Structural and biochemical characterization of Rm3, a subclass B3 metallo-β-lactamase identified from a functional metagenomic study

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 10, 2016, Pages 5828-5840

  Salimraj, Ramya ^a   Zhang, Lihong ^b,d   Hinchliffe, Philip ^a   Wellington, Elizabeth M H ^b   Brem, Jürgen ^c   Schofield, Christopher J ^c   Gaze, William H ^b,d   Spencer, James ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF EXETER MEDICAL SCHOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMOXICILLIN; AMPICILLIN; AZTREONAM; BACTERIAL ENZYME; BETA LACTAM ANTIBIOTIC; BIOCIDE; CARBAPENEM DERIVATIVE; CARBENICILLIN; CEFOTAXIME; CEFTAZIDIME; CEPHALOSPORIN DERIVATIVE; FEZ 1 PROTEIN; IMIPENEM; METALLO BETA LACTAMASE; PENICILLIN DERIVATIVE; RM3 PROTEIN; TEMOCILLIN; UNCLASSIFIED DRUG; ZINC; BETA LACTAMASE; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CHROMOSOME; BINDING AFFINITY; BIOCHEMICAL ANALYSIS; BLA RM3 GENE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ESCHERICHIA COLI; GENE EXPRESSION; GENE PRODUCT; GENOMICS; HYDROLYSIS; METAGENOMICS; NONHUMAN; PERIPLASM; PRIORITY JOURNAL; PROTEIN FOLDING; STEREOSPECIFICITY; CHEMISTRY; DRUG EFFECTS; GENETICS; METABOLISM; MICROBIAL SENSITIVITY TEST; MOLECULAR MODEL; PHYLOGENY; PROCEDURES; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

BETA-LACTAMASES; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; METAGENOMICS; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; PHYLOGENY; PROTEIN CONFORMATION; RECOMBINANT PROTEINS;

EID: 84992659574     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00750-16     Document Type: Article

References (73)

1. Fisher JF, Meroueh SO, Mobashery S. 2005. Bacterial resistance to β-lactam antibiotics: compelling opportunism, compelling opportunity. Chem Rev 105:395-424. http://dx.doi.org/10.1021/cr030102i.
2. Bush K. 2013. Proliferation and significance of clinically relevant β-lactamases. Ann N Y Acad Sci 1277:84-90. http://dx.doi.org/10.1111/nyas.12023.
3. D'Andrea MM, Arena F, Pallecchi L, Rossolini GM. 2013. CTX-M-type β-lactamases: a successful story of antibiotic resistance. Int J Med Microbiol 303:305-317. http://dx.doi.org/10.1016/j.ijmm.2013.02.008.
4. Wellington EM, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM, Johnson-Rollings AS, Jones DL, Lee NM, Otten W, Thomas CM, Williams AP. 2013. The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect Dis 13:155-165. http://dx.doi.org/10.1016/S1473-3099(12)70317-1.
5. Humeniuk C, Arlet G, Gautier V, Grimont P, Labia R, Philippon A. 2002. β-Lactamases of Kluyvera ascorbata, probable progenitors of some plasmid-encoded CTX-M types. Antimicrob Agents Chemother 46:3045-3049. http://dx.doi.org/10.1128/AAC.46.9.3045-3049.2002.
6. Poirel L, Kampfer P, Nordmann P. 2002. Chromosome-encoded Ambler class A β-lactamase of Kluyvera georgiana, a probable progenitor of a subgroup of CTX-M extended-spectrum β-lactamases. Antimicrob Agents Chemother 46:4038-4040. http://dx.doi.org/10.1128/AAC.46.12.4038-4040.2002.
7. Sarria JC, Vidal AM, Kimbrough RC, III. 2001. Infections caused by Kluyvera species in humans. Clin Infect Dis 33:E69-E74. http://dx.doi.org/10.1086/322686.
8. Ambler RP. 1980. The structure of β-lactamases. Philos Trans R Soc Lond B Biol Sci 289:321-331. http://dx.doi.org/10.1098/rstb.1980.0049.
