Elucidating the role of residue 67 in IMP-type metallo-β-lactamase evolution

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 12, 2015, Pages 7299-7307

  LaCuran, Alecander E ^a   Pegg, Kevin M ^b   Liu, Eleanor M ^a   Bethel, Christopher R ^c   Ai, Ni ^d   Welsh, William J ^e,f   Bonomo, Robert A ^c,g   Oelschlaeger, Peter ^a  

^a WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^b CALIFORNIA STATE POLYTECHNIC UNIVERSITY   (United States)

^c LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^d ZHEJIANG UNIVERSITY   (China)

^e RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^f RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMPICILLIN; AZTREONAM; BETA LACTAM ANTIBIOTIC; CEFALOTIN; CEFOTAXIME; CEFOXITIN; CEFTAZIDIME; CHLORAMPHENICOL; CHROMACEF; DORIPENEM; IMIPENEM; IMIPENEMASE 1; IMIPENEMASE 1 V671; IMIPENEMASE 1 V67A; IMIPENEMASE 10; ISOLEUCINE; KANAMYCIN; MEROPENEM; METALLO BETA LACTAMASE; METHYL GROUP; PENICILLIN DERIVATIVE; PENICILLIN G; PHENYLALANINE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; VALINE; BETA LACTAM; BETA LACTAMASE; BETA-LACTAMASE IMP-1; RECOMBINANT PROTEIN;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; BINDING AFFINITY; BIOCHEMISTRY; BIOPHYSICS; CATALYTIC EFFICIENCY; CIRCULAR DICHROISM; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DENATURATION; ELECTROSPRAY MASS SPECTROMETRY; ESCHERICHIA COLI; HYDROLYSIS; IMMUNOBLOTTING; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR DOCKING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; STATIC ELECTRICITY; THERMAL DENATURATION; WILD TYPE; CHEMISTRY; CLASSIFICATION; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION; GENETICS; KINETICS; METABOLISM; MICROBIAL SENSITIVITY TEST; MOLECULAR EVOLUTION; MUTATION; STRUCTURE ACTIVITY RELATION;

AMINO ACID SUBSTITUTION; BETA-LACTAMASES; BETA-LACTAMS; CATALYTIC DOMAIN; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; GENE EXPRESSION; HYDROLYSIS; KINETICS; MICROBIAL SENSITIVITY TESTS; MOLECULAR DOCKING SIMULATION; MUTATION; PHENYLALANINE; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; VALINE;

EID: 84954482366     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01651-15     Document Type: Article

References (59)

