.; Lee, J.K.; Yoon, C.N.; Mannervik, B.; Benkovic, S.J.; Kim, H.-S. Design and evolution of new catalytic activity with an existing protein scaffold. Science 2006, 311, 535-538.
107. Sun, S.; Zhang, W.; Mannervik, B.; Andersson, D.I. Evolution of broad spectrum β-lactam resistance in an engineered metallo-β-lactamase. J. Biol. Chem. 2013, 288, 2314-2324.
108. Gonzalez, L.J.; Moreno, D.M.; Bonomo, R.A.; Vila, A.J. Host-specific enzyme-substrate interactions in SPM-1 metallo-β-lactamase are modulated by second sphere residues. PLoS Pathog. 2014, 10, e1003817.
109. Liu, J.Z.; Jellbauer, S.; Poe, A.J.; Ton, V.; Pesciaroli, M.; Kehl-Fie, T.E.; Restrepo, N.A.; Hosking, M.P.; Edwards, R.A.; Battistoni, A. et al. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 2012, 11, 227-239.
110. Hood, M.I.; Mortensen, B.L.; Moore, J.L.; Zhang, Y.; Kehl-Fie, T.E.; Sugitani, N.; Chazin, W.J.; Caprioli, R.M.; Skaar, E.P. Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog. 2012, 8, e1003068.