An update on β-lactamase inhibitor discovery and development

Antibiotic resistance; Beta-lactamase; Crystal structure; Drug discovery; Inhibitor; Review; Gram negative bacterium; Gram negative infection; Bacterial Proteins; Drug Combinations; Drug Design; Gram-Negative Bacteria; Gram-Negative Bacterial Infections; Molecular Structure; Structure-Activity Relationship

Abstract :

[en] Antibiotic resistance, and the emergence of pan-resistant clinical isolates, seriously threatens our capability to treat bacterial diseases, including potentially deadly hospital-acquired infections. This growing issue certainly requires multiple adequate responses, including the improvement of both diagnosis methods and use of antibacterial agents, and obviously the development of novel antibacterial drugs, especially active against Gram-negative pathogens, which represent an urgent medical need. Considering the clinical relevance of both β-lactam antibiotics and β-lactamase-mediated resistance, the discovery and development of combinations including a β-lactamase inhibitor seems to be particularly attractive, despite being extremely challenging due to the enormous diversity, both structurally and mechanistically, of the potential β-lactamase targets. This review will cover the evolution of currently available β-lactamase inhibitors along with the most recent research leading to new β-lactamase inhibitors of potential clinical interest or already in the stage of clinical development. © 2017 Elsevier Ltd

Disciplines :

Life sciences: Multidisciplinary, general & others
Microbiology
Biochemistry, biophysics & molecular biology

Author, co-author :

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

Mangani, S.; Department of Biotechnology, Chemistry and Pharmacy, University of Siena, Via Aldo Moro 2, Siena, 53100, Italy

Language :

English

Title :

An update on β-lactamase inhibitor discovery and development

Publication date :

2018

Journal title :

Drug Resistance Updates

ISSN :

1368-7646

Publisher :

Churchill Livingstone

Volume :

Pages :

13-29

Peer reviewed :

Peer reviewed

Available on ORBi :

since 13 November 2020

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57 (1 by ULiège)

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1 (1 by ULiège)