9. Palzkill T. 2013. Metallo-β-lactamase structure and function. Ann N Y Acad Sci 1277:91-104. http://dx.doi.org/10.1111/j.1749-6632.2012.06796.x.
10. Crowder MW, Spencer J, Vila AJ. 2006. Metallo-β-lactamases: novel weaponry for antibiotic resistance in bacteria. Acc Chem Res 39:721-728. http://dx.doi.org/10.1021/ar0400241.
11. Drawz SM, Bonomo RA. 2010. Three decades of β-lactamase inhibitors. Clin Microbiol Rev 23:160-201. http://dx.doi.org/10.1128/CMR.00037-09.
12. Dortet L, Poirel L, Nordmann P. 2014. Worldwide dissemination of the NDM-type carbapenemases in Gram-negative bacteria. Biomed Res Int 2014:249856. http://dx.doi.org/10.1155/2014/249856.
13. Papagiannitsis CC, Izdebski R, Baraniak A, Fiett J, Herda M, Hrabak J, Derde LP, Bonten MJ, Carmeli Y, Goossens H, Hryniewicz W, Brun-Buisson C, Gniadkowski M, MOSAR WP2, WP3 and WP5 Study Groups, MOSAR WP2, WP3 and WP5 Study Groups. 2015. Survey of metallo-β-lactamase-producing Enterobacteriaceae colonizing patients in European ICUs and rehabilitation units, 2008-11. J Antimicrob Chemother 70:1981-1988. http://dx.doi.org/10.1093/jac/dkv055.
14. AIM-1, and its unique genetic context in Pseudomonas aeruginosa from Australia. Antimicrob Agents Chemother 56:6154-6159. http://dx.doi.org/10.1128/AAC.05654-11.
15. Wachino J, Yoshida H, Yamane K, Suzuki S, Matsui M, Yamagishi T, Tsutsui A, Konda T, Shibayama K, Arakawa Y. 2011. SMB-1, a novel subclass B3 metallo-β-lactamase, associated with ISCR1 and a class 1 integron, from a carbapenem-resistant Serratia marcescens clinical isolate. Antimicrob Agents Chemother 55:5143-5149. http://dx.doi.org/10.1128/AAC.05045-11.
16. Bicknell R, Emanuel EL, Gagnon J, Waley SG. 1985. The production and molecular properties of the zinc β-lactamase of Pseudomonas maltophilia IID 1275. Biochem J 229:791-797. http://dx.doi.org/10.1042/bj2290791.
17. Bellais S, Aubert D, Naas T, Nordmann P. 2000. Molecular and biochemical heterogeneity of class B carbapenem-hydrolyzing β-lactamases in Chryseobacterium meningosepticum. Antimicrob Agents Chemother 44:1878-1886. http://dx.doi.org/10.1128/AAC.44.7.1878-1886.2000.
18. Bebrone C. 2007. Metallo-β-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily. Biochem Pharmacol 74:1686-1701. http://dx.doi.org/10.1016/j.bcp.2007.05.021.
19. Gaze WH, Krone SM, Larsson DG, Li XZ, Robinson JA, Simonet P, Smalla K, Timinouni M, Topp E, Wellington EM, Wright GD, Zhu YG. 2013. Influence of humans on evolution and mobilization of environmental antibiotic resistome. Emerg Infect Dis 19:120871. http://dx.doi.org/10.3201/eid1907.120871.
20. Allen HK, Moe LA, Rodbumrer J, Gaarder A, Handelsman J. 2009. Functional metagenomics reveals diverse β-lactamases in a remote Alaskan soil. ISME J 3:243-251. http://dx.doi.org/10.1038/ismej.2008.86.
21. Amos GC, Zhang L, Hawkey PM, Gaze WH, Wellington EM. 2014. Functional metagenomic analysis reveals rivers are a reservoir for diverse antibiotic resistance genes. Vet Microbiol 171:441-447. http://dx.doi.org/10.1016/j.vetmic.2014.02.017.
