Boric acid and acetate anion binding to subclass B3 metallo-β-lactamase BJP-1 provides clues for mechanism of action and inhibitor design

Di Pisa, F.; Pozzi, C.; Benvenuti, M.; Docquier, Jean-Denis; De Luca, F.; Mangani, S.

doi:10.1016/j.ica.2017.07.030

Article (Scientific journals)

Boric acid and acetate anion binding to subclass B3 metallo-β-lactamase BJP-1 provides clues for mechanism of action and inhibitor design

Di Pisa, F.; Pozzi, C.; Benvenuti, M. et al.

2018 • In Inorganica Chimica Acta, 470, p. 331-341

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/252549

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10.1016/j.ica.2017.07.030

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Keywords :

Antibiotic resistance; Inhibitor; Metallo β-lactamase; Subclass B3; X-ray crystallography; Antibiotics; Boric acid; Crystal atomic structure; Enzymes; Health risks; Molecules; X ray analysis; X rays; Zinc compounds; Bacterial resistance; Lactamases; Microbial infections; Risk to human health; Small molecule inhibitor; X ray crystallography

Abstract :

[en] Microbial infections represent a major risk to human health. In this respect, β-lactam antibiotics constitute a key therapeutic resource against such infections. However, we are facing increasing microbial resistance to antibiotic treatment and particularly worrisome is the emergence of resistant bacterial strains towards β-lactam antibiotics that can rapidly disseminate worldwide. β-lactamase enzymes are the main determinant of bacterial resistance and among them metallo-β-lactamases (MBLs) are most threatening, as exemplified by the recent resistance outbreaks due to New Delhi β-lactamase 1 (NDM-1) producing bacteria. MBLs are mono or di-zinc enzymes able to inactivate clinically important β-lactam antibiotics including carbapenems, which are used as a last resort therapy in severe infections. Under this scenery, the discovery of new potent inhibitors of MBLs becomes an urgent need and X-ray crystallography of MBLs in complex with small molecule inhibitors provides the possibility to accelerate the process of drug discovery. We present here the atomic-resolution crystal structures of BJP-1, a di-zinc MBL, in complex with two small molecules and their comparison with other MBL complexes with inhibitors. These structural data, besides providing hints about the mechanism of di-zinc MBLs, might be the starting point for a fragment-based lead-discovery program. © 2017 Elsevier B.V.

Disciplines :

Biochemistry, biophysics & molecular biology
Microbiology

Author, co-author :

Di Pisa, F.; Department of Biotechnology, Chemistry and Pharmacy, University of Siena, Siena, 53100, Italy

Pozzi, C.; Department of Biotechnology, Chemistry and Pharmacy, University of Siena, Siena, 53100, Italy

Benvenuti, M.; Department of Biotechnology, Chemistry and Pharmacy, University of Siena, Siena, 53100, Italy

Docquier, Jean-Denis ; Université de Liège - ULiège > Département des sciences de la vie > Centre d'ingénierie des protéines

De Luca, F.; Department of Medical Biotechnology, University of Siena53100, Italy

Mangani, S.; Department of Biotechnology, Chemistry and Pharmacy, University of Siena, Siena, 53100, Italy, Magnetic Resonance Center CERM, University of Florence, Sesto Fiorentino (Fi), 50019, Italy

Language :

English

Title :

Boric acid and acetate anion binding to subclass B3 metallo-β-lactamase BJP-1 provides clues for mechanism of action and inhibitor design

Publication date :

2018

Journal title :

Inorganica Chimica Acta

ISSN :

0020-1693

Publisher :

Elsevier S.A.

Volume :

470

Pages :

