[en] Metallo-β-lactamases, enzymes which inactivate β-lactam
antibiotics, are of increasing biological and clinical significance
as a source of antibiotic resistance in pathogenic bacteria.
In the present study we describe the high-resolution solution
NMR structures of the Bacillus cereus metallo-β-lactamase
BcII and of its complex with R-thiomandelic acid, a broadspectrum
inhibitor of metallo-β-lactamases. This is the first
reported solution structure of any metallo-β-lactamase. There are
differences between the solution structure of the free enzyme
and previously reported crystal structures in the loops flanking
the active site, which are important for substrate and inhibitor
binding and catalysis. The binding of R-thiomandelic acid and
the roles of active-site residues are defined in detail. Changes
in the enzyme structure upon inhibitor binding clarify the role
of the mobile β3–β4 loop. Comparisons with other metallo-β-
lactamases highlight the roles of individual amino-acid residues in
the active site and the β3–β4 loop in inhibitor binding and provide
information on the basis of structure–activity relationships among
metallo-β-lactamase inhibitors.
Disciplines :
Chemistry
Author, co-author :
Karsisiotis, Andreas Ioannis
Damblon, Christian ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie biologique structurale
Roberts, Gordon C K
Language :
English
Title :
Solution structures of the Bacillus cereus metallo-β-lactamase BcII and its complex with the broad spectrum inhibitor R-thiomandelic acid
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Frère, J. M., Dubus, A., Galleni, M., Matagne, A. and Amicosante, G. (1999) Mechanistic diversity of β-lactamases. Biochem. Soc. Trans. 27, 58-63
Bebrone, C. (2007) Metallo-β-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily. Biochem. Pharmacol. 74, 1686-1701
Palzkill, T. (2013) Metallo-β-lactamase structure and function. Ann. N.Y. Acad. Sci. 1277, 91-104
Galleni, M., Lamotte-Brasseur, J., Rossolini, G. M., Spencer, J., Dideberg, O., Frère, J. M. and Metallo-β-Lactamase Working Group (2001) Standard numbering scheme for class B β-lactamases. Antimicrob. Agents Chemother. 45, 660-663
Widmann, M., Pleiss, J. and Oelschlaeger, P. (2012) Systematic analysis of metallo-β-lactamases using an automated database. Antimicrob. Agents Chemother. 56, 3481-3491
Fritsche, T. R., Sader, H. S., Toleman, M. A., Walsh, T. R. and Jones, R. N. (2005) Emerging metallo-β-lactamase-mediated resistances: a summary report from the worldwide SENTRY antimicrobial surveillance program. Clin. Infect. Dis. 41, S276-S278
Cornaglia, G., Giamarellou, H. and Rossolini, G. M. (2011) Metallo-β-lactamases: a last frontier for β-lactams? Lancet Infect. Dis. 11, 381-393
Nordmann, P., Poirel, L., Walsh, T. R. and Livermore, D. M. (2011) The emerging NDM carbapenemases. Trends Microbiol. 19, 588-595
Reference deleted
Daiyasu, H., Osaka, K., Ishino, Y. and Toh, H. (2001) Expansion of the zinc metallo-hydrolase family of the β-lactamase fold. FEBS Lett. 503, 1-6
Drawz, S. M. and Bonomo, R. A. (2010) Three decades of β-lactamase inhibitors. Clin. Microbiol. Rev. 23, 160-201
Toney, J. H. and Moloughney, J. G. (2004) Metallo-β-lactamase inhibitors: promise for the future? Curr. Opin. Invest. Drugs 5, 823-826