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Scopus citations^®

174

Scopus citations^®
without self-citations

160

OpenCitations

137

OpenAlex citations

177

Bibliography

Aitha, M., Al-Adbul-Wahid, S., Tierney, D.L., Crowder, M.W., Probing substrate binding to the metal binding sites in metallo-β-lactamase L1 during catalysis. Med. Chem. Commun. 7 (2016), 194–201, 10.1039/C5MD00358J.
Aoki, N., Ishii, Y., Tateda, K., Saga, T., Kimura, S., Kikuchi, Y., Kobayashi, T., Tanabe, Y., Tsukada, H., Gejyo, F., Yamaguchi, K., Efficacy of calcium-EDTA as an inhibitor for metallo-β-lactamase in a mouse model of Pseudomonas aeruginosa pneumonia. Antimicrob. Agents Chemother. 54 (2010), 4582–4588, 10.1128/AAC.00511-10.
Arjomandi, O.K., Hussein, W.M., Vella, P., Yusof, Y., Sidjabat, H.E., Schenk, G., McGeary, R.P., Design, synthesis, and in vitro and biological evaluation of potent amino acid-derived thiol inhibitors of the metallo-β-lactamase IMP-1. Eur. J. Med. Chem. 114 (2016), 318–327, 10.1016/j.ejmech.2016.03.017.
Ban, H.S., Nakamura, H., Boron-based drug design. Chem. Rec. 15 (2015), 616–635, 10.1002/tcr.201402100.
Bebrone, C., Metallo-β-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily. Biochem. Pharmacol. 74 (2007), 1686–1701, 10.1016/j.bcp.2007.05.021.
Bebrone, C., Delbruck, H., Kupper, M.B., Schlomer, P., Willmann, C., Frere, J.M., Fischer, R., Galleni, M., Hoffmann, K.M., The structure of the dizinc subclass B2 metallo-β-lactamase CphA reveals that the second inhibitory zinc ion binds in the histidine site. Antimicrob. Agents Chemother. 53 (2009), 4464–4471, 10.1128/AAC.00288-09.
Beesley, T., Gascoyne, N., Knott-Hunziker, V., Petursson, S., Waley, S.G., Jaurin, B., Grundström, T., The inhibition of class C β-lactamases by boronic acids. Biochem. J. 209 (1983), 229–233, 10.1042/bj2090229.
Benini, S., Rypniewski, W., Wilson, K.S., Ciurli, S., Mangani, S., The complex of Bacillus pasteurii urease with β-mercaptoethanol from X-ray data at 1.65-Å resolution. J. Biol. Inorg. Chem. 3 (1998), 268–273, 10.1007/s007750050231.
Benini, S., Rypniewski, W.R., Wilson, K.S., Mangani, S., Ciurli, S., Molecular details of urease inhibition by boric acid: insights into the catalytic mechanism. J. Am. Chem. Soc 126 (2004), 3714–3715, 10.1021/ja049618p.
Biswas, S., Brunel, J.-M., Dubus, J.-C., Reynaud-Gaubert, M., Rolain, J.-M., Colistin: an update on the antibiotic of the 21st century. Expert Rev. Anti. Infect. Ther. 10 (2012), 917–934, 10.1586/eri.12.78.
Blizzard, T.A., Chen, H., Kim, S., Wu, J., Bodner, R., Gude, C., Imbriglio, J., Young, K., Park, Y.-W., Ogawa, A., Raghoobar, S., Hairston, N., Painter, R.E., Wisniewski, D., Scapin, G., Fitzgerald, P., Sharma, N., Lu, J., Ha, S., Hermes, J., Hammond, M.L., Discovery of MK-7655, a β-lactamase inhibitor for combination with Primaxin®. Bioorg. Med. Chem. Lett. 24 (2014), 780–785, 10.1016/j.bmcl.2013.12.101.
Bonnefoy, A., Dupuis-Hamelin, C., Steier, V., Delachaume, C., Seys, C., Stachyra, T., Fairley, M., Guitton, M., Lampilas, M., In vitro activity of AVE1330A, an innovative broad-spectrum non-β-lactam β-lactamase inhibitor. J. Antimicrob. Chemother. 54 (2004), 410–417, 10.1093/jac/dkh358.
Bou, G., Santillana, E., Sheri, A., Beceiro, A., Sampson, J.M., Kalp, M., Bethel, C.R., Distler, A.M., Drawz, S.M., Pagadala, S.R.R., van den Akker, F., Bonomo, R.A., Romero, A., Buynak, J.D., Design, synthesis, and crystal structures of 6-alkylidene-2’-substituted penicillanic acid sulfones as potent inhibitors of Acinetobacter baumannii OXA-24 carbapenemase. J. Am. Chem. Soc 132 (2010), 13320–13331, 10.1021/ja104092z.
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, 10.1038/ncomms12406.
Brem, J., van Berkel, S.S., Aik, W., Rydzik, A.M., Avison, M.B., Pettinati, I., Umland, K.D., Kawamura, A., Spencer, J., Claridge, T.D., McDonough, M.A., Schofield, C.J., Rhodanine hydrolysis leads to potent thioenolate mediated metallo-β-lactamase inhibition. Nat. Chem. 6 (2014), 1084–1090, 10.1038/nchem.2110.
Brem, J., van Berkel, S.S., Zollman, D., Lee, S.Y., Gileadi, O., McHugh, P.J., Walsh, T.R., McDonough, M.A., Schofield, C.J., Structural basis of metallo-β-lactamase inhibition by captopril stereoisomers. Antimicrob. Agents Chemother. 60 (2016), 142–150, 10.1128/AAC.01335-15.
Brindisi, M., Brogi, S., Giovani, S., Gemma, S., Lamponi, S., De Luca, F., Novellino, E., Campiani, G., Docquier, J.-D., Butini, S., Targeting clinically-relevant metallo-β-lactamases: from high-throughput docking to broad-spectrum inhibitors. J. Enzyme Inhib. Med. Chem. 31 (2016), 98–109, 10.3109/14756366.2016.1172575.
Burns, C.J., Goswami, R., Jackson, R.W., Lessen, T., Li, W., Pevear, D., Tirunahari, P.K., Xu, H., 2010. β-lactamase inhibitors. Patent WO 2010/130708 A1.
Bush, K., Carbapenemases: partners in crime. J. Glob. Antimicrob. Resist. 1 (2013), 7–16, 10.1016/j.jgar.2013.01.005.
Bush, K., Improving known classes of antibiotics: an optimistic approach for the future. Curr. Opin. Pharmacol. 12 (2012), 527–534, 10.1016/j.coph.2012.06.003.
Bush, K., Bradford, P.A., β-lactams and β-lactamase inhibitors: an overview. Cold Spring Harb. Perspect. Med., 6, 2016, a025247, 10.1101/cshperspect.a025247.
Bush, K., Jacoby, G.A., Updated functional classification of β-lactamases. Antimicrob. Agents Chemother. 54 (2010), 969–976, 10.1128/AAC.01009-09.
Buzzoni, V., Blasquez, J., Ferrari, S., Calò, S., Venturelli, A., Costi, M.P., Aza-boronic acids as non β-lactam inhibitors of AmpC β-lactamase. Bioorg. Med. Chem. Lett. 14 (2004), 3979–3983, 10.1016/j.bmcl.2004.05.054.