331-341

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 13 November 2020

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Bibliography

Aitha, M., Marts, A.R., Bergstrom, A., Møller, A.J., Moritz, L., Turner, L., Nix, J.C., Bonomo, R.A., Page, R.C., Tierney, D.L., et al. Biochemical, mechanistic, and spectroscopic characterization of metallo-β-lactamase VIM-2. Biochemistry 53 (2014), 7321–7331.
Babic, M., Hujer, A.M., Bonomo, R.A., What's new in antibiotic resistance? Focus on beta-lactamases. Drug Resist. Updat. Rev. Comment. Antimicrob. Anticancer Chemother. 9 (2006), 142–156.
Bellais, S., Léotard, S., Poirel, L., Naas, T., Nordmann, P., Molecular characterization of a carbapenem-hydrolyzing beta-lactamase from Chryseobacterium (Flavobacterium) indologenes. FEMS Microbiol. Lett. 171 (1999), 127–132.
Benvenuti, M., Mangani, S., Crystallization of soluble proteins in vapor diffusion for x-ray crystallography. Nat. Protoc. 2 (2007), 1633–1651.
Brem, J., Cain, R., Cahill, S., McDonough, M.A., Clifton, I.J., Jiménez-Castellanos, J.-C., Avison, M.B., Spencer, J., Fishwick, C.W.G., Schofield, C.J., Structural basis of metallo-β-lactamase, serine-β-lactamase and penicillin-binding protein inhibition by cyclic boronates. Nat. Commun., 7, 2016, 12406.
Bush, K., The ABCD's of β-lactamase nomenclature. J. Infect. Chemother. Off. J. Jpn. Soc. Chemother. 19 (2013), 549–559.
Bush, K., Jacoby, G.A., Updated functional classification of β-lactamases. Antimicrob. Agents Chemother. 54 (2010), 969–976.
Cag, Y., Caskurlu, H., Fan, Y., Cao, B., Vahaboglu, H., Resistance mechanisms. Ann. Transl. Med., 4, 2016 326–326.
Collaborative Computational Project, Number 4, The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50 (1994), 760–763.
Cowtan, K., Emsley, P., Wilson, K.S., From crystal to structure with CCP4. Acta Crystallogr. D Biol. Crystallogr. 67 (2011), 233–234.
Crowder, M.W., Spencer, J., Vila, A.J., Metallo-β-lactamases: novel weaponry for antibiotic resistance in bacteria. Acc. Chem. Res. 39 (2006), 721–728.
Docquier, J.-D., Pantanella, F., Giuliani, F., Thaller, M.C., Amicosante, G., Galleni, M., Frère, J.-M., Bush, K., Rossolini, G.M., CAU-1, a subclass B3 metallo-beta-lactamase of low substrate affinity encoded by an ortholog present in the Caulobacter crescentus chromosome. Antimicrob. Agents Chemother. 46 (2002), 1823–1830.
Docquier, J.-D., Benvenuti, M., Calderone, V., Stoczko, M., Menciassi, N., Rossolini, G.M., Mangani, S., 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 (2010), 4343–4351.
Emsley, P., Cowtan, K., Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004), 2126–2132.
Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 486–501.
Evans, P., Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62 (2006), 72–82.
Faridoon, Ul Islam, N., An update on the status of potent inhibitors of metallo-β-lactamases. Sci. Pharm. 81 (2013), 309–327.
Fast, W., Sutton, L.D., Metallo-β-lactamase: inhibitors and reporter substrates. Biochim. Biophys. Acta BBA Proteins Proteomics 1834 (2013), 1648–1659.
Furuyama, T., Nonomura, H., Ishii, Y., Hanson, N.D., Shimizu-Ibuka, A., Structural and mutagenic analysis of metallo-β-lactamase IMP-18. Antimicrob. Agents Chemother. 60 (2016), 5521–5526.
Galleni, M., Lamotte-Brasseur, J., Rossolini, G.M., Spencer, J., Dideberg, O., Frère, J.-M., Group, T.M.-β-L.W., Standard numbering scheme for class B β-lactamases. Antimicrob. Agents Chemother. 45 (2001), 660–663.
Garau, G., García-Sáez, I., Bebrone, C., Anne, C., Mercuri, P., Galleni, M., Frère, J.-M., Dideberg, O., Update of the standard numbering scheme for class B β-lactamases. Antimicrob. Agents Chemother. 48 (2004), 2347–2349.
Garcı́a-Sáez, I., Mercuri, P.S., Papamicael, C., Kahn, R., Frère, J.M., Galleni, M., Rossolini, G.M., Dideberg, O., 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 (2003), 651–660.