Toney, J. H., Cleary, K. A., Hammond, G. G., Yuan, X. L., May, W. J., Hutchins, S. M., Ashton, W. T. and Vanderwall, D. E. (1999) Structure-activity relationships of biphenyl tetrazoles as metallo-β-lactamase inhibitors. Bioorg. Med. Chem. Lett. 9, 2741-2746
Payne, D. J., Hueso-Rodriguez, J. A., Boyd, H., Concha, N. O., Janson, C. A., Gilpin, M., Bateson, J. H., Cheever, C., Niconovich, N. L., Pearson, S. et al. (2002) Identification of a series of tricyclic natural products as potent broad-spectrum inhibitors of metallo-β-lactamases. Antimicrob. Agents Chemother. 46, 1880-1886
Fitzgerald, P. M. D., Wu, J. K. and Toney, J. H. (1998) Unanticipated inhibition of the metallo-β-lactamase from Bacteroides fragilis by 4-morpholineethanesulfonic acid (MES): a crystallographic study at 1.85-Å resolution. Biochemistry 37, 6791-6800
Concha, N. O., Janson, C. A., Rowling, P., Pearson, S., Cheever, C. A., Clarke, B. P., Lewis, C., Galleni, M., Frère, J. M., Payne, D. J. 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
Toney, J. H., Hammond, G. G., Fitzgerald, P. M. D., Sharma, N., Balkovec, J. M., Rouen, G. P., Olson, S. H., Hammond, M. L., Greenlee, M. L. and Gao, Y. D. (2001) Succinic acids as potent inhibitors of plasmid-borne IMP-1 metallo-β-lactamase. J. Biol. Chem. 276, 31913-31918
Kurosaki, H., Yamaguchi, Y., Yasuzawa, H., Jin, W. C., Yamagata, Y. and Arakawa, Y. (2006) Probing, inhibition, and crystallographic characterization of metallo-β-lactamase (IMP-1) with fluorescent agents containing dansyl and thiol groups. ChemMedChem 1, 969-972
Garcia-Saez, I., Hopkins, J., Papamicael, C., Franceschini, N., Amicosante, G., Rossolini, G. M., Galleni, M., Frère, J. M. and Dideberg, O. (2003) The 1.5-Å structure of Chryseobacterium meningosepticum zinc β-lactamase in complex with the inhibitor, D-captopril. J. Biol. Chem. 278, 23868-23873
Líenard, B. M. R., Garau, G., Horsfall, L., Karsisiotis, A. I., Damblon, C., Lassaux, P., Papamicael, C., Roberts, G. C. K., Galleni, M., Dideberg, O. et al. (2008) Structural basis for the broad-spectrum inhibition of metallo-β-lactamases by thiols. Org. Biomol. Chem. 6, 2282-2294
Mollard, C., Moali, C., Papamicael, C., Damblon, C., Vessilier, S., Amicosante, G., Schofield, C. J., Galleni, M., Frère, J. M. and Roberts, G. C. K. (2001) Thiomandelic acid, a broad spectrum inhibitor of zinc β-lactamases-kinetic and spectroscopic studies. J. Biol. Chem. 276, 45015-45023
Siemann, S., Evanoff, D. P., Marrone, L., Clarke, A. J., Viswanatha, T. and Dmitrienko, G. I. (2002) N-arylsulfonyl hydrazones as inhibitors of IMP-1 metallo-β-lactamase. Antimicrob. Agents Chemother. 46, 2450-2457
Lassaux, P., Hamel, M., Gulea, M., Delbruck, H., Mercuri, P. S., Horsfall, L., Dehareng, D., Kupper, M., Frère, J. M., Hoffmann, K. et al. (2010) Mercapto phosphonate compounds as broad-spectrum inhibitors of the metallo-β-lactamases. J. Med. Chem. 53, 4862-4876
Siemann, S., Clarke, A. J., Viswanatha, T. and Dmitrienko, G. I. (2003) Thiols as classical and slow-binding inhibitors of IMP-1 and other binuclear metallo-β-lactamases. Biochemistry 42, 1673-1683
Goto, M., Takahashi, T., Yamashita, F., Koreeda, A., Mori, H., Ohta, M. and Arakawa, Y. (1997) Inhibition of the metallo-β-lactamase produced from Serratia marcescens by thiol compounds. Biol. Pharm. Bull. 20, 1136-1140