Chen, A.Y., Thomas, P.W., Stewart, A.C., Bergstrom, A., Cheng, Z., Miller, C., Bethel, C.R., Marshall, S.H., Credille, C.V., Riley, C.L., Page, R.C., Bonomo, R.A., Crowder, M.W., Tierney, D.L., Fast, W., Cohen, S.M., Dipicolinic acid derivatives as inhibitors of New Delhi metallo-β-lactamase-1. J. Med. Chem. 60 (2017), 7267–7283, 10.1021/acs.jmedchem.7b00407.
Chiou, J., Wan, S., Chan, K.-F., So, P.-K., He, D., Chan, E.W., Chan, T., Wong, K., Tao, J., Chen, S., Ebselen as a potent covalent inhibitor of New Delhi metallo-β-lactamase (NDM-1). Chem. Commun. (Camb). 51 (2015), 9543–9546, 10.1039/c5cc02594j.
Christopeit, T., Albert, A., Leiros, H.-K.S., Discovery of a novel covalent non-β-lactam inhibitor of the metallo-β-lactamase NDM-1. Bioorg. Med. Chem. 24 (2016), 2947–2953, 10.1016/j.bmc.2016.04.064.
Christopeit, T., Leiros, H.-K.S., Fragment-based discovery of inhibitor scaffolds targeting the metallo-β-lactamases NDM-1 and VIM-2. Bioorg. Med. Chem. Lett. 26 (2016), 1973–1977, 10.1016/j.bmcl.2016.03.004.
Compain, F., Arthur, M., Impaired inhibition by avibactam and resistance to the ceftazidime-avibactam combination due to the D 179 Y substitution in the β-lactamase KPC-2. Antimicrob. Agents Chemother. 61 (2017), 17–e00451, 10.1128/AAC.00451-17.
Crandon, J.L., Nicolau, D.P., In vitro activity of cefepime/AAI101 and comparators against cefepime non-susceptible Enterobacteriaceae. Pathogens 4 (2015), 620–625, 10.3390/pathogens4030620.
Dobias, J., Dénervaud-Tendon, V., Poirel, L., Nordmann, P., Activity of the novel siderophore cephalosporin cefiderocol against multidrug-resistant Gram-negative pathogens. Eur. J. Clin. Microbiol. Infect. Dis., 2017, 10.1007/s10096-017-3063-z.
Docquier, J.-D., Lamotte-Brasseur, J., Galleni, M., Amicosante, G., Frère, J.-M., Rossolini, G.M., On functional and structural heterogeneity of VIM-type metallo-β-lactamases. J. Antimicrob. Chemother. 51 (2003), 257–266, 10.1093/jac/dkg067.
Dortet, L., Poirel, L., Nordmann, P., Worldwide dissemination of the NDM-type carbapenemases in gram-negative bacteria. Biomed Res. Int., 2014, 2014, 249856, 10.1155/2014/249856.
Doumith, M., Mushtaq, S., Livermore, D.M., Woodford, N., New insights into the regulatory pathways associated with the activation of the stringent response in bacterial resistance to the PBP2-targeted antibiotics, mecillinam and OP0595/RG6080. J. Antimicrob. Chemother. 71 (2016), 2810–2814, 10.1093/jac/dkw230.
Drawz, S.M., Babic, M., Bethel, C.R., Taracila, M., Distler, A.M., Ori, C., Caselli, E., Prati, F., Bonomo, R.A., Inhibition of the class C β-lactamase from Acinetobacter spp.: insights into effective inhibitor design. Biochemistry 49 (2010), 329–340, 10.1021/bi9015988.
Drawz, S.M., Bethel, C.R., Doppalapudi, V.R., Sheri, A., Pagadala, S.R.R., Hujer, A.M., Skalweit, M.J., Anderson, V.E., Chen, S.G., Buynak, J.D., Bonomo, R.A., Penicillin sulfone inhibitors of class D β-lactamases. Antimicrob. Agents Chemother. 54 (2010), 1414–1424, 10.1128/AAC.00743-09.
Drawz, S.M., Bonomo, R.A., Three decades of β-lactamase inhibitors. Clin. Microbiol. Rev. 23 (2010), 160–201, 10.1128/CMR.00037-09.
Durand-Réville, T.F., Guler, S., Comita-Prevoir, J., Chen, B., Bifulco, N., Huynh, H., Lahiri, S., Shapiro, A.B., McLeod, S.M., Carter, N.M., Moussa, S.H., Velez-Vega, C., Olivier, N.B., McLaughlin, R., Gao, N., Thresher, J., Palmer, T., Andrews, B., Giacobbe, R.A., Newman, J.V., Ehmann, D.E., de Jonge, B., O'Donnell, J., Mueller, J.P., Tommasi, R.A., Miller, A.A., ETX2514 is a broad-spectrum β-lactamase inhibitor for the treatment of drug-resistant Gram-negative bacteria including Acinetobacter baumannii. Nat. Microbiol., 2, 2017, 17104, 10.1038/nmicrobiol.2017.104.
Ehmann, D.E., Jahic, H., Ross, P.L., Gu, R.-F., Hu, J., Durand-Reville, T.F., Lahiri, S., Thresher, J., Livchak, S., Gao, N., Palmer, T., Walkup, G.K., Fisher, S.L., Kinetics of avibactam inhibition against class A, C, and D β-Lactamases. J. Biol. Chem. 288 (2013), 27960–27971, 10.1074/jbc.M113.485979.
Ehmann, D.E., Jahic, H., Ross, P.L., Gu, R.-F., Hu, J., Kern, G., Walkup, G.K., Fisher, S.L., Avibactam is a covalent, reversible, non-β-lactam β-lactamase inhibitor. Proc. Natl. Acad. Sci. 109 (2012), 11663–11668, 10.1073/pnas.1205073109.
Eidam, O., Romagnoli, C., Caselli, E., Babaoglu, K., Pohlhaus, D.T., Karpiak, J., Bonnet, R., Shoichet, B.K., Prati, F., Design, synthesis, crystal structures, and antimicrobial activity of sulfonamide boronic acids as β-lactamase inhibitors. J. Med. Chem. 53 (2010), 7852–7863, 10.1021/jm101015z.
Eidam, O., Romagnoli, C., Dalmasso, G., Barelier, S., Caselli, E., Bonnet, R., Shoichet, B.K., Prati, F., Fragment-guided design of subnanomolar β-lactamase inhibitors active in vivo. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 17448–17453, 10.1073/pnas.1208337109.
Falagas, M.E., Skalidis, T., Vardakas, K.Z., Legakis, N.J., Hellenic Cefiderocol Study Group, Activity of cefiderocol (S-649266) against carbapenem-resistant Gram-negative bacteria collected from inpatients in Greek hospitals. J. Antimicrob. Chemother. 72 (2017), 1704–1708, 10.1093/jac/dkx049.
Falconer, S.B., Reid-Yu, S.A., King, A.M., Gehrke, S.S., Wang, W., Britten, J.F., Coombes, B.K., Wright, G.D., Brown, E.D., Zinc chelation by a small-molecule adjuvant potentiates meropenem activity in vivo against NDM-1-producing Klebsiella pneumoniae. ACS Infect. Dis. 1 (2015), 533–543, 10.1021/acsinfecdis.5b00033.
Fast, W., Sutton, L.D., Metallo-β-lactamase: inhibitors and reporter substrates. Biochim. Biophys. Acta. 1834 (2013), 1648–1659, 10.1016/j.bbapap.2013.04.024.
Feng, L., Yang, K.-W., Zhou, L.-S., Xiao, J.-M., Yang, X., Zhai, L., Zhang, Y.-L., Crowder, M.W., N-heterocyclic dicarboxylic acids: broad-spectrum inhibitors of metallo-β-lactamases with co-antibacterial effect against antibiotic-resistant bacteria. Bioorg. Med. Chem. Lett. 22 (2012), 5185–5189, 10.1016/j.bmcl.2012.06.074.