1. 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.
2. 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.
3. Oelschlaeger P, Mayo SL, Pleiss J. 2005. Impact of remote mutations on metallo-β-lactamase substrate specificity: implications for the evolution of antibiotic resistance. Protein Sci 14:765-774. http://dx.doi.org/10.1110 /ps.041093405.
4. Zhao WH, Hu ZQ. 2011. IMP-type metallo-β-lactamases in Gramnegative bacilli: distribution, phylogeny, and association with integrons. Crit Rev Microbiol 37:214-226. http://dx.doi.org/10.3109/1040841X.2011.559944.
5. Chouchani C, Marrakchi R, Henriques I, Correia A. 2013. Occurrence of IMP-8, IMP-10, and IMP-13 metallo-β-lactamases located on class 1 integrons and other extended-spectrum β-lactamases in bacterial isolates from Tunisian rivers. Scand J Infect Dis 45:95-103. http://dx.doi.org/10.3109/00365548.2012.717712.
6. Galleni M, Lamotte-Brasseur J, Rossolini GM, Spencer J, Dideberg O, Frere JM, Metallo-β-Lactamases Working Group. 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.
7. 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. http://dx.doi.org/10.1128/AAC.48.7.2347-2349.2004.
8. Bush K. 2010. Alarming β-lactamase-mediated resistance in multidrugresistant Enterobacteriaceae. Curr Opin Microbiol 13:558-564. http://dx.doi.org/10.1016/j.mib.2010.09.006.
9. Cornaglia G, Giamarellou H, Rossolini GM. 2011. Metallo-β-lactamases: a last frontier for β-lactams? Lancet Infect Dis 11:381-393. http://dx.doi.org/10.1016/S1473-3099(11)70056-1.
10. Miriagou V, Cornaglia G, Edelstein M, Galani I, Giske CG, Gniadkowski M, Malamou-Lada E, Martinez-Martinez L, Navarro F, Nordmann P, Peixe L, Pournaras S, Rossolini GM, Tsakris A, Vatopoulos A, Canton R. 2010. Acquired carbapenemases in Gram-negative bacterial pathogens: detection and surveillance issues. Clin Microbiol Infect 16: 112-122. http://dx.doi.org/10.1111/j.1469-0691.2009.03116.x.
11. Oelschlaeger P, Ai N, Duprez KT, Welsh WJ, Toney JH. 2010. Evolving carbapenemases: can medicinal chemists advance one step ahead of the coming storm? J Med Chem 53:3013-3027. http://dx.doi.org/10.1021 /jm9012938.
12. 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. http://dx.doi.org/10.1146/annurev-micro-090110-102911.
13. Bush K, Palzkill TG, Jacoby GA. 2015. β-Lactamase classification and amino acid sequences for TEM, SHV and OXA extended-spectrum and inhibitor resistant enzymes. Lahey Clinic, Burlington, MA. http://www.lahey.org/studies/other.asp-table1. Accessed 6 July 2015.
14. Osano E, Arakawa Y, Wacharotayankun R, Ohta M, Horii T, Ito H, Yoshimura F, Kato N. 1994. Molecular characterization of an enterobacterial metallo-β-lactamase found in a clinical isolate of Serratia marcescens that shows imipenem resistance. Antimicrob Agents Chemother 38:71-78. http://dx.doi.org/10.1128/AAC.38.1.71.
15. Watanabe M, Iyobe S, Inoue M, Mitsuhashi S. 1991. Transferable imipenem resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 35:147-151. http://dx.doi.org/10.1128/AAC.35.1.147.
16. Koh TH, Babini GS, Woodford N, Sng LH, Hall LM, Livermore DM. 1999. Carbapenem-hydrolysing IMP-1 β-lactamase in Klebsiella pneumoniae from Singapore. Lancet 353:2162. http://dx.doi.org/10.1016 /S0140-6736(05)75604-X.
17. Jones RN, Deshpande LM, Bell JM, Turnidge JD, Kohno S, Hirakata Y, Ono Y, Miyazawa Y, Kawakama S, Inoue M, Hirata Y, Toleman MA. 2004. Evaluation of the contemporary occurrence rates of metallo-β-lactamases in multidrug-resistant Gram-negative bacilli in Japan: report from the SENTRY Antimicrobial Surveillance Program (1998-2002). Diagn Microbiol Infect Dis 49:289-294. http://dx.doi.org/10.1016/j.diagmicrobio.2004.04.007.
18. Shibata N, Doi Y, Yamane K, Yagi T, Kurokawa H, Shibayama K, Kato H, Kai K, Arakawa Y. 2003. PCR typing of genetic determinants for metallo-β-lactamases and integrases carried by gram-negative bacteria isolated in Japan, with focus on the class 3 integron. J Clin Microbiol 41:5407-5413. http://dx.doi.org/10.1128/JCM.41.12.5407-5413.2003.
19. Iyobe S, Kusadokoro H, Takahashi A, Yomoda S, Okubo T, Nakamura A, O'Hara K. 2002. Detection of a variant metallo-β-lactamase, IMP-10, from two unrelated strains of Pseudomonas aeruginosa and an Alcaligenes xylosoxidans strain. Antimicrob Agents Chemother 46:2014-2016. http: //dx.doi.org/10.1128/AAC.46.6.2014-2016.2002.