Wachino, J., Yamaguchi, Y., Mori, S., Kurosaki, H., Arakawa, Y. and 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
Damblon, C., Jensen, M., Ababou, A., Barsukov, I., Papamicael, C., Schofield, C. J., Olsen, L., Bauer, R. and Roberts, G. C. K. (2003) The inhibitor thiomandelic acid binds to both metal ions in metallo-β-lactamase and induces positive cooperativity in metal binding. J. Biol. Chem. 278, 29240-29251
Toney, J. H., Fitzgerald, P. M. D., Grover-Sharma, N., Olson, S. H., May, W. J., Sundelof, J. G., Vanderwall, D. E., Cleary, K. A., Grant, S. K., Wu, J. K. et al. (1998) Antibiotic sensitization using biphenyl tetrazoles as potent inhibitors of Bacteroides fragilis metallo-β-lactamase. Chem. Biol. 5, 185-196
Huntley, J. J. A., Fast, W., Benkovic, S. J., Wright, P. E. and Dyson, H. J. (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
Moali, C., Anne, C., Lamotte-Brasseur, J., Groslambert, S., Devreese, B., Van Beeumen, J., Galleni, M. and Frère, J. M. (2003) Analysis of the importance of the metallo-β-lactamase active site loop in substrate binding and catalysis. Chem. Biol. 10, 319-329
Karsisiotis, A. I., Damblon, C. F. and Roberts, G. C. K. (2013) Complete 1H, 15N and 13C resonance assignments of Bacillus cereus metallo-β- lactamase and its complex with the inhibitor R -thiomandelic acid. Biomol. NMR Assignments, doi:10.1007/s12104-013-9507-1
Marion, D., Kay, L. E., Sparks, S. W., Torchia, D. A. and Bax, A. (1989) 3-Dimensional heteronuclear NMR of N-15-labeled proteins. J. Am. Chem. Soc. 111, 1515-1517
Pascal, S. M., Muhandiram, D. R., Yamazaki, T., Forman-Kay, J. D. and Kay, L. E. (1994) Simultaneous acquisition of N-15-edited and C-13-edited NOE spectra of proteins dissolved in H2O. J. Magn. Reson., Ser. B 103, 197-201
Zuiderweg, E. R. P., McIntosh, L. P., Dahlquist, F. W. and Fesik, S. W. (1990) 3-Dimensional C-13-resolved proton NOE spectroscopy of uniformly C-13-labeled proteins for the NMR assignment and structure determination of larger molecules. J. Magn. Reson. 86, 210-216
Zwahlen, C., Legault, P., Vincent, S. B. F., Greenblatt, J., Konrat, R. and Kay, L. E. (1997) Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage λ N-Peptide/boxB RNA complex. J. Am. Chem. Soc. 119, 6711-6721
Jardetzky, O. and Roberts, G. C. K. (1981) NMR in Molecular Biology. Academic Press, New York
Cheung, H. T. A., Searle, M. S., Feeney, J., Birdsall, B., Roberts, G. C. K., Kompis, I. and Hammond, S. J. (1986) Trimethoprim binding to Lactobacillus casei dihydrofolate reductase: a C-13 NMR-study using selectively C-13-enriched trimethoprim. Biochemistry 25, 1925-1931
Herrmann, T., Guntert, P. and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319, 209-227
Guntert, P. (2004) Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278, 353-378
Reference deleted
Cornilescu, G., Delaglio, F. and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302
Guntert, P. and Wuthrich, K. (1991) Improved efficiency of protein structure calculations from NMR data using the program DIANA with redundant dihedral angle constraints. J. Biomol. NMR 1, 447-456
Laskowski, R. A., Rullmann, J. A. C., MacArthur, M. W., Kaptein, R. and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486