Frère, J.M., Joris, B., Granier, B., Matagne, A., Jacob, F., Bourguignon-Bellefroid, C., Diversity of the mechanisms of resistance to β-lactam antibiotics. Res. Microbiol. 142 (1991), 705–710, 10.1016/0923-2508(91)90084-N.
Garau, G., Garcia-Saez, I., Bebrone, C., Anne, C., Mercuri, P., Galleni, M., Frere, J.M., Dideberg, O., Update of the standard numbering scheme for class B β-lactamases. Antimicrob. Agents Chemother. 48 (2004), 2347–2349, 10.1128/AAC.48.7.2347-2349.2004.
Garcia-Saez, I., Hopkins, J., Papamicael, C., Franceschini, N., Amicosante, G., Rossolini, G.M., Galleni, M., Frere, J.M., Dideberg, O., The 1.5-Å structure of Chryseobacterium meningosepticum zinc β-lactamase in complex with the inhibitor, D-captopril. J. Biol. Chem. 278 (2003), 23868–23873, 10.1074/jbc.M301062200.
Garcia-Saez, 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, 10.1016/S0022-2836(02)01271-8.
González, M.M., Kosmopoulou, M., Mojica, M.F., Castillo, V., Hinchliffe, P., Pettinati, I., Brem, J., Schofield, C.J., Mahler, G., Bonomo, R.A., Llarrull, L.I., Spencer, J., Vila, A.J., Bisthiazolidines: a substrate-mimicking scaffold as an inhibitor of the NDM-1 carbapenemase. ACS Infect. Dis. 1 (2015), 544–554, 10.1021/acsinfecdis.5b00046.
Griffith, D.C., Loutit, J.S., Morgan, E.E., Durso, S., Dudley, M.N., Phase 1 study of the safety, tolerability, and pharmacokinetics of the β-lactamase inhibitor vaborbactam (RPX7009) in healthy adult subjects. Antimicrob. Agents Chemother. 60 (2016), 6326–6332, 10.1128/AAC.00568-16.
Griffith, E.C., Su, Z., Turk, B.E., Chen, S., Chang, Y.-H., Wu, Z., Biemann, K., Liu, J.O., Methionine aminopeptidase (type 2) is the common target for angiogenesis inhibitors AGM-1470 and ovalicin. Chem. Biol. 4 (1997), 461–471, 10.1016/S1074-5521(97)90198-8.
Haenni, A.L., Robert, M., Vetter, W., Roux, L., Barbier, M., Lederer, E., Chemical structure of aspergillomarasmines A and B. Helv. Chim. Acta 48 (1965), 729–750, 10.1002/hlca.19650480409.
Hai, Y., Edwards, J.E., Van Zandt, M.C., Hoffmann, K.F., Christianson, D.W., Crystal structure of Schistosoma mansoni arginase, a potential drug target for the treatment of schistosomiasis. Biochemistry 53 (2014), 4671–4684, 10.1021/bi5004519.
Hecker, S.J., Reddy, K.R., Glinka, T.W., Totrov, M., Lomovskaya, O., Tsivkovski, R., Rubio-Aparicio, D., Clifton, M.C., Atkins, K., Fairman, J.W., Griffith, D., Dudley, M.N., Discovery of a new series of broad-spectrum carbapenemase inhibitors (BCIs) with activity vs serine and metallo β-lactamases. American Society for Microbiology, 55th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC/ICC), 2015, ASM Press, San Diego, CA Abstract F-270.
Hecker, S.J., Reddy, K.R., Totrov, M., Hirst, G.C., Lomovskaya, O., Griffith, D.C., King, P., Tsivkovski, R., Sun, D., Sabet, M., Tarazi, Z., Clifton, M.C., Atkins, K., Raymond, A., Potts, K.T., Abendroth, J., Boyer, S.H., Loutit, J.S., Morgan, E.E., Durso, S., Dudley, M.N., Discovery of a cyclic boronic acid β-lactamase inhibitor (RPX7009) with utility vs class A serine carbapenemases. J. Med. Chem. 58 (2015), 3682–3692, 10.1021/acs.jmedchem.5b00127.
Helfand, M.S., Totir, M.A., Carey, M.P., Hujer, A.M., Bonomo, R.A., Carey, P.R., Following the reactions of mechanism-based inhibitors with β-lactamase by Raman crystallography. Biochemistry 42 (2003), 13386–13392, 10.1021/bi035716w.
Hideshima, T., Richardson, P.G., Anderson, K.C., Mechanism of action of proteasome inhibitors and deacetylase inhibitors and the biological basis of synergy in multiple myeloma. Mol. Cancer Ther. 10 (2011), 2034–2042, 10.1158/1535-7163.MCT-11-0433.
Higgins, P.G., Stefanik, D., Page, M.G.P., Hackel, M., Seifert, H., In vitro activity of the siderophore monosulfactam BAL30072 against meropenem-non-susceptible Acinetobacter baumannii. J. Antimicrob. Chemother. 67 (2012), 1167–1169, 10.1093/jac/dks009.
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., Bonomo, R.A., Vila, A.J., Spencer, J., Cross-class metallo-β-lactamase inhibition by bisthiazolidines reveals multiple binding modes. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E3745–E3754, 10.1073/pnas.1601368113.
Hiraiwa, Y., Saito, J., Watanabe, T., Yamada, M., Morinaka, A., Fukushima, T., Kudo, T., X-ray crystallographic analysis of IMP-1 metallo-β-lactamase complexed with a 3-aminophthalic acid derivative, structure-based drug design, and synthesis of 3,6-disubstituted phthalic acid derivative inhibitors. Bioorg. Med. Chem. Lett. 24 (2014), 4891–4894, 10.1016/j.bmcl.2014.08.039.
Hofer, B., Dantier, C., Gebhardt, K., Desarbre, E., Schmitt-Hoffmann, A., Page, M.G.P., Combined effects of the siderophore monosulfactam BAL30072 and carbapenems on multidrug-resistant Gram-negative bacilli. J. Antimicrob. Chemother. 68 (2013), 1120–1129, 10.1093/jac/dks527.
Hornsey, M., Phee, L., Stubbings, W., Wareham, D.W., In vitro activity of the novel monosulfactam BAL30072 alone and in combination with meropenem versus a diverse collection of important Gram-negative pathogens. Int. J. Antimicrob. Agents 42 (2013), 343–346, 10.1016/j.ijantimicag.2013.05.010.
Ishii, Y., Eto, M., Mano, Y., Tateda, K., Yamaguchi, K., In vitro potentiation of carbapenems with ME1071, a novel metallo-β-lactamase inhibitor, against metallo-β-lactamase-producing Pseudomonas aeruginosa clinical isolates. Antimicrob. Agents Chemother. 54 (2010), 3625–3629, 10.1128/AAC.01397-09.