22. Torres-Cortes G, Millan V, Ramirez-Saad HC, Nisa-Martinez R, Toro N, Martinez-Abarca F. 2011. Characterization of novel antibiotic resistance genes identified by functional metagenomics on soil samples. Environ Microbiol 13:1101-1114. http://dx.doi.org/10.1111/j.1462-2920.2010.02422.x.
23. Shoemaker WR, Muscarella ME, Lennon JT. 2015. Genome sequence of the soil bacterium Janthinobacterium sp. KBS0711. Genome Announc 3(3):e00689-15. http://dx.doi.org/10.1128/genomeA.00689-15.
24. Forsberg KJ, Patel S, Gibson MK, Lauber CL, Knight R, Fierer N, Dantas G. 2014. Bacterial phylogeny structures soil resistomes across habitats. Nature 509:612-616. http://dx.doi.org/10.1038/nature13377.
25. Docquier JD, Lopizzo T, Liberatori S, Prenna M, Thaller MC, Frere JM, Rossolini GM. 2004. Biochemical characterization of the THIN-B metallo-β-lactamase of Janthinobacterium lividum. Antimicrob Agents Chemother 48:4778-4783. http://dx.doi.org/10.1128/AAC.48.12.4778-4783.2004.
26. Stoczko M, Frere JM, Rossolini GM, Docquier JD. 2006. Postgenomic scan of metallo-β-lactamase homologues in rhizobacteria: identification and characterization of BJP-1, a subclass B3 ortholog from Bradyrhizobium japonicum. Antimicrob Agents Chemother 50:1973-1981. http://dx.doi.org/10.1128/AAC.01551-05.
27. Gaze WH, Abdouslam N, Hawkey PM, Wellington EM. 2005. Incidence of class 1 integrons in a quaternary ammonium compound-polluted environment. Antimicrob Agents Chemother 49:1802-1807. http://dx.doi.org/10.1128/AAC.49.5.1802-1807.2005.
28. Newman JR, Fuqua C. 1999. Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227:197-203. http://dx.doi.org/10.1016/S0378-1119(98)00601-5.
29. Andrews JM. 2001. Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48(Suppl 1):5-16. http://dx.doi.org/10.1093/jac/48.suppl-1.5.
30. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185:60-89. http://dx.doi.org/10.1016/0076-6879(90)85008-C.
31. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685. http://dx.doi.org/10.1038/227680a0.
32. Brem J, Struwe WB, Rydzik AM, Tarhonskaya H, Pfeffer I, Flashman E, van Berkel SS, Spencer J, Claridge TD, McDonough MA, Benesch JL, Schofield CJ. 2015. Studying the active-site loop movement of the Sao Paolo metallo-β-lactamase-1. Chem Sci 6:956-963. http://dx.doi.org/10.1039/C4SC01752H.
33. Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF. 1999. Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531-552.
34. Laraki N, Franceschini N, Rossolini GM, Santucci P, Meunier C, de Pauw E, Amicosante G, Frere JM, Galleni M. 1999. Biochemical characterization of the Pseudomonas aeruginosa 101/1477 metallo-β-lactamase IMP-1 produced by Escherichia coli. Antimicrob Agents Chemother 43:902-906.
35. Toth M, Vakulenko V, Antunes NT, Frase H, Vakulenko SB. 2012. Class A carbapenemase FPH-1 from Francisella philomiragia. Antimicrob Agents Chemother 56:2852-2857. http://dx.doi.org/10.1128/AAC.00223-12.
36. Radaev S, Li S, Sun PD. 2006. A survey of protein-protein complex crystallizations. Acta Crystallogr D Biol Crystallogr 62:605-612. http://dx.doi.org/10.1107/S0907444906011735.
37. Kabsch W. 2010. XDS. Acta Crystallogr D Biol Crystallogr 66:125-132. http://dx.doi.org/10.1107/S0907444909047337.
38. Evans PR. 2011. An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr D Biol Crystallogr 67:282-292. http://dx.doi.org/10.1107/S090744491003982X.
39. Winter G. 2010. xia2: an expert system for macromolecular crystallography data reduction. J Appl Crystallogr 43:186-190. http://dx.doi.org/10.1107/S0021889809045701.
40. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40:658-674. http://dx.doi.org/10.1107/S0021889807021206.
41. Stein N. 2008. CHAINSAW: a program for mutating pdb files used as templates in molecular replacement. J Appl Crystallogr 41:641-643. http://dx.doi.org/10.1107/S0021889808006985.
42. Lienard BM, Garau G, Horsfall L, Karsisiotis AI, Damblon C, Lassaux P, Papamicael C, Roberts GC, Galleni M, Dideberg O, Frere JM, Schofield CJ. 2008. Structural basis for the broad-spectrum inhibition of metallo-β-lactamases by thiols. Org Biomol Chem 6:2282-2294. http://dx.doi.org/10.1039/b802311e.
43. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66:486-501. http://dx.doi.org/10.1107/S0907444910007493.
44. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53:240-255. http://dx.doi.org/10.1107/S0907444996012255.
45. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66:12-21. http://dx.doi.org/10.1107/S0907444909042073.
46. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213-221. http://dx.doi.org/10.1107/S0907444909052925.
47. Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DG. 2015. Cooccurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics 16:964. http://dx.doi.org/10.1186/s12864-015-2153-5.
48. Buffet-Bataillon S, Tattevin P, Bonnaure-Mallet M, Jolivet-Gougeon A. 2012. Emergence of resistance to antibacterial agents: the role of quaternary ammonium compounds - a critical review. Int J Antimicrob Agents 39:381-389. http://dx.doi.org/10.1016/j.ijantimicag.2012.01.011.
49. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785-786. http://dx.doi.org/10.1038/nmeth.1701.
50. Stoczko M, Frere JM, Rossolini GM, Docquier JD. 2008. Functional diversity among metallo-β-lactamases: characterization of the CAR-1 enzyme of Erwinia carotovora. Antimicrob Agents Chemother 52:2473-2479. http://dx.doi.org/10.1128/AAC.01062-07.
51. Docquier JD, Pantanella F, Giuliani F, Thaller MC, Amicosante G, Galleni M, Frere JM, Bush K, Rossolini GM. 2002. CAU-1, a subclass B3 metallo-β-lactamase of low substrate affinity encoded by an ortholog present in the Caulobacter crescentus chromosome. Antimicrob Agents Chemother 46:1823-1830. http://dx.doi.org/10.1128/AAC.46.6.1823-1830.2002.
52. Galleni M, Lamotte-Brasseur J, Rossolini GM, Spencer J, Dideberg O, Frere JM. 2001. Standard numbering scheme for class B β-lactamases. Antimicrob Agents Chemother 45:660-663. http://dx.doi.org/10.1128/AAC.45.3.660-663.2001.
53. Docquier J-D, Benvenuti M, Calderone V, Stoczko M, Menciassi N, Rossolini GM, Mangani S. 2010. High-resolution crystal structure of the subclass B3 metallo-β-lactamase BJP-1: rational basis for substrate specificity and interaction with sulfonamides. Antimicrob Agents Chemother 54:4343-4351. http://dx.doi.org/10.1128/AAC.00409-10.
54. Page MI, Badarau A. 2008. The mechanisms of catalysis by metallo β-lactamases. Bioinorg Chem Appl 2008:576297. http://dx.doi.org/101155/2008/576297.
55. Addison AW, Rao TN, Reedijk J, Vanrijn J, Verschoor GC. 1984. Synthesis, structure, and spectroscopic properties of copper(II) compounds containing nitrogen sulfur donor ligands - the crystal and molecular-structure of aqua[1,7-bis(N-methylbenzimidazol-2′-yl)-2,6-dithiaheptane]copper(II) perchlorate. J Chem Soc Dalton Trans 1984:1349-1356. http://dx.doi.org/10.1039/DT9840001349.
56. 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. http://dx.doi.org/10.1093/jb/mvq029.
