Structural and biochemical characterization of VIM-26 shows that Leu224 has implications for the substrate specificity of VIM metallo-β-lactamases

FEBS Journal

Volumn 282, Issue 6, 2015, Pages 1031-1042

  Leiros, Hanna Kirsti S ^a   Edvardsen, Kine Susann Waade ^a,c   Bjerga, Gro Elin Kjæreng ^a,d   Samuelsen, Ørjan ^b  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^c UNIVERSITY OF BERGEN   (Norway)

^d UNIVERSITY OF BERGEN   (Norway)

Author keywords

antibiotic resistance; drug binding site; Klebsiella pneumoniae; metallo lactamase; minimum inhibitory concentrations

Indexed keywords

AMPICILLIN; ARGININE; BACTERIAL PROTEIN; CEFEPIME; CEFOXITIN; CEFTAZIDIME; CEFUROXIME; CEPHALOSPORINASE; ERTAPENEM; HISTIDINE; IMIPENEM; LEUCINE; MEROPENEM; METALLO BETA LACTAMASE; PENICILLIN G; PENICILLINASE; PROTEIN VARIANT; PROTEIN VIM 1; PROTEIN VIM 2; PROTEIN VIM 26; PROTEIN VIM 7; RECOMBINANT PROTEIN; SERINE; TYROSINE; UNCLASSIFIED DRUG; ZINC; ANTIINFECTIVE AGENT; BETA LACTAMASE; BETA-LACTAMASE VIM-26, KLEBSIELLA PNEUMONIAE; CARBAPENEM DERIVATIVE; CEPHALOSPORIN DERIVATIVE; ION; PENICILLIN DERIVATIVE; PROTEIN BINDING;

ARTICLE; CATALYSIS; DRUG BINDING SITE; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SPECIFICITY; GEOMETRY; KLEBSIELLA PNEUMONIAE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; PROTEIN ISOLATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; ANTIBIOTIC RESISTANCE; BINDING SITE; CHEMISTRY; ENZYMOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

KLEBSIELLA PNEUMONIAE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAMASES; BINDING SITES; CARBAPENEMS; CATALYSIS; CEPHALOSPORINS; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, BACTERIAL; IONS; KLEBSIELLA PNEUMONIAE; LEUCINE; PENICILLINS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SERINE; SUBSTRATE SPECIFICITY;

EID: 84925615027     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13200     Document Type: Article

References (40)