Ito-Horiyama, T., Ishii, Y., Ito, A., Sato, T., Nakamura, R., Fukuhara, N., Tsuji, M., Yamano, Y., Yamaguchi, K., Tateda, K., Stability of novel siderophore cephalosporin S-649266 against clinically relevant carbapenemases. Antimicrob. Agents Chemother. 60 (2016), 4384–4386, 10.1128/AAC.03098-15.
Ito, A., Kohira, N., Bouchillon, S.K., West, J., Rittenhouse, S., Sader, H.S., Rhomberg, P.R., Jones, R.N., Yoshizawa, H., Nakamura, R., Tsuji, M., Yamano, Y., In vitro antimicrobial activity of S-649266, a catechol-substituted siderophore cephalosporin, when tested against non-fermenting Gram-negative bacteria. J. Antimicrob. Chemother. 71 (2016), 670–677, 10.1093/jac/dkv402.
Ito, A., Nishikawa, T., Matsumoto, S., Yoshizawa, H., Sato, T., Nakamura, R., Tsuji, M., Yamano, Y., Siderophore cephalosporin cefiderocol utilizes ferric iron transporter systems for antibacterial activity against Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 60 (2016), 7396–7401, 10.1128/AAC.01405-16.
Karsisiotis, A.I., Damblon, C.F., Roberts, G.C.K., A variety of roles for versatile zinc in metallo-β-lactamases. Metallomics 6 (2014), 1181–1197, 10.1039/C4MT00066H.
Ke, W., Sampson, J.M., Ori, C., Prati, F., Drawz, S.M., Bethel, C.R., Bonomo, R.A., van den Akker, F., Novel insights into the mode of inhibition of class A SHV-1 β-lactamases revealed by boronic acid transition state inhibitors. Antimicrob. Agents Chemother. 55 (2011), 174–183, 10.1128/AAC.00930-10.
Khan, A.U., Maryam, L., Zarrilli, R., Structure, genetics and worldwide spread of New Delhi metallo-β-lactamase (NDM): a threat to public health. BMC Microbiol., 17, 2017, 101, 10.1186/s12866-017-1012-8.
Kiener, P.A., Waley, S.G., Reversible inhibitors of penicillinases. Biochem. J. 169 (1978), 197–204, 10.1042/bj1690197.
King, A.M., Reid-Yu, S.A., Wang, W., King, D.T., De Pascale, G., Strynadka, N.C., Walsh, T.R., Coombes, B.K., Wright, G.D., Aspergillomarasmine A overcomes metallo-β-lactamase antibiotic resistance. Nature 510 (2014), 503–506, 10.1038/nature13445.
King, D.T., Worrall, L.J., Gruninger, R., Strynadka, N.C., New Delhi metallo-β-lactamase: structural insights into β-lactam recognition and inhibition. J. Am. Chem. Soc. 134 (2012), 11362–11365, 10.1021/ja303579d.
Klingler, F.-M., Moser, D., Büttner, D., Wichelhaus, T.A., Löhr, F., Dötsch, V., Proschak, E., Probing metallo-β-lactamases with molecular fragments identified by consensus docking. Bioorg. Med. Chem. Lett. 25 (2015), 5243–5246, 10.1016/j.bmcl.2015.09.056.
Klingler, F.-M., Wichelhaus, T.A., Frank, D., Cuesta-Bernal, J., El-Delik, J., Müller, H.F., Sjuts, H., Göttig, S., Koenigs, A., Pos, K.M., Pogoryelov, D., Proschak, E., Approved drugs containing thiols as inhibitors of metallo-β-lactamases: strategy to combat multidrug-resistant bacteria. J. Med. Chem. 58 (2015), 3626–3630, 10.1021/jm501844d.
Kohira, N., West, J., Ito, A., Ito-Horiyama, T., Nakamura, R., Sato, T., Rittenhouse, S., Tsuji, M., Yamano, Y., In vitro antimicrobial activity of a siderophore cephalosporin, S-649266, against Enterobacteriaceae clinical isolates, including carbapenem-resistant strains. Antimicrob. Agents Chemother. 60 (2016), 729–734, 10.1128/AAC.01695-15.
Koteva, K., King, A.M., Capretta, A., Wright, G.D., Total synthesis and activity of the metallo-β-lactamase inhibitor Aspergillomarasmine A. Angew. Chem. Int. Ed. Engl. 55 (2016), 2210–2212, 10.1002/anie.201510057.
Kuzin, A.P., Nukaga, M., Nukaga, Y., Hujer, A., Bonomo, R.A., Knox, J.R., Inhibition of the SHV-1 β-lactamase by sulfones: crystallographic observation of two reaction intermediates with tazobactam. Biochemistry 40 (2001), 1861–1866, 10.1021/bi0022745.
Lahiri, S.D., Johnstone, M.R., Ross, P.L., McLaughlin, R.E., Olivier, N.B., Alm, R.A., Avibactam and class C β-lactamases: mechanism of inhibition, conservation of the binding pocket, and implications for resistance. Antimicrob. Agents Chemother. 58 (2014), 5704–5713, 10.1128/AAC.03057-14.
Lahiri, S.D., Mangani, S., Durand-Reville, T., Benvenuti, M., De Luca, F., Sanyal, G., Docquier, J.D., Structural insight into potent broad-spectrum inhibition with reversible recyclization mechanism: Avibactam in complex with CTX-M-15 and pseudomonas aeruginosa AmpC β-lactamases. Antimicrob. Agents Chemother. 57 (2013), 2496–2505, 10.1128/AAC.02247-12.
Lahiri, S.D., Mangani, S., Jahić, H., Benvenuti, M., Durand-Reville, T.F., De Luca, F., Ehmann, D.E., Rossolini, G.M., Alm, R.A., Docquier, J.-D., Molecular basis of selective inhibition and slow reversibility of avibactam against class D carbapenemases: a structure-guided study of OXA-24 and OXA-48. ACS Chem. Biol. 10 (2015), 591–600, 10.1021/cb500703p.
Lahiri, S.D., Walkup, G.K., Whiteaker, J.D., Palmer, T., McCormack, K., Tanudra, M.A., Nash, T.J., Thresher, J., Johnstone, M.R., Hajec, L., Livchak, S., McLaughlin, R.E., Alm, R.A., Selection and molecular characterization of ceftazidime/avibactam-resistant mutants in Pseudomonas aeruginosa strains containing derepressed AmpC. J. Antimicrob. Chemother. 70 (2015), 1650–1658, 10.1093/jac/dkv004.
Lei, J., Hansen, G., Nitsche, C., Klein, C.D., Zhang, L., Hilgenfeld, R., Crystal structure of Zika virus NS2B-NS3 protease in complex with a boronate inhibitor. Science 353 (2016), 503–505, 10.1126/science.aag2419.
Liao, D., Yang, S., Wang, J., Zhang, J., Hong, B., Wu, F., Lei, X., Total synthesis and structural reassignment of aspergillomarasmine A. Angew. Chem. Int. Ed. Engl. 55 (2016), 4291–4295, 10.1002/anie.201509960.
Liénard, B.M.R., Garau, G., Horsfall, L., Karsisiotis, A.I., Damblon, C., Lassaux, P., Papamicael, C., Roberts, G.C.K., Galleni, M., Dideberg, O., Frère, J.-M., Schofield, C.J., Structural basis for the broad-spectrum inhibition of metallo-β-lactamases by thiols. Org. Biomol. Chem. 6 (2008), 2282–2294, 10.1039/b802311e.