57. Wachino J, Yamaguchi Y, Mori S, Kurosaki H, Arakawa Y, Shibayama K. 2013. Structural insights into the subclass B3 metallo-β-lactamase SMB-1 and the mode of inhibition by the common metallo-β-lactamase inhibitor mercaptoacetate. Antimicrob Agents Chemother 57:101-109. http://dx.doi.org/10.1128/AAC.01264-12.
58. Krissinel E, Henrick K. 2004. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 60:2256-2268. http://dx.doi.org/10.1107/S0907444904026460.
59. Ullah JH, Walsh TR, Taylor IA, Emery DC, Verma CS, Gamblin SJ, Spencer J. 1998. The crystal structure of the L1 metallo-β-lactamase from Stenotrophomonas maltophilia at 1.7 Å resolution. J Mol Biol 284:125-136. http://dx.doi.org/10.1006/jmbi.1998.2148.
60. Garcia-Saez I, Mercuri PS, Papamicael C, Kahn R, Frere JM, Galleni M, Rossolini GM, Dideberg O. 2003. Three-dimensional structure of FEZ-1, a monomeric subclass B3 metallo-β-lactamase from Fluoribacter gormanii, in native form and in complex with D-captopril. J Mol Biol 325:651-660. http://dx.doi.org/10.1016/S0022-2836(02)01271-8.
61. Leiros HK, Borra PS, Brandsdal BO, Edvardsen KS, Spencer J, Walsh TR, Samuelsen O. 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. http://dx.doi.org/10.1128/AAC.00448-12.
62. Carenbauer AL, Garrity JD, Periyannan G, Yates RB, Crowder MW. 2002. Probing substrate binding to metallo-β-lactamase L1 from Stenotrophomonas maltophilia by using site-directed mutagenesis. BMC Biochem 3:4. http://dx.doi.org/10.1186/1471-2091-3-4.
63. Mercuri PS, Garcia-Saez I, De Vriendt K, Thamm I, Devreese B, Van Beeumen J, Dideberg O, Rossolini GM, Frere JM, Galleni M. 2004. Probing the specificity of the subclass B3 FEZ-1 metallo-β-lactamase by site-directed mutagenesis. J Biol Chem 279:33630-33638. http://dx.doi.org/10.1074/jbc.M403671200.
64. Garrity JD, Carenbauer AL, Herron LR, Crowder MW. 2004. Metal binding Asp-120 in metallo-β-lactamase L1 from Stenotrophomonas maltophilia plays a crucial role in catalysis. J Biol Chem 279:920-927. http://dx.doi.org/10.1074/jbc.M309852200.
65. 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. http://dx.doi.org/10.1021/ja0536062.
66. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. http://dx.doi.org/10.1038/msb.2011.75.
67. Kabsch W, Sander C. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637. http://dx.doi.org/10.1002/bip.360221211.
68. Robert X, Gouet P. 2014. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:W320-W324. http://dx.doi.org/10.1093/nar/gku316.
69. Felsenstein J. 1989. PHYLIP - phylogeny inference package (version 3.2). Cladistics 5:164-166.
70. T produced in Escherichia coli. Antimicrob Agents Chemother 45:1254-1262. http://dx.doi.org/10.1128/AAC.45.4.1254-1262.2001.
71. Crowder MW, Walsh TR, Banovic L, Pettit M, Spencer J. 1998. Overexpression, purification, and characterization of the cloned metallo-β-lactamase L1 from Stenotrophomonas maltophilia. Antimicrob Agents Chemother 42:921-926.
72. Simm AM, Higgins CS, Carenbauer AL, Crowder MW, Bateson JH, Bennett PM, Clarke AR, Halford SE, Walsh TR. 2002. Characterization of monomeric L1 metallo-β-lactamase and the role of the N-terminal extension in negative cooperativity and antibiotic hydrolysis. J Biol Chem 277:24744-24752. http://dx.doi.org/10.1074/jbc.M201524200.
73. Spencer J, Clarke AR, Walsh TR. 2001. Novel mechanism of hydrolysis of therapeutic beta-lactams by Stenotrophomonas maltophilia L1 metallo-β-lactamase. J Biol Chem 276:33638-33644. http://dx.doi.org/10.1074/jbc.M105550200.