1. WHO (2014) World Health Organization: Antimicrobial resistance: globalreport on surveillance, ISBN-978-992-974-156474-156478.
2. Palzkill T, (2013) Metallo-β-lactamase structure and function. Ann N Y Acad Sci 1277, 91-104.
3. Patel G, &, Bonomo RA, (2013) "Stormy waters ahead": global emergence of carbapenemases. Front Microbiol 4, 48.
4. Walsh TR, Toleman MA, Poirel L, &, Nordmann P, (2005) Metallo-β-lactamases: the quiet before the storm? Clin Microbiol Rev 18, 306-325.
5. Rodriguez-Martinez JM, Nordmann P, Fortineau N, &, Poirel L, (2010) VIM-19, a metallo-β-lactamase with increased carbapenemase activity from Escherichia coli and Klebsiella pneumoniae. Antimicrob Agents Chemother 54, 471-476.
6. Samuelsen Ø, Toleman MA, Hasseltvedt V, Fuursted K, Leegaard TM, Walsh TR, Sundsfjord A, &, Giske CG, (2011) Molecular characterization of VIM-producing Klebsiella pneumoniae from Scandinavia reveals genetic relatedness with international clonal complexes encoding transferable multidrug resistance. Clin Microbiol Infect 17, 1811-1816.
7. Merino M, Perez-Llarena FJ, Kerff F, Poza M, Mallo S, Rumbo-Feal S, Beceiro A, Juan C, Oliver A, &, Bou G, (2010) 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 65, 1950-1954.
8. Zhang H, &, Hao Q, (2011) Crystal structure of NDM-1 reveals a common β-lactam hydrolysis mechanism. FASEB J 25, 2574-2582.
9. Borra PS, Leiros H-KS, Ahmad R, Spencer J, Leiros I, Walsh TR, Sundsfjord A, &, Samuelsen Ø, (2011) Structural and Computational Investigations of VIM-7: insights into the Substrate Specificity of VIM Metallo-β-Lactamases. J Mol Biol 411, 174-189.
10. Borra PS, Samuelsen Ø, Spencer J, Walsh TR, Lorentzen MS, &, Leiros H-KS, (2013) Crystal Structures of Pseudomonas aeruginosa GIM-1: active-Site Plasticity in Metallo-β-Lactamases. Antimicrob Agents Chemother 57, 848-854.
11. Castanheira M, Deshpande LM, Mendes RE, Rodriguez-Noriega E, Jones RN, &, Morfin-Otero R, (2011) Comment on: 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 66, 684-685. author reply 686.
12. Materon IC, &, Palzkill T, (2001) Identification of residues critical for metallo-β-lactamase function by codon randomization and selection. Protein Sci 10, 2556-2565.
13. Samuelsen Ø, Castanheira M, Walsh TR, &, Spencer J, (2008) Kinetic characterization of VIM-7, a divergent member of the VIM metallo-β-lactamase family. Antimicrob Agents Chemother 52, 2905-2908.
14. Leiros H-KS, Skagseth S, Edvardsen KS, Lorentzen MS, Bjerga GE, Leiros I, &, Samuelsen Ø, (2014) His224 Alters the R2 Drug Binding Site and Phe218 Influences the Catalytic Efficiency of the Metallo-β-Lactamase VIM-7. Antimicrob Agents Chemother 58, 4826-4836.
15. Yamaguchi Y, Jin W, Matsunaga K, Ikemizu S, Yamagata Y, Wachino J, Shibata N, Arakawa Y, &, Kurosaki H, (2007) Crystallographic investigation of the inhibition mode of a VIM-2 metallo-β-lactamase from Pseudomonas aeruginosa by a mercaptocarboxylate inhibitor. J Med Chem 50, 6647-6653.
16. Lassaux P, Traore DA, Loisel E, Favier A, Docquier JD, Sohier JS, Laurent C, Bebrone C, Frere JM, Ferrer JL, et al,. (2011) Biochemical and structural characterization of the subclass B1 metallo-β-lactamase VIM-4. Antimicrob Agents Chemother 55, 1248-1255.
17. Johnson AP, &, Woodford N, (2013) Global spread of antibiotic resistance: the example of New Delhi metallo-β-lactamase (NDM)-mediated carbapenem resistance. J Med Microbiol 62, 499-513.
18. Drawz SM, &, Bonomo RA, (2010) Three decades of β-lactamase inhibitors. Clin Microbiol Rev 23, 160-201.
19. King AM, Reid-Yu SA, Wang W, King DT, De Pascale G, Strynadka NC, Walsh TR, Coombes BK, &, Wright GD, (2014) Aspergillomarasmine A overcomes metallo-β-lactamase antibiotic resistance. Nature 510, 503-506.
20. Drawz SM, Papp-Wallace KM, &, Bonomo RA, (2014) New β-lactamase inhibitors: a therapeutic renaissance in an MDR world. Antimicrob Agents Chemother 58, 1835-1846.