20. Koh TH, Khoo CT, Tan TT, Arshad MA, Ang LP, Lau LJ, Hsu LY, Ooi EE. 2010. Multilocus sequence types of carbapenem-resistant Pseudomonas aeruginosa in Singapore carrying metallo-β-lactamase genes, including the novel bla(IMP-26) gene. J Clin Microbiol 48:2563-2564. http://dx.doi.org/10.1128/JCM.01905-09.
21. Tada T, Miyoshi-Akiyama T, Shimada K, Shimojima M, Kirikae T. 2013. IMP-43 and IMP-44 metallo-β-lactamases with increased carbapenemase activities in multidrug-resistant Pseudomonas aeruginosa. Antimicrob Agents Chemother 57:4427-4432. http://dx.doi.org/10.1128 /AAC.00716-13.
22. Meini MR, Llarrull LI, Vila AJ. 2014. Evolution of metallo-β-lactamases: trends revealed by natural diversity and evolution. Antibiotics (Basel) 3:285-316. http://dx.doi.org/10.3390/antibiotics3030285.
23. Concha NO, Janson CA, Rowling P, Pearson S, Cheever CA, Clarke BP, Lewis C, Galleni M, Frere JM, Payne DJ, Bateson JH, Abdel-Meguid SS. 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. http://dx.doi.org/10.1021/bi992569m.
24. Scrofani SD, Chung J, Huntley JJ, Benkovic SJ, Wright PE, Dyson HJ. 1999. NMR characterization of the metallo-β-lactamase from Bacteroides fragilis and its interaction with a tight-binding inhibitor: role of an active-site loop. Biochemistry 38:14507-14514. http://dx.doi.org /10.1021/bi990986t.
25. Moali C, Anne C, Lamotte-Brasseur J, Groslambert S, Devreese B, Van Beeumen J, Galleni M, Frere JM. 2003. Analysis of the importance of the metallo-β-lactamase active site loop in substrate binding and catalysis. Chem Biol 10:319-329. http://dx.doi.org/10.1016/S1074-5521(03)00070-X.
26. Pegg KM, Liu EM, Lacuran AE, Oelschlaeger P. 2013. Biochemical characterization of IMP-30, a metallo-β-lactamase with enhanced activity toward ceftazidime. Antimicrob Agents Chemother 57:5122-5126. http: //dx.doi.org/10.1128/AAC.02341-12.
27. 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. http://dx.doi.org/10.1016/j.jmb.2004.09.074.
28. Pal A, Tripathi A. 2013. An in silico approach for understanding the molecular evolution of clinically important metallo-β-lactamases. Infect Genet Evol 20:39-47. http://dx.doi.org/10.1016/j.meegid.2013.07.028.
29. 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. http://dx.doi.org/10.1021/jm701031n.
30. Xiong J, Hynes MF, Ye H, Chen H, Yang Y, M'Zali F, Hawkey PM. 2006. bla(IMP-9) and its association with large plasmids carried by Pseudomonas aeruginosa isolates from the People's Republic of China. Antimicrob Agents Chemother 50:355-358. http://dx.doi.org/10.1128/AAC.50.1.355-358.2006.
31. Pournaras S, Kock R, Mossialos D, Mellmann A, Sakellaris V, Stathopoulos C, Friedrich AW, Tsakris A. 2013. Detection of a phylogenetically distinct IMP-type metallo-β-lactamase, IMP-35, in a CC235 Pseudomonas aeruginosa from the Dutch-German border region (Euregio). J Antimicrob Chemother 68:1271-1276. http://dx.doi.org/10.1093/jac/dkt004.
32. Wang Y, Wang X, Schwarz S, Zhang R, Lei L, Liu X, Lin D, Shen J. 2014. IMP-45-producing multidrug-resistant Pseudomonas aeruginosa of canine origin. J Antimicrob Chemother 69:2579-2581. http://dx.doi.org /10.1093/jac/dku133.
33. Liu EM, Pegg KM, Oelschlaeger P. 2012. 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 56:6403-6406. http://dx.doi.org/10.1128/AAC.01440-12.
34. Hunt JB, Neece SH, Ginsburg A. 1985. The use of 4-(2-pyridylazo)resorcinol in studies of zinc release from Escherichia coli aspartate transcarbamoylase. Anal Biochem 146:150-157. http://dx.doi.org/10.1016/0003-2697(85)90409-9.
35. Fast W, Wang Z, Benkovic SJ. 2001. Familial mutations and zinc stoichiometry determine the rate-limiting step of nitrocefin hydrolysis by metallo-β-lactamase from Bacteroides fragilis. Biochemistry 40:1640-1650. http://dx.doi.org/10.1021/bi001860v.
36. Tremblay LW, Fan F, Blanchard JS. 2010. Biochemical and structural characterization of Mycobacterium tuberculosis β-lactamase with the carbapenems ertapenem and doripenem. Biochemistry 49:3766-3773. http: //dx.doi.org/10.1021/bi100232q.
37. Clinical and Laboratory Standards Institute. 2012. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard, ninth edition. M07-A9. Clinical and Laboratory Standards Institute, Wayne, PA.
38. Pegg KM, Liu EM, George AC, LaCuran AE, Bethel CR, Bonomo RA, Oelschlaeger P. 2014. Understanding the determinants of substrate specificity in IMP family metallo-β-lactamases: the importance of residue 262. Protein Sci 23:1451-1460. http://dx.doi.org/10.1002/pro.2530.
