Host-Specific Enzyme-Substrate Interactions in SPM-1 Metallo-β-Lactamase Are Modulated by Second Sphere Residues

PLoS Pathogens

Volumn 10, Issue 1, 2014, Pages

  González, Lisandro J ^a   Moreno, Diego M ^b   Bonomo, Robert A ^c   Vila, Alejandro J ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^b Universidad Nacional de Rosario   (Argentina)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE; BETA-LACTAMASE SPM-1, PSEUDOMONAS AERUGINOSA;

ANIMAL; ANTIBIOTIC RESISTANCE; CHEMISTRY; CYTOPLASM; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; RABBIT;

ANIMALS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; CATALYTIC DOMAIN; ENZYME STABILITY; MUTATION; PERIPLASM; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RABBITS; SUBSTRATE SPECIFICITY;

EID: 84893809221     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003817     Document Type: Article

References (46)

1. Llarrull LI, Testero SA, Fisher JF, Mobashery S, (2010) The future of the β-lactams. Curr Opin Microbiol 13: 551-557.
2. Fisher JF, Meroueh SO, Mobashery S, (2005) Bacterial resistance to β-lactam antibiotics: compelling opportunism, compelling opportunity. Chem Rev 105: 395-424.
3. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, et al. (2009) Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis 48: 1-12.
4. Helfand MS, Bonomo RA, (2003) β-Lactamases: a survey of protein diversity. Curr Drug Targets Infect Disord 3: 9-23.
5. Walsh TR, Toleman MA, Poirel L, Nordmann P, (2005) Metallo-β-lactamases: the quiet before the storm? Clin Microbiol Rev 18: 306-325.
6. Crowder MW, Spencer J, Vila AJ, (2006) Metallo-β-lactamases: novel weaponry for antibiotic resistance in bacteria. Acc Chem Res 39: 721-728.
7. Palzkill T, (2013) Metallo-β-lactamase structure and function. Ann N Y Acad Sci 1277: 91-104.
8. Nordmann P, Poirel L, Toleman MA, Walsh TR, (2011) Does broad-spectrum β-lactam resistance due to NDM-1 herald the end of the antibiotic era for treatment of infections caused by Gram-negative bacteria? J Antimicrob Chemother 66: 689-692.
9. Bebrone C, (2007) Metallo-β-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily. Biochem Pharmacol 74: 1686-1701.
10. Rasia RM, Vila AJ, (2004) Structural determinants of substrate binding to Bacillus cereus metallo-β-lactamase. J Biol Chem 279: 26046-26051.
11. Strateva T, Yordanov D, (2009) Pseudomonas aeruginosa- a phenomenon of bacterial resistance. J Med Microbiol 58: 1133-1148.
12. Sader HS, Reis AO, Silbert S, Gales AC, (2005) IMPs, VIMs and SPMs: the diversity of metallo-β-lactamases produced by carbapenem-resistant Pseudomonas aeruginosa in a Brazilian hospital. Clin Microbiol Infect 11: 73-76.
13. Toleman MA, Simm AM, Murphy TA, Gales AC, Biedenbach DJ, et al. (2002) Molecular characterization of SPM-1, a novel metallo-β-lactamase isolated in Latin America: report from the SENTRY antimicrobial surveillance programme. J Antimicrob Chemother 50: 673-679.
14. Gales AC, Menezes LC, Silbert S, Sader HS, (2003) Dissemination in distinct Brazilian regions of an epidemic carbapenem-resistant Pseudomonas aeruginosa producing SPM metallo-β-lactamase. J Antimicrob Chemother 52: 699-702.
15. Murphy TA, Simm AM, Toleman MA, Jones RN, Walsh TR, (2003) Biochemical Characterization of the Acquired Metallo-β-Lactamase SPM-1 from Pseudomonas aeruginosa. Antimicrobial Agents in Chemotherapy 47: 582-587.
16. Nouer SA, Nucci M, de Oliveira MP, Pellegrino FL, Moreira BM, (2005) Risk factors for acquisition of multidrug-resistant Pseudomonas aeruginosa producing SPM metallo-β-lactamase. Antimicrobial Agents in Chemotherapy 49: 3663-3667.
17. Silva FM, Carmo MS, Silbert S, Gales AC, (2011) SPM-1-producing Pseudomonas aeruginosa: analysis of the ancestor relationship using multilocus sequence typing, pulsed-field gel electrophoresis, and automated ribotyping. Microb Drug Resist 17: 215-220.
18. Salabi AE, Toleman MA, Weeks J, Bruderer T, Frei R, et al. (2010) First report of the metallo-β-lactamase SPM-1 in Europe. Antimicrob Agents Chemother 54: 582.
19. Murphy TA, Catto LE, Halford SE, Hadfield AT, Minor W, et al. (2006) Crystal structure of Pseudomonas aeruginosa SPM-1 provides insights into variable zinc affinity of metallo-β-lactamases. J Mol Biol 357: 890-903.
20. Hood MI, Skaar EP, (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10: 525-537.
