Crystal structure of the mobile metallo-β-lactamase AIM-1 from Pseudomonas aeruginosa: Insights into antibiotic binding and the role of Gln157

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 8, 2012, Pages 4341-4353

  Leiros, Hanna Kirsti S ^a   Borr, Pardha S ^a   Brandsdal, Bjørn Olav ^a   Edvardsen, Kine Susann Waade ^a   Spencer, James ^b   Walsh, Timothy R ^c   Samuelsen, Ørjan ^d  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ADELAIDE IMIPENEMASE 1; AMPICILLIN; CEFEPIME; CEFOXITIN; CEFTAZIDIME; CEFUROXIME; ERTAPENEM; GLUTAMINE; IMIPENEM; MEROPENEM; METALLO BETA LACTAMASE; PENICILLIN G; PIPERACILLIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CATALYSIS; CRYSTAL STRUCTURE; DISULFIDE BOND; DRUG PROTEIN BINDING; ENZYME ACTIVE SITE; ENZYME CONFORMATION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QUANTUM MECHANICS; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BETA-LACTAMASES; BETA-LACTAMS; BINDING SITES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

EID: 84864378897     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00448-12     Document Type: Article

References (63)

1. Amara P, Field MJ. 2003. Evaluation of an ab initio quantum mechanical/molecular mechanical hybrid-potential link-atom method. Theor. Chem. Acc. 109:43-52. (Pubitemid 36299366)
2. Bebrone C. 2007. Metallo-β-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily. Biochem. Pharmacol. 74:1686-1701.
3. Bebrone C, et al. 2010. Current challenges in antimicrobial chemotherapy: focus on β-lactamase inhibition. Drugs 70:651-679.
4. Borra PS, et al. 2011. Structural and computational investigations of VIM-7: insights into the substrate specificity of VIM metallo-β-lactamases. J. Mol. Biol. 411:174-189.
5. 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.
6. Bush K. 2010. Bench-to-bedside review: the role of β-lactamases in antibiotic-resistant Gram-negative infections. Crit. Care 14:224.
7. Bush K, Fisher JF. 2011. Epidemiological expansion, structural studies and clinical challenges of new β-lactamases from Gram-negative bacteria. Annu. Rev. Microbiol. 65:455-478.
8. Buynak JD, et al. 2004. Penicillin-derived inhibitors that simultaneously target both metallo- and serine-β-lactamases. Bioorg. Med. Chem. Lett. 14:1299-1304. (Pubitemid 38229875)
9. 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.
10. Cohen SX, et al. 2008. ARP/wARP and molecular replacement: the next generation. Acta Crystallogr. D Biol. Crystallogr. 64:49-60.
11. Collaborative Computational Project-4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
12. Concha NO, et al. 2000. Crystal structure of the IMP-1 metallo β-lactamase from Pseudomonas aeruginosa and its complex with a mercaptocarboxylate inhibitor: binding determinants of a potent, broad-spectrum inhibitor. Biochemistry 39:4288-4298. (Pubitemid 30212644)
13. Concha NO, Rasmussen BA, Bush K, Herzberg O. 1996. Crystal structure of the wide-spectrum binuclear zinc β-lactamase from Bacteroides fragilis. Structure 4:823-836. (Pubitemid 26312366)
14. Crisp J, et al. 2007. Structural basis for the role of Asp-120 in metallo-β-lactamases. Biochemistry 46:10664-10674. (Pubitemid 47417259)
15. Docquier JD, et al. 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.
16. Docquier JD, et al. 2003. On functional and structural heterogeneity of VIM-type metallo-β-lactamases. J. Antimicrob. Chemother. 51:257-266.
17. Dunietz BD, et al. 2000. Large scale ab initio quantum chemical calculation of the intermediates in the soluble methane monooxygenase catalytic cycle. J. Am. Chem. Soc. 122:2828-2839. (Pubitemid 30191043)
18. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132. (Pubitemid 41742764)
19. Felici A, et al. 1993. An overview of the kinetic parameters of class B β-lactamases. Biochem. J. 291(Pt. 1):151-155. (Pubitemid 23107763)
20. Garau G, et al. 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. (Pubitemid 39600934)
21. Garau G, et al. 2004. Update of the standard numbering scheme for class B β-lactamases. Antimicrob. Agents Chemother. 48:2347-2349. (Pubitemid 38823395)
22. García-Saez I, et al. 2003. The 1.5-Å structure of Chryseobacterium meningosepticum zinc β-lactamase in complex with the inhibitor, Dcaptopril. J. Biol. Chem. 278:23868-23873. (Pubitemid 36830213)
23. García-Sáez I, et al. 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. (Pubitemid 36268689)
24. Garman EF. 2010. Radiation damage in macromolecular crystallography: what is it and why should we care? Acta Crystallogr. D Biol. Crystallogr. 66:339-351.
25. Garrity JD, Pauff JM, Crowder MW. 2004. Probing the dynamics of a mobile loop above the active site of L1, a metallo-β-lactamase from Stenotrophomonas maltophilia, via site-directed mutagenesis and stoppedflow fluorescence spectroscopy. J. Biol. Chem. 279:39663-39670. (Pubitemid 39258234)
26. Gouet P, Courcelle E, Stuart DI, Metoz F. 1999. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15:305-308. (Pubitemid 29213756)
27. Hay PJ, Wadt WR. 1985. Ab initio effective core potentials for molecular calculations. Potentials for K to Au including the outermost core orbitals. J. Chem. Phys. 82:299-310.
28. Huntley JJ, Fast W, Benkovic SJ, Wright PE, Dyson HJ. 2003. Role of a solvent-exposed tryptophan in the recognition and binding of antibiotic substrates for a metallo-β-lactamase. Protein Sci. 12:1368-1375. (Pubitemid 36759341)
29. Jones G, Willett P, Glen RC. 1995. Molecular recognition of receptor sites using a genetic algorithm with a description of desolvation. J. Mol. Biol. 245:43-53.
30. Jorgensen WL, Maxwell DS, Tirado-Rives J. 1996. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118:11225-11236. (Pubitemid 26399746)
31. Kabsch W. 1993. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallog. 24:795-800.
32. Kaminskaia NV, Spingler B, Lippard SJ. 2001. Intermediate in β-lactam hydrolysis catalyzed by a dinuclear zinc(II) complex: relevance to the mechanism of metallo-β-lactamase. J. Am. Chem. Soc. 123:6555-6563. (Pubitemid 32923023)
33. Lassaux P, et al. 2010. Mercaptophosphonate compounds as broadspectrum inhibitors of the metallo-β-lactamases. J. Med. Chem. 53:4862-4876.
34. Leiros H-KS, McSweeney SM, Smalås AO. 2001. Atomic resolution structures of trypsin provide insight into structural radiation damage. Acta Crystallogr. D 57:488-497. (Pubitemid 32296025)
35. 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.
36. Liénard BM, et al. 2008. Structural basis for the broad-spectrum inhibition of metallo-β-lactamases by thiols. Org. Biomol. Chem. 6:2282-2294. (Pubitemid 351852832)
37. Maltezou HC. 2009. Metallo-β-lactamases in Gram-negative bacteria: introducing the era of pan-resistance? Int. J. Antimicrob. Agents 33:405.e1-405.e7.
38. McCoy AJ, et al. 2007. Phaser crystallographic software. J. Appl. Crystallogr. 40:658-674. (Pubitemid 47080256)
39. Mercuri PS, et al. 2001. Biochemical characterization of the FEZ-1 metallo-β-lactamase of Legionella gormanii ATCC 33297T produced in Escherichia coli. Antimicrob. Agents Chemother. 45:1254-1262. (Pubitemid 32231009)