Liu, X.-L., Shi, Y., Kang, J.S., Oelschlaeger, P., Yang, K.-W., Amino acid thioester derivatives: a highly promising scaffold for the development of metallo-β-lactamase L1 inhibitors. ACS Med. Chem. Lett. 6 (2015), 660–664, 10.1021/acsmedchemlett.5b00098.
Livermore, D.M., Mushtaq, S., Morinaka, A., Ida, T., Maebashi, K., Hope, R., Activity of carbapenems with ME1071 (disodium 2,3-diethylmaleate) against Enterobacteriaceae and Acinetobacter spp. with carbapenemases, including NDM enzymes. J. Antimicrob. Chemother. 68 (2013), 153–158, 10.1093/jac/dks350.
Livermore, D.M., Mushtaq, S., Warner, M., Miossec, C., Woodford, N., NXL104 combinations versus Enterobacteriaceae with CTX-M extended-spectrum β-lactamases and carbapenemases. J. Antimicrob. Chemother. 62 (2008), 1053–1056, 10.1093/jac/dkn320.
Livermore, D.M., Mushtaq, S., Warner, M., Woodford, N., Activity of OP0595/β-lactam combinations against Gram-negative bacteria with extended-spectrum, AmpC and carbapenem-hydrolysing β-lactamases. J. Antimicrob. Chemother. 70 (2015), 3032–3041, 10.1093/jac/dkv239.
Livermore, D.M., Warner, M., Jamrozy, D., Mushtaq, S., Nichols, W.W., Mustafa, N., Woodford, N., In vitro selection of ceftazidime-avibactam resistance in Enterobacteriaceae with KPC-3 carbapenemase. Antimicrob. Agents Chemother. 59 (2015), 5324–5330, 10.1128/AAC.00678-15.
Livermore, D.M., Warner, M., Mushtaq, S., Woodford, N., Interactions of OP0595, a novel triple-action diazabicyclooctane, with β-lactams against OP0595-resistant Enterobacteriaceae mutants. Antimicrob. Agents Chemother. 60 (2015), 554–560, 10.1128/AAC.02184-15.
Lomovskaya, O., Rubio-Aparicio, D., Sun, D., Griffith, D., Dudley, M.N., Microbiological characterization of novel broad-spectrum inhibitors of serine and metallo carbapenemases. American Society for Microbiology, 55th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC/ICC), 2015, ASM Press, San Diego, CA Abstract F-264.
Matagne, A., Ghuysen, M.F., Frère, J.M., Interactions between active-site-serine β-lactamases and mechanism-based inactivators: a kinetic study and an overview. Biochem. J., 1993, 705–711, 10.1042/bj2950705.
Mazzei, L., Cianci, M., Musiani, F., Ciurli, S., Inactivation of urease by 1,4-benzoquinone: chemistry at the protein surface. Dalton Trans. 45 (2016), 5455–5459, 10.1039/c6dt00652c.
Meini, M.-R., Llarrull, L.I., Vila, A.J., Overcoming differences: the catalytic mechanism of metallo-β-lactamases. FEBS Lett. 589 (2015), 3419–3432, 10.1016/j.febslet.2015.08.015.
Mikami, Y., Suzuki, T., Novel microbial inhibitors of angiotensin-converting enzyme. Aspergillomarasmines A and B. Agric. Biol. Chem. 47 (1983), 2693–2695, 10.1271/bbb1961.47.2693.
Mojica, M.F., Bonomo, R.A., Fast, W., B1-Metallo-β-lactamases: where do we stand?. Curr. Drug Targets 17 (2016), 1029–1050.
Mojica, M.F., Mahler, S.G., Bethel, C.R., Taracila, M.A., Kosmopoulou, M., Papp-Wallace, K.M., Llarrull, L.I., Wilson, B.M., Marshall, S.H., Wallace, C.J., Villegas, M.V., Harris, M.E., Vila, A.J., Spencer, J., Bonomo, R.A., Exploring the role of residue 228 in substrate and inhibitor recognition by VIM metallo-β-lactamases. Biochemistry 54 (2015), 3183–3196, 10.1021/acs.biochem.5b00106.
Monaco, M., Giani, T., Raffone, M., Arena, F., Garcia-Fernandez, A., Pollini, S., Grundmann, H., Pantosti, A., Rossolini, G.M., Colistin resistance superimposed to endemic carbapenem-resistant Klebsiella pneumoniae: a rapidly evolving problem in Italy, November 2013 to April 2014. Eurosurveillance, 2014, 19, 10.2807/1560-7917.ES2014.19.42.20939.
Monnaie, D., Frère, J.M., Interaction of clavulanate with class C β-lactamases. FEBS Lett. 334 (1993), 269–271, 10.1016/0014-5793(93)80692-N.
Morandi, F., Caselli, E., Morandi, S., Focia, P.J., Blázquez, J., Shoichet, B.K., Prati, F., Nanomolar inhibitors of AmpC β-lactamase. J. Am. Chem. Soc. 125 (2003), 685–695, 10.1021/ja0288338.
Morandi, S., Morandi, F., Caselli, E., Shoichet, B.K., Prati, F., Structure-based optimization of cephalothin-analogue boronic acids as β-lactamase inhibitors. Bioorg. Med. Chem. 16 (2008), 1195–1205, 10.1016/j.bmc.2007.10.075.
Morinaka, A., Tsutsumi, Y., Yamada, M., Suzuki, K., Watanabe, T., Abe, T., Furuuchi, T., Inamura, S., Sakamaki, Y., Mitsuhashi, N., Ida, T., Livermore, D.M., OP0595, a new diazabicyclooctane: mode of action as a serine β-lactamase inhibitor, antibiotic and β-lactam “enhancer”. J. Antimicrob. Chemother. 70 (2015), 2779–2786, 10.1093/jac/dkv166.
Moya, B., Barcelo, I.M., Bhagwat, S., Patel, M., Bou, G., Papp-Wallace, K.M., Bonomo, R.A., Oliver, A., WCK 5107 (zidebactam) and WCK 5153 are novel inhibitors of PBP2 showing potent “β-lactam enhancer” activity against Pseudomonas aeruginosa, including multidrug-resistant metallo-β-lactamase-producing high-risk clones. Antimicrob. Agents Chemother. 61 (2017), 16–e02529, 10.1128/AAC.02529-16.
Moynié, L., Luscher, A., Rolo, D., Pletzer, D., Tortajada, A., Weingart, H., Braun, Y., Page, M.G.P., Naismith, J.H., Köhler, T., Structure and fnction of the PiuA and PirA siderophore-drug receptors from Pseudomonas aeruginosa and Acinetobacter baumannii. Antimicrob. Agents Chemother. 61 (2017), 16–e02531, 10.1128/AAC.02531-16.
Murphy, T.A., Catto, L.E., Halford, S.E., Hadfield, A.T., Minor, W., Walsh, T.R., Spencer, J., Crystal structure of Pseudomonas aeruginosa SPM-1 provides insights into variable zinc affinity of metallo-β-lactamases. J. Mol. Biol. 357 (2006), 890–903, 10.1016/j.jmb.2006.01.003.
Mushtaq, S., Warner, M., Williams, G., Critchley, I., Livermore, D.M., Activity of chequerboard combinations of ceftaroline and NXL104 versus β-lactamase-producing Enterobacteriaceae. J. Antimicrob. Chemother. 65 (2010), 1428–1432, 10.1093/jac/dkq161.