Vriend, G. (1990) WHAT IF: a molecular modeling and drug design program. J. Mol. Graphics 8, 52-56
Koradi, R., Billeter, M. and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55
Carfi, A., Duee, E., Galleni, M., Frère, J. M. and Dideberg, O. (1998) 1.85Å resolution structure of the zinc(II) β-lactamase from Bacillus cereus. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 313-323
Fabiane, S. M., Sohi, M. K., Wan, T., Payne, D. J., Bateson, J. H., Mitchell, T. and Sutton, B. J. (1998) Crystal structure of the zinc-dependent β-lactamase from Bacillus cereus at 1.9Å resolution: binuclear active site with features of a mononuclear enzyme. Biochemistry 37, 12404-12411
Scrofani, S. D. B., Chung, J., Huntley, J. J. A., Benkovic, S. J., Wright, P. E. and Dyson, H. J. (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
Kim, Y., Cunningham, M. A., Mire, J., Tesar, C., Sacchettini, J. and Joachimiak, A. (2013) NDM-1, the ultimate promiscuous enzyme: substrate recognition and catalytic mechanism. FASEB J. 27, 1917-1927
Yamaguchi, Y., Jin, W., Matsunaga, K., Ikemizu, S., Yamagata, Y., Wachino, J. I., Shibata, N., Arakawa, Y. and 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
Huntley, J. J. A., Scrofani, S. D. B., Osborne, M. J., Wright, P. E. and Dyson, H. J. (2000) Dynamics of the metallo-β-lactamase from Bacteroides fragilis in the presence and absence of a tight-binding inhibitor. Biochemistry 39, 13356-13364
Leiros, H.-K. S., Borra, P. S., Bransdal, B. O., Edvardsen, K. S. W., Spencer, J., Walsh, T. R. and 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
Greenlee, M. L., Laub, J. B., Balkovec, J. M., Hammond, M. L., Hammond, G. G., Pompliano, D. L. and Epstein-Toney, J. H. (1999) Synthesis and SAR of thioester and thiol inhibitors of IMP-1 metallo-β-lactamase. Bioorg. Med. Chem. Lett. 9, 2549-2554
Garcia-Saez, I., Mercuri, P. S., Papamicael, C., Kahn, R., Frère, J. M., Galleni, M., Rossolini, G. M. and 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
Heinz, U., Bauer, R., Wommer, S., Meyer-Klaucke, W., Papamichaels, C., Bateson, J. and Adolph, H. W. (2003) Coordination geometries of metal ions in D- or L-captopril-inhibited metallo-β-lactamases. J. Biol. Chem. 278, 20659-20666
Bounaga, S., Galleni, M., Laws, A. P. and Page, M. I. (2001) Cysteinyl peptide inhibitors of Bacillus cereus zinc β-lactamase. Bioorg. Med. Chem. 9, 503-510
Sun, Q., Law, A., Crowder, M. W. and Geysen, H. M. (2006) Homo-cysteinyl peptide inhibitors of the L1 metallo-β-lactamase, and SAR as determined by combinatorial library synthesis. Bioorg. Med. Chem. Lett. 16, 5169-5175
Docquier, J. D., Lamotte-Brasseur, J., Galleni, M., Amicosante, G., Frère, J. M. and Rossolini, G. M. (2003) On functional and structural heterogeneity of VIM-type metallo-β-lactamases. J. Antimicrob. Chemother. 51, 257-266
Ullah, J. H., Walsh, T. R., Taylor, I. A., Emery, D. C., Verma, C. S., Gamblin, S. J. and Spencer, J. (1998) The crystal structure of the L1 metallo-β-lactamase from Stenotrophomonas maltophilia at 1.7Å resolution. J. Mol. Biol. 284, 125-136
Nauton, L., Kahn, R., Garau, G., Hernandez, J. F. and 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
Similar publications
Sorry the service is unavailable at the moment. Please try again later.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.