Garrity, J.D., Pauff, J.M., Crowder, M.W., 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 stopped-flow fluorescence spectroscopy. J. Biol. Chem. 279 (2004), 39663–39670.
Hecker, S.J., Reddy, K.R., Totrov, M., Hirst, G.C., Lomovskaya, O., Griffith, D.C., King, P., Tsivkovski, R., Sun, D., Sabet, M., et al. Discovery of a cyclic boronic acid β-lactamase inhibitor (RPX7009) with utility vs class A serine carbapenemases. J. Med. Chem. 58 (2015), 3682–3692.
Hinchliffe, P., González, M.M., Mojica, M.F., González, J.M., Castillo, V., Saiz, C., Kosmopoulou, M., Tooke, C.L., Llarrull, L.I., Mahler, G., et al. Cross-class metallo-β-lactamase inhibition by bisthiazolidines reveals multiple binding modes. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E3745–3754.
Huntley, J.J.A., Fast, W., Benkovic, S.J., Wright, P.E., Dyson, H.J., Role of a solvent-exposed tryptophan in the recognition and binding of antibiotic substrates for a metallo-β-lactamase. Protein Sci. 12 (2003), 1368–1375.
Jacoby, G.A., Β-lactamase nomenclature. Antimicrob. Agents Chemother. 50 (2006), 1123–1129.
King, D.T., Worrall, L.J., Gruninger, R., Strynadka, N.C.J., New Delhi Metallo-β-lactamase: structural insights into β-lactam recognition and inhibition. J. Am. Chem. Soc. 134 (2012), 11362–11365.
Kupper, M.B., Herzog, K., Bennink, S., Schlömer, P., Bogaerts, P., Glupczynski, Y., Fischer, R., Bebrone, C., Hoffmann, K.M., The three-dimensional structure of VIM-31 – a metallo-β-lactamase from Enterobacter cloacae in its native and oxidized form. FEBS J. 282 (2015), 2352–2360.
Langer, G., Cohen, S.X., Lamzin, V.S., Perrakis, A., Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3 (2008), 1171–1179.
Laskowski, R.A., MacArthur, M.W., Thornton, J.M., Validation of protein models derived from experiment. Curr. Opin. Struct. Biol. 8 (1998), 631–639.
Leiros, H.-K.S., Borra, P.S., Brandsdal, B.O., Edvardsen, K.S.W., Spencer, J., Walsh, T.R., Samuelsen, Ø., 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 (2012), 4341–4353.
Leslie, A.G.W., The integration of macromolecular diffraction data. Acta Crystallogr. D Biol. Crystallogr. 62 (2006), 48–57.
Livermore, D.M., Has the era of untreatable infections arrived?. J. Antimicrob. Chemother. 64 (2009), i29–i36.
Meini, M.-R., Llarrull, L.I., Vila, A.J., Overcoming differences: the catalytic mechanism of metallo-β-lactamases. FEBS Lett. 589 (2015), 3419–3432.
Mercuri, P.S., García-Sáez, I., Vriendt, K.D., Thamm, I., Devreese, B., Beeumen, J.V., Dideberg, O., Rossolini, G.M., Frère, J.-M., Galleni, M., Probing the specificity of the subclass B3 FEZ-1 metallo-β-lactamase by site-directed mutagenesis. J. Biol. Chem. 279 (2004), 33630–33638.
Moali, C., Anne, C., Lamotte-Brasseur, J., Groslambert, S., Devreese, B., Van Beeumen, J., Galleni, M., Frère, J.-M., Analysis of the importance of the metallo-β-lactamase active site loop in substrate binding and catalysis. Chem. Biol. 10 (2003), 319–329.
Morán-Barrio, J., Lisa, M.-N., Larrieux, N., Drusin, S.I., Viale, A.M., Moreno, D.M., Buschiazzo, A., Vila, A.J., Crystal structure of the metallo-β-lactamase GOB in the periplasmic dizinc form reveals an unusual metal site. Antimicrob. Agents Chemother. 60 (2016), 6013–6022.
Murshudov, G.N., Skubák, P., Lebedev, A.A., Pannu, N.S., Steiner, R.A., Nicholls, R.A., Winn, M.D., Long, F., Vagin, A.A., REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67 (2011), 355–367.
Nauton, L., Kahn, R., Garau, G., Hernandez, J.F., Dideberg, O., Structural insights into the design of inhibitors for the L1 metallo-β-lactamase from Stenotrophomonas maltophilia. J. Mol. Biol. 375 (2008), 257–269.
Osano, E., Arakawa, Y., Wacharotayankun, R., Ohta, M., Horii, T., Ito, H., Yoshimura, F., Kato, N., Molecular characterization of an enterobacterial metallo beta-lactamase found in a clinical isolate of Serratia marcescens that shows imipenem resistance. Antimicrob. Agents Chemother. 38 (1994), 71–78.