21. Hood MI, Mortensen BL, Moore JL, Zhang Y, Kehl-Fie TE, et al. (2012) Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin-mediated zinc sequestration. PLoS Pathog 8: e1003068.
22. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, et al. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
23. 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.
24. Materon IC, Palzkill T, (2001) Identification of residues critical for metallo-β-lactamase function by codon randomization and selection. Protein Sci 10: 2556-2565.
25. Shin KS, Son BR, Hong SB, Kim J, (2008) Dipicolinic acid-based disk methods for detection of metallo-β-lactamase-producing Pseudomonas spp. and Acinetobacter spp. Diagn Microbiol Infect Dis 62: 102-105.
26. Poirel L, Magalhaes M, Lopes M, Nordmann P, (2004) Molecular Analysis of Metallo-β-Lactamase Gene blaSPM-1-Surrounding Sequences from Disseminated Pseudomonas aeruginosa Isolates in Recife, Brazil. Antimicrob Agents Chemother 48: 1406-1409.
27. Moran-Barrio J, Limansky AS, Viale AM, (2009) Secretion of GOB metallo-β-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 53: 2908-2917.
28. Gonzalez JM, Meini MR, Tomatis PE, Medrano Martin FJ, Cricco JA, et al. (2012) Metallo-β-lactamases withstand low Zn(II) conditions by tuning metal-ligand interactions. Nat Chem Biol 8: 698-700.
29. Nordmann P, Gniadkowski M, Giske CG, Poirel L, Woodford N, et al. (2012) Identification and screening of carbapenemase-producing Enterobacteriaceae. Clin Microbiol Infect 18: 432-438.
30. Lancaster KM (2012) Biological Outer-Sphere Coordination. In: Mingos DMP, Day P, Dahl JP, editors. Molecular Electronic Structures of Transition Metal Complexes I. Structure and Bonding: Springer Berlin Heidelberg. pp. 119-153.
31. Tomatis PE, Rasia RM, Segovia L, Vila AJ, (2005) Mimicking natural evolution in metallo-β-lactamases through second-shell ligand mutations. Proc Natl Acad Sci U S A 102: 13761-13766.
32. Tomatis PE, Fabiane SM, Simona F, Carloni P, Sutton BJ, et al. (2008) Adaptive protein evolution grants organismal fitness by improving catalysis and flexibility. Proc Natl Acad Sci U S A 105: 20605-20610.
33. Oelschlaeger P, Mayo SL, (2005) Hydroxyl groups in the ββ sandwich of metallo-β-lactamases favor enzyme activity: a computational protein design study. J Mol Biol 350: 395-401.
34. Oelschlaeger P, (2008) Outsmarting metallo-β-lactamases by mimicking their natural evolution. J Inorg Biochem 102: 2043-2051.
35. Garau G, Garcia-Saez I, Bebrone C, Anne C, Mercuri P, et al. (2004) Update of the standard numbering scheme for class B β-lactamases. Antimicrobial Agents in Chemotherapy 48: 2347-2349.
36. Patel G, Bonomo RA, (2013) "Stormy waters ahead": global emergence of carbapenemases. Front Microbiol 4: 48.
37. Choi KH, Kumar A, Schweizer HP, (2006) A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 64: 391-397.
38. Marchiaro P, Mussi MA, Ballerini V, Pasteran F, Viale AM, et al. (2005) Sensitive EDTA-based microbiological assays for detection of metallo-β-lactamases in nonfermentative gram-negative bacteria. J Clin Microbiol 43: 5648-5652.
39. Jensch T, Fricke B, (1997) Localization of alanyl aminopeptidase and leucyl aminopeptidase in cells of Pseudomonas aeruginosa by application of different methods for periplasm release. J Basic Microbiol 37: 115-128.
40. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
41. Case DADT, Cheatham III TE, Simmerling CL, Wang J, et al. (2010) AMBER 11. University of California, San Francisco (San Francisco).
42. Fabiane SM, Sohi MK, Wan T, Payne DJ, Bateson JH, et al. (1998) Crystal structure of the zinc-dependent β-lactamase from Bacillus cereus at 1.9 A resolution: binuclear active site with features of a mononuclear enzime. Biochemistry 37: 12404-12411.
43. Jorgensen WLCJ, Madura JD, Impey RW, Klein ML, (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926-935.
44. Brock A, Luty IGT, van Gunsteren Wilfred F, (1995) Lattice-sum methods for calculating electrostatic interactions in molecular simulations. J Chem Phys 103: 3014-3022.
45. Ryckaert GC, H.J.C Berendsen, (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. Journal of Computational Physics 23: 327-341.
46. Suarez D, Brothers EN, Merz KM Jr, (2002) Insights into the structure and dynamics of the dinuclear zinc β-lactamase site from Bacteroides fragilis. Biochemistry 41: 6615-6630.