39. Zauhar RJ, Moyna G, Tian L, Li Z, Welsh WJ. 2003. Shape signatures: a new approach to computer-aided ligand-and receptor-based drug design. J Med Chem 46:5674-5690. http://dx.doi.org/10.1021/jm030242k.
40. Dewar MJS, Zoebisch EG, Healy EF, Stewart JJP. 1985. The development and use of quantum-mechanical molecular models. 76. AM1: a new general-purpose quantum-mechanical molecular model. J Am Chem Soc 107:3902-3909. http://dx.doi.org/10.1021/Ja00299a024
41. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, Olson AJ. 1998. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem 19:1639-1662. http://dx.doi.org/10.1002/(SICI)1096-987X(19981115)19:14-1639::AID-JCC10-3.0.CO;2-B.
42. Irwin JJ, Raushel FM, Shoichet BK. 2005. Virtual screening against metalloenzymes for inhibitors and substrates. Biochemistry 44:12316-12328. http://dx.doi.org/10.1021/bi050801k.
43. Stote RH, Karplus M. 1995. Zinc binding in proteins and solution: a simple but accurate nonbonded representation. Proteins 23:12-31. http: //dx.doi.org/10.1002/prot.340230104.
44. Carfi A, Pares S, Duee E, Galleni M, Duez C, Frere JM, Dideberg O. 1995. The 3-D structure of a zinc metallo-β-lactamase from Bacillus cereus reveals a new type of protein fold. EMBO J 14:4914-4921.
45. 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. http://dx.doi.org/10.1016/j.jmb.2005.04.044.
46. Whitmore L, Wallace BA. 2004. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32:W668-W673. http://dx.doi.org/10.1093 /nar/gkh371.
47. Whitmore L, Wallace BA. 2008. Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89:392-400. http://dx.doi.org/10.1002/bip.20853.
48. Compton LA, Johnson WC, Jr. 1986. Analysis of protein circular dichroism spectra for secondary structure using a simple matrix multiplication. Anal Biochem 155:155-167. http://dx.doi.org/10.1016 /0003-2697(86)90241-1.
49. Sreerama N, Woody RW. 2000. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287:252-260. http://dx.doi.org/10.1006/abio.2000.4880.
50. Bryson JW, Betz SF, Lu HS, Suich DJ, Zhou HX, O'Neil KT, DeGrado WF. 1995. Protein design: a hierarchic approach. Science 270:935-941. http://dx.doi.org/10.1126/science.270.5238.935.
51. Meiler J, Mueller M, Zeidler A, Schmaeschke F. 2001. Generation and evaluation of dimension-reduced amino acid parameter representations by artificial neural networks. J Mol Model 7:360-369. http://dx.doi.org/10.1007/s008940100038.
52. Widmann M, Pleiss J, Oelschlaeger P. 2012. Systematic analysis of metallo-β-lactamases using an automated database. Antimicrob Agents Chemother 56:3481-3491. http://dx.doi.org/10.1128/AAC.00255-12.
53. Bebrone C, Anne C, Kerff F, Garau G, De Vriendt K, Lantin R, Devreese B, Van Beeumen J, Dideberg O, Frere JM, Galleni M. 2008. Mutational analysis of the zinc-and substrate-binding sites in the CphA metallo-β-lactamase from Aeromonas hydrophila. Biochem J 414:151-159. http://dx.doi.org/10.1042/BJ20080375.
54. King DT, Worrall LJ, Gruninger R, Strynadka NC. 2012. New Delhi metallo-β-lactamase: structural insights into β-lactam recognition and inhibition. J Am Chem Soc 134:11362-11365. http://dx.doi.org/10.1021 /ja303579d.
55. Feng H, Ding J, Zhu D, Liu X, Xu X, Zhang Y, Zang S, Wang DC, Liu W. 2014. Structural and mechanistic insights into NDM-1 catalyzed hydrolysis of cephalosporins. J Am Chem Soc 136:14694-14697. http://dx.doi.org/10.1021/ja508388e.
56. Oelschlaeger P, Schmid RD, Pleiss J. 2003. Modeling domino effects in enzymes: molecular basis of the substrate specificity of the bacterial metallo-β-lactamases IMP-1 and IMP-6. Biochemistry 42:8945-8956. http: //dx.doi.org/10.1021/bi0300332.
57. Xiong J, Alexander DC, Ma JH, Deraspe M, Low DE, Jamieson FB, Roy PH. 2013. Complete sequence of pOZ176, a 500-kilobase IncP-2 plasmid encoding IMP-9-mediated carbapenem resistance, from outbreak isolate Pseudomonas aeruginosa 96. Antimicrob Agents Chemother 57:3775-3782. http://dx.doi.org/10.1128/AAC.00423-13.
58. Oelschlaeger P, Toney JH. 13 October 2009. Are human microflora influenced by environmental exposure to antibiotics? Science http://www.sciencemag.org/content/325/5944/1128/reply. Accessed 8 July 2015.
59. Kuemmerer K. 2008. Substance flow associated with medical care - significance of different sources, p 43-59. In Pharmaceuticals in the environment: sources, fate, effects and risks. Springer, Berlin, Germany.