Page, M.I., Badarau, A., The mechanisms of catalysis by metallo beta-lactamases. Bioinorg. Chem. Appl., 2008 576297.
Palzkill, T., Metallo-β-lactamase structure and function. Ann. N. Y. Acad. Sci. 1277 (2013), 91–104.
Papp-Wallace, K.M., Bonomo, R.A., New β-lactamase inhibitors in the Clinic. Infect. Dis. Clin. North Am. 30 (2016), 441–464.
Pettinati, I., Brem, J., Lee, S.Y., McHugh, P.J., Schofield, C.J., The chemical biology of human metallo-β-lactamase fold proteins. Trends Biochem. Sci. 41 (2016), 338–355.
Potterton, L., McNicholas, S., Krissinel, E., Gruber, J., Cowtan, K., Emsley, P., Murshudov, G.N., Cohen, S., Perrakis, A., Noble, M., Developments in the CCP4 molecular-graphics project. Acta Crystallogr. D Biol. Crystallogr. 60 (2004), 2288–2294.
Rasmussen, B.A., Gluzman, Y., Tally, F.P., Cloning and sequencing of the class B beta-lactamase gene (ccrA) from Bacteroides fragilis TAL3636. Antimicrob. Agents Chemother. 34 (1990), 1590–1592.
Saavedra, M.J., Peixe, L., Sousa, J.C., Henriques, I., Alves, A., Correia, A., Sfh-I, a subclass B2 metallo-beta-lactamase from a Serratia fonticola environmental isolate. Antimicrob. Agents Chemother. 47 (2003), 2330–2333.
Salimraj, R., Zhang, L., Hinchliffe, P., Wellington, E.M.H., Brem, J., Schofield, C.J., Gaze, W.H., Spencer, J., Structural and biochemical characterization of Rm3, a subclass B3 metallo-β-lactamase identified from a functional metagenomic study. Antimicrob. Agents Chemother. 60 (2016), 5828–5840.
Sgrignani, J., De Luca, F., Torosyan, H., Docquier, J.-D., Duan, D., Novati, B., Prati, F., Colombo, G., Grazioso, G., Structure-based approach for identification of novel phenylboronic acids as serine-β-lactamase inhibitors. J. Comput. Aided Mol. Des. 30 (2016), 851–861.
Spencer, J., Read, J., Sessions, R.B., Howell, S., Blackburn, G.M., Gamblin, S.J., Antibiotic recognition by binuclear metallo-β-lactamases revealed by X-ray crystallography. J. Am. Chem. Soc. 127 (2005), 14439–14444.
Stoczko, M., Frère, J.-M., Rossolini, G.M., Docquier, J.-D., 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 (2006), 1973–1981.
Tondi, D., Venturelli, A., Bonnet, R., Pozzi, C., Shoichet, B.K., Costi, M.P., Targeting Class A and C Serine β-Lactamases with a Broad-Spectrum Boronic Acid Derivative. J. Med. Chem. 57 (2014), 5449–5458.
Ullah, J.H., Walsh, T.R., Taylor, I.A., Emery, D.C., Verma, C.S., Gamblin, S.J., Spencer, J., The crystal structure of the L1 metallo-β-lactamase from Stenotrophomonas maltophilia at 1.7 Å resolution1. J. Mol. Biol. 284 (1998), 125–136.
Vagin, A., Teplyakov, A., Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 22–25.
Wachino, J., Yoshida, H., Yamane, K., Suzuki, S., Matsui, M., Yamagishi, T., Tsutsui, A., Konda, T., Shibayama, K., Arakawa, Y., 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 (2011), 5143–5149.
Wachino, J., Yamaguchi, Y., Mori, S., Kurosaki, H., Arakawa, Y., Shibayama, K., 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 (2013), 101–109.
Wachino, J.-I., Yamaguchi, Y., Mori, S., Jin, W., Kimura, K., Kurosaki, H., Arakawa, Y., Structural insights into recognition of hydrolyzed carbapenems and inhibitors by subclass B3 metallo-β-lactamase SMB-1. Antimicrob. Agents Chemother. 60 (2016), 4274–4282.
Wang, Z., Fast, W., Valentine, A.M., Benkovic, S.J., Metallo-beta-lactamase: structure and mechanism. Curr. Opin. Chem. Biol. 3 (1999), 614–622.
Yamaguchi, Y., Matsueda, S., Matsunaga, K., Takashio, N., Toma-Fukai, S., Yamagata, Y., Shibata, N., Wachino, J., Shibayama, K., Arakawa, Y., et al. Crystal Structure of IMP-2 Metallo-β-lactamase from Acinetobacter spp. Biol. Pharm. Bull. 38 (2015), 96–101.
Zhang, H., Hao, Q., Crystal structure of NDM-1 reveals a common β-lactam hydrolysis mechanism. FASEB J. 25 (2011), 2574–2582.