40. Mercuri PS, et al. 2004. Probing the specificity of the subclass B3 FEZ-1 metallo-β-lactamase by site-directed mutagenesis. J. Biol. Chem. 279:33630-33638. (Pubitemid 39063012)
41. Moali C, et al. 2003. Analysis of the importance of the metallo-β-lactamase active site loop in substrate binding and catalysis. Chem. Biol. 10:319-329. (Pubitemid 36516650)
42. Murshudov GN, Vagin AA, Lebedev A, Wilson KS, Dodson EJ. 1999. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. D Biol. Crystallogr. 55:247-255. (Pubitemid 29053823)
43. Nauton L, Kahn R, Garau G, Hernandez JF, Dideberg O. 2008. Structural insights into the design of inhibitors for the L1 metallo-β-lactamase from Stenotrophomonas maltophilia. J. Mol. Biol. 375:257-269. (Pubitemid 350167435)
44. Page MI, Badarau A. 2008. The mechanisms of catalysis by metallo β-lactamases. Bioinorg. Chem. Appl. 2008:576297. doi:10.1155/2008/576297.
45. Rasmussen BA, Bush K. 1997. Carbapenem-hydrolyzing β-lactamases. Antimicrob. Agents Chemother. 41:223-232.
46. 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. (Pubitemid 36183645)
47. Ravelli RB, McSweeney SM. 2000. The 'fingerprint' that X-rays can leave on structures. Structure 8:315-328. (Pubitemid 30148697)
48. Rocchia W, et al. 2002. Rapid grid-based construction of the molecular surface and the use of induced surface charge to calculate reaction field energies: applications to the molecular systems and geometric objects. J. Comput. Chem. 23:128-137. (Pubitemid 34063137)
49. 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.
50. Schmidt A, Jelsch C, Østergaard P, Rypniewski W, Lamzin VS. 2003. Trypsin revisited: crystallography AT (SUB) atomic resolution and quantum chemistry revealing details of catalysis. J. Biol. Chem. 278:43357-43362. (Pubitemid 37345957)
51. Siezen RJ, Leunissen JA. 1997. Subtilases: the superfamily of subtilisinlike serine proteases. Protein Sci. 6:501-523. (Pubitemid 27120048)
52. Simm AM, et al. 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. (Pubitemid 34952006)
53. Spencer J, et al. 2005. Antibiotic recognition by binuclear metallo-β-lactamases revealed by X-ray crystallography. J. Am. Chem. Soc. 127:14439-14444. (Pubitemid 41457603)
54. 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. (Pubitemid 43807514)
55. Tioni MF, et al. 2008. Trapping and characterization of a reaction intermediate in carbapenem hydrolysis by B. cereus metallo-β-lactamase. J. Am. Chem. Soc. 130:15852-15863.
56. Ullah JH, et al. 1998. The crystal structure of the L1 metallo-β-lactamase from Stenotrophomonas maltophilia at 1.7 Å resolution. J. Mol. Biol. 284:125-136. (Pubitemid 28524001)
57. Wachino J, et al. 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.
58. Walsh TR. 2010. Emerging carbapenemases: a global perspective. Int. J. Antimicrob. Agents 36S. 3:S8-S14.
59. Walsh TR, Toleman MA, Poirel L, Nordmann P. 2005. Metallo-β- lactamases: the quiet before the storm? Clin. Microbiol. Rev. 18:306-325.
60. Wang Z, Fast W, Benkovic SJ. 1999. On the mechanism of the metallo-β-lactamase from Bacteroides fragilis. Biochemistry 38:10013-10023.
61. Wright GD. 2007. The antibiotic resistome: the nexus of chemical and genetic diversity. Nat. Rev. Microbiol. 5:175-186. (Pubitemid 46291277)
62. Yamaguchi Y, et al. 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. (Pubitemid 350309101)
63. Yong D, et al. A novel sub-group metallo-β-lactamase (MBL), AIM-1 emerges in Pseudomonas aeruginosa from Australia. Antimicrob. Agents Chemother., in press.