Mushtaq, S., Woodford, N., Hope, R., Adkin, R., Livermore, D.M., Activity of BAL30072 alone or combined with β-lactamase inhibitors or with meropenem against carbapenem-resistant Enterobacteriaceae and non-fermenters. J. Antimicrob. Chemother. 68 (2013), 1601–1608, 10.1093/jac/dkt050.
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, 10.1016/j.jmb.2007.10.036.
Ness, S., Martin, R., Kindler, A.M., Paetzel, M., Gold, M., Jensen, S.E., Jones, J.B., Strynadka, N.C., Structure-based design guides the improved efficacy of deacylation transition state analogue inhibitors of TEM-1 β-lactamase. Biochemistry 39 (2000), 5312–5321, 10.1021/bi992505b.
Nordmann, P., Naas, T., Poirel, L., Global spread of carbapenemase-producing Enterobacteriaceae. Emerg. Infect. Dis. 17 (2011), 1791–1798, 10.3201/eid1710.110655.
O'Niel, J., Review on antimicrobial resistance, antimicrobial resistance: tackling a crisis for the health and wealth of Nations. Nature, 2014, 10.1038/510015a.
Olsen, L., Jost, S., Adolph, H.-W., Pettersson, I., Hemmingsen, L., Jørgensen, F.S., New leads of metallo-β-lactamase inhibitors from structure-based pharmacophore design. Bioorg. Med. Chem. 14 (2006), 2627–2635, 10.1016/j.bmc.2005.11.046.
Paech, F., Messner, S., Spickermann, J., Wind, M., Schmitt-Hoffmann, A.-H., Witschi, A.T., Howell, B.A., Church, R.J., Woodhead, J., Engelhardt, M., Krähenbühl, S., Maurer, M., Mechanisms of hepatotoxicity associated with the monocyclic β-lactam antibiotic BAL 30072. Arch. Toxicol., 2017, 10.1007/s00204-017-1994-x.
Page, M.G.P., Siderophore conjugates. Ann. N. Y. Acad. Sci. 1277 (2013), 115–126, 10.1111/nyas.12024.
Page, M.G.P., Dantier, C., Desarbre, E., Gaucher, B., Gebhardt, K., Schmitt-Hoffmann, A., In vitro and in vivo properties of BAL30376, a β-lactam and dual β-lactamase inhibitor combination with enhanced activity against Gram-negative bacilli that express multiple β-lactamases. Antimicrob. Agents Chemother. 55 (2011), 1510–1519, 10.1128/AAC.01370-10.
Palzkill, T., Metallo-β-lactamase structure and function. Ann. N. Y. Acad. Sci. 1277 (2013), 91–104, 10.1111/j.1749-6632.2012.06796.x.
Papp-Wallace, K.M., Winkler, M.L., Taracila, M.A., Bonomo, R.A., Variants of β-lactamase KPC-2 that are resistant to inhibition by avibactam. Antimicrob. Agents Chemother. 59 (2015), 3710–3717, 10.1128/AAC.04406-14.
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, 10.1016/j.tibs.2015.12.007.
Prosperi-Meys, C., Llabres, G., de Seny, D., Soto, R.P., Valladares, M.H., Laraki, N., Frere, J.M., Galleni, M., Interaction between class B β-lactamases and suicide substrates of active-site serine β-lactamases. FEBS Lett. 443 (1999), 109–111, 10.1016/S0014-5793(98)01689-5.
Rossolini, G.M., Arena, F., Pecile, P., Pollini, S., Update on the antibiotic resistance crisis. Curr. Opin. Pharmacol. 18 (2014), 56–60, 10.1016/j.coph.2014.09.006.
Rossolini, G.M., Docquier, J.-D., New β-lactamases: a paradigm for the rapid response of bacterial evolution in the clinical setting. Future Microbiol. 1 (2006), 295–308, 10.2217/17460913.1.3.295.
Scott, L.J., Ceftolozane/tazobactam: a review in complicated intra-abdominal and urinary tract infections. Drugs 76 (2016), 231–242, 10.1007/s40265-015-0524-5.
Sevaille, L., Gavara, L., Bebrone, C., De Luca, F., Nauton, L., Achard, M., Mercuri, P., Tanfoni, S., Borgianni, L., Guyon, C., Lonjon, P., Turan-Zitouni, G., Dzieciolowski, J., Becker, K., Bénard, L., Condon, C., Maillard, L., Martinez, J., Frère, J.-M., Dideberg, O., Galleni, M., Docquier, J.-D., Hernandez, J.-F., 1,2,4-triazole-3-thione compounds as inhibitors of dizinc metallo-β-lactamases. Chem. Med. Chem. 12 (2017), 972–985, 10.1002/cmdc.201700186.
Shapiro, A., Guler, S., Carter, N., Comita-Prevoir, J., McLeod, S., DeJonge, B., McLaughlin, R., Huynh, H., Gao, N., Prince, D., Ferguson, A., Velez, C., Durand-Révillle, T., Miller, A., Mueller, J., Tommasi, R., ETX2514, a novel, rationally designed inhibitor of class A, C and D β-lactamases, for the treatement of Gram-negative infections. ASM Microbe, 2016, American Society for Microbiology, Boston Abstract LB-024.
Shapiro, A.B., Gao, N., Jahić, H., Carter, N.M., Chen, A., Miller, A.A., Reversibility of covalent, broad-spectrum serine β-lactamase inhibition by the diazabicyclooctenone ETX2514. ACS Infect. Dis., 2017, s1, 10.1021/acsinfecdis.7b00113.
Shields, R.K., Chen, L., Cheng, S., Chavda, K.D., Press, E.G., Snyder, A., Pandey, R., Doi, Y., Kreiswirth, B.N., Nguyen, M.H., Clancy, C.J., Emergence of ceftazidime-avibactam resistance due to plasmid-borne blaKPC-3 mutations during treatment of carbapenem-resistant Klebsiella pneumoniae infections. Antimicrob. Agents. Chemother. 61 (2017), 16–e02097, 10.1128/AAC.02097-16.
Shields, R.K., Nguyen, M.H., Press, E.G., Chen, L., Kreiswirth, B.N., Clancy, C.J., In vitro selection of meropenem resistance among ceftazidime-avibactam-resistant, meropenem-susceptible Klebsiella pneumoniae isolates with variant KPC-3 carbapenemases. Antimicrob. Agents. Chemother. 61 (2017), 17–e00079, 10.1128/AAC.00079-17.
Sin, N., Meng, L., Wang, M.Q., Wen, J.J., Bornmann, W.G., Crews, C.M., The anti-angiogenic agent fumagillin covalently binds and inhibits the methionine aminopeptidase, MetAP-2. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 6099–6103, 10.1073/pnas.94.12.6099.
Smoum, R., Rubinstein, A., Dembitsky, V.M., Srebnik, M., Boron containing compounds as protease inhibitors. Chem. Rev. 112 (2012), 4156–4220, 10.1021/cr608202m.
Somboro, A.M., Tiwari, D., Bester, L.A., Parboosing, R., Chonco, L., Kruger, H.G., Arvidsson, P.I., Govender, T., Naicker, T., Essack, S.Y., NOTA: a potent metallo-β-lactamase inhibitor. J. Antimicrob. Chemother. 70 (2015), 1594–1596, 10.1093/jac/dku538.