21. Franceschini N, Caravelli B, Docquier JD, Galleni M, Frere JM, Amicosante G, &, Rossolini GM, (2000) Purification and biochemical characterization of the VIM-1 metallo-β-lactamase. Antimicrob Agents Chemother 44, 3003-3007.
22. Docquier JD, Lamotte-Brasseur J, Galleni M, Amicosante G, Frere JM, &, Rossolini GM, (2003) On functional and structural heterogeneity of VIM-type metallo-β-lactamases. J Antimicrob Chemother 51, 257-266.
23. Gacar GG, Midilli K, Kolayli F, Ergen K, Gundes S, Hosoglu S, Karadenizli A, &, Vahaboglu H, (2005) Genetic and enzymatic properties of metallo-β-lactamase VIM-5 from a clinical isolate of Enterobacter cloacae. Antimicrob Agents Chemother 49, 4400-4403.
24. Murphy TA, Catto LE, Halford SE, Hadfield AT, Minor W, Walsh TR, &, Spencer J, (2006) Crystal structure of Pseudomonas aeruginosa SPM-1 provides insights into variable zinc affinity of metallo-β-lactamases. J Mol Biol 357, 890-903.
25. Davies AM, Rasia RM, Vila AJ, Sutton BJ, &, Fabiane SM, (2005) Effect of pH on the active site of an Arg121Cys mutant of the metallo-β-lactamase from Bacillus cereus: implications for the enzyme mechanism. Biochemistry 44, 4841-4849.
26. Garcia-Saez I, Docquier JD, Rossolini GM, &, Dideberg O, (2008) The three-dimensional structure of VIM-2, a Zn-β-lactamase from Pseudomonas aeruginosa in its reduced and oxidised form. J Mol Biol 375, 604-611.
27. Leiros H-KS, Timmins J, Ravelli RB, &, McSweeney SM, (2006) Is radiation damage dependent on the dose rate used during macromolecular crystallography data collection? Acta Crystallogr D Biol Crystallogr 62, 125-132.
28. Ravelli RB, Leiros H-KS, Pan B, Caffrey M, &, McSweeney S, (2003) Specific radiation damage can be used to solve macromolecular crystal structures. Structure 11, 217-224.
29. Garau G, Bebrone C, Anne C, Galleni M, Frere JM, &, Dideberg O, (2005) A metallo-β-lactamase enzyme in action: crystal structures of the monozinc carbapenemase CphA and its complex with biapenem. J Mol Biol 345, 785-795.
30. Yanchak MP, Taylor RA, &, Crowder MW, (2000) Mutational analysis of metallo-β-lactamase CcrA from Bacteroides fragilis. Biochemistry 39, 11330-11339.
31. Brown NG, Horton LB, Huang W, Vongpunsawad S, &, Palzkill T, (2011) Analysis of the functional contributions of Asn233 in metallo-β-lactamase IMP-1. Antimicrob Agents Chemother 55, 5696-5702.
32. Materon IC, Beharry Z, Huang W, Perez C, &, Palzkill T, (2004) Analysis of the context dependent sequence requirements of active site residues in the metallo-β-lactamase IMP-1. J Mol Biol 344, 653-663.
33. Yamaguchi Y, Takashio N, Wachino J, Yamagata Y, Arakawa Y, Matsuda K, &, Kurosaki H, (2010) Structure of metallo-β-lactamase IND-7 from a Chryseobacterium indologenes clinical isolate at 1.65-Å resolution. J Biochem 147, 905-915.
34. Leiros H-KS, Borra PS, Brandsdal BO, Edvardsen KS, Spencer J, Walsh TR, &, Samuelsen Ø, (2012) Crystal Structure of the Mobile Metallo-β-Lactamase AIM-1 from Pseudomonas aeruginosa: insights into Antibiotic Binding and the Role of Gln157. Antimicrob Agents Chemother 56, 4341-4353.
35. Garau G, Garcia-Saez I, Bebrone C, Anne C, Mercuri P, Galleni M, Frere JM, &, Dideberg O, (2004) Update of the standard numbering scheme for class B β-lactamases. Antimicrob Agents Chemother 48, 2347-2349.
36. Kabsch W, (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Crystallogr 24, 795-800.
37. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, &, Read RJ, (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr D Biol Crystallogr 61, 458-464.
38. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al,. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr D66, 213-221.
39. Emsley P, Lohkamp B, Scott WG, &, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66, 486-501.
40. Spencer J, Read J, Sessions RB, Howell S, Blackburn GM, &, Gamblin SJ, (2005) Antibiotic recognition by binuclear metallo-β-lactamases revealed by X-ray crystallography. J Am Chem Soc 127, 14439-14444.