Stachyra, T., Levasseur, P., Péchereau, M.C., Girard, A.M., Claudon, M., Miossec, C., Black, M.T., In vitro activity of β -lactamase inhibitor NXL104 against KPC-2 carbapenemase and Enterobacteriaceae expressing KPC carbapenemases. J. Antimicrob. Chemother. 64 (2009), 326–329, 10.1093/jac/dkp197.
Strynadka, N.C., Adachi, H., Jensen, S.E., Johns, K., Sielecki, A., Betzel, C., Sutoh, K., James, M.N., Molecular structure of the acyl-enzyme intermediate in β-lactam hydrolysis at 1.7 A resolution. Nature. 359 (1992), 700–705, 10.1038/359700a0.
Strynadka, N.C., Martin, R., Jensen, S.E., Gold, M., Jones, J.B., Structure-based design of a potent transition state analogue for TEM-1 β-lactamase. Nat. Struct. Biol. 3 (1996), 688–695, 10.1038/nsb0896-688.
Tan, L., Tao, Y., Wang, T., Zou, F., Zhang, S., Kou, Q., Niu, A., Chen, Q., Chu, W., Chen, X., Wang, H., Yang, Y., Discovery of novel pyridone-conjugated monosulfactams as potent and broad-spectrum antibiotics for multidrug-resistant Gram-negative infections. J. Med. Chem. 60 (2017), 2669–2684, 10.1021/acs.jmedchem.6b01261.
Thomas, P.W., Cammarata, M., Brodbelt, J.S., Fast, W., Covalent inhibition of New Delhi metallo-β-lactamase-1 (NDM-1) by cefaclor. Chem. Bio. Chem. 15 (2014), 2541–2548, 10.1002/cbic.201402268.
Tondi, D., Calò, S., Shoichet, B.K., Costi, M.P., Structural study of phenyl boronic acid derivatives as AmpC β-lactamase inhibitors. Bioorg. Med. Chem. Lett. 20 (2010), 3416–3419, 10.1016/j.bmcl.2010.04.007.
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, 10.1021/jm5006572.
Vallejo, J.A., Martínez-Guitián, M., Vázquez-Ucha, J.C., González-Bello, C., Poza, M., Buynak, J.D., Bethel, C.R., Bonomo, R.A., Bou, G., Beceiro, A., LN-1-255, a penicillanic acid sulfone able to inhibit the class D carbapenemase OXA-48. J. Antimicrob. Chemother. 71 (2016), 2171–2180, 10.1093/jac/dkw105.
Van Zandt, M.C., Whitehouse, D.L., Golebiowski, A., Ji, M.K., Zhang, M., Beckett, R.P., Jagdmann, G.E., Ryder, T.R., Sheeler, R., Andreoli, M., Conway, B., Mahboubi, K., D'Angelo, G., Mitschler, A., Cousido-Siah, A., Ruiz, F.X., Howard, E.I., Podjarny, A.D., Schroeter, H., Discovery of R-2-amino-6-borono-2-(2-(piperidin-1-yl)ethyl)hexanoic acid and congeners as highly potent inhibitors of human arginases I and II for treatment of myocardial reperfusion injury. J. Med. Chem. 56 (2013), 2568–2580, 10.1021/jm400014c.
Vella, P., Hussein, W.M., Leung, E.W.W., Clayton, D., Ollis, D.L., Mitić, N., Schenk, G., McGeary, R.P., The identification of new metallo-β-lactamase inhibitor leads from fragment-based screening. Bioorg. Med. Chem. Lett. 21 (2011), 3282–3285, 10.1016/j.bmcl.2011.04.027.
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, 10.1128/AAC.03108-15.
Walsh, T.R., Toleman, M.A., Poirel, L., Nordmann, P., Metallo-β-lactamases: the quiet before the storm?. Clin. Microbiol. Rev. 18 (2005), 306–325, 10.1128/CMR.18.2.306-325.2005.
Weston, G.S., Blázquez, J., Baquero, F., Shoichet, B.K., Structure-based enhancement of boronic acid-based inhibitors of AmpC β-lactamase. J. Med. Chem. 41 (1998), 4577–4586, 10.1021/jm980343w.
Winkler, M.L., Rodkey, E.A., Taracila, M.A., Drawz, S.M., Bethel, C.R., Papp-Wallace, K.M., Smith, K.M., Xu, Y., Dwulit-Smith, J.R., Romagnoli, C., Caselli, E., Prati, F., van den Akker, F., Bonomo, R.A., Design and exploration of novel boronic acid inhibitors reveals important interactions with a clavulanic acid-resistant sulfhydryl-variable (SHV) β-lactamase. J. Med. Chem. 56 (2013), 1084–1097, 10.1021/jm301490d.
World Health Organization, Antimicrobial resistance global report on surveillance 2014. World Health Organization., 2014 9789241564748.
Yamada, K., Yanagihara, K., Kaku, N., Harada, Y., Migiyama, Y., Nagaoka, K., Morinaga, Y., Nakamura, S., Imamura, Y., Miyazaki, T., Izumikawa, K., Kakeya, H., Hasegawa, H., Yasuoka, A., Kohno, S., In vivo efficacy of biapenem with ME1071, a novel metallo-β-lactamase (MBL) inhibitor, in a murine model mimicking ventilator-associated pneumonia caused by MBL-producing Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 42 (2013), 238–243, 10.1016/j.ijantimicag.2013.05.016.
Yang, S.-K., Kang, J.S., Oelschlaeger, P., Yang, K.-W., Azolylthioacetamide: A highly promising scaffold for the development of metallo-β-lactamase inhibitors. ACS Med. Chem. Lett. 6 (2015), 455–460, 10.1021/ml500534c.
Yoshizumi, A., Ishii, Y., Livermore, D.M., Woodford, N., Kimura, S., Saga, T., Harada, S., Yamaguchi, K., Tateda, K., Livermore, D.M., Efficacies of calcium-EDTA in combination with imipenem in a murine model of sepsis caused by Escherichia coli with NDM-1 β-lactamase. J. Infect. Chemother. 19 (2013), 992–995, 10.1007/s10156-012-0528-y.
Zervosen, A., Valladares, M.H., Devreese, B., Prosperi-Meys, C., Adolph, H.W., Mercuri, P.S., Vanhove, M., Amicosante, G., van Beeumen, J., Frère, J.M., Galleni, M., Inactivation of Aeromonas hydrophila metallo-è-lactamase by cephamycins and moxalactam. Eur. J. Biochem. 268 (2001), 3840–3850, 10.1046/j.1432-1327.2001.02298.x.
Zhai, L., Zhang, Y.-L., Kang, J.S., Oelschlaeger, P., Xiao, L., Nie, S.-S., Yang, K.-W., Triazolylthioacetamide: a valid scaffold for the development of New Delhi metallo-β-lactamase-1 (NDM-1) inhibitors. ACS Med. Chem. Lett. 7 (2016), 413–417, 10.1021/acsmedchemlett.5b00495.
Zhang, Y.-L., Yang, K.-W., Zhou, Y.-J., LaCuran, A.E., Oelschlaeger, P., Crowder, M.W., Diaryl-substituted azolylthioacetamides: inhibitor discovery of New Delhi metallo-β-lactamase-1 (NDM-1). ChemMedChem. 9 (2014), 2445–2448, 10.1002/cmdc.201402249.