Elucidation of critical chemical moieties of metallo-β-lactamase inhibitors and prioritisation of target metallo-β-lactamases

References

• Ventola CL. The antibiotic resistance crisis: part 2: management strategies and new agents. P T. 2015;40(5):1–13.
   Google Scholar
• Kim DW, Cha CJ. Antibiotic resistome from the one-health perspective: understanding and controlling antimicrobial resistance transmission. Exp Mol Med. 2021;53(3):301–309.
   PubMed Web of Science ®Google Scholar
• Papp-Wallace KM, Endimiani A, Taracila MA, Bonomo RA. Carbapenems: past, present, and future. Antimicrob Agents Chemother. 2011;55(11):4943–4960.
   PubMed Web of Science ®Google Scholar
• Bahr G, González LJ, Vila AJ. Metallo-β-lactamases in the age of multidrug resistance: From structure and mechanism to evolution, dissemination, and inhibitor design. Chem Rev. 2021;121(13):7957–8094.
   PubMed Web of Science ®Google Scholar
• Tooke CL, Hinchliffe P, Bragginton EC, Colenso CK, Hirvonen VHA, Takebayashi Y, Spencer J. βLactamases and β-lactamase inhibitors in the 21st century. J Mol Biol. 2019;431(18):3472–3500.
   PubMed Web of Science ®Google Scholar
• Mojica MF, Rossi MA, Vila AJ, Bonomo RA. The urgent need for metallo-β-lactamase inhibitors: an unattended global threat. Lancet Infect Dis. 2022;22(1):e28–e34.
   PubMed Web of Science ®Google Scholar
• Yang Y, Yan YH, Schofield CJ, McNally A, Zong Z, Li GB. Metallo-β-lactamase-mediated antimicrobial resistance and progress in inhibitor discovery. Trends Microbiol. 2023;31(7):735–748.
   PubMed Web of Science ®Google Scholar
• Liu B, Trout REL, Chu GH, McGarry D, Jackson RW, Hamrick JC, Daigle DM, Cusick SM, Pozzi C, De Luca F, et al. Discovery of taniborbactam (VNRX-5133): a broad-spectrum serine- and metallo-β-lactamase inhibitor for carbapenem-resistant bacterial infections. J Med Chem. 2020;63(6):2789–2801. ‘
   PubMed Web of Science ®Google Scholar
• Hecker SJ, Reddy KR, Lomovskaya O, Griffith DC, Rubio-Aparicio D, Nelson K, Tsivkovski R, Sun D, Sabet M, Tarazi Z, et al. Discovery of cyclic boronic acid QPX7728, an ultrabroad-spectrum inhibitor of serine and metallo-β-lactamases. J Med Chem. 2020;63(14):7491–7507.
   PubMed Web of Science ®Google Scholar
• Reddy KR, Parkinson J, Sabet M, Tarazi Z, Boyer SH, Lomovskaya O, Griffith DC, Hecker SJ, Dudley MN. Selection of QPX7831, an orally bioavailable prodrug of boronic acid β-lactamase inhibitor QPX7728. J Med Chem. 2021;64(23):17523–17529.
   PubMed Web of Science ®Google Scholar
• Wu W, Feng Y, Tang G, Qiao F, McNally A, Zong Z. NDM metallo-β-lactamases and their bacterial producers in health care settings. Clin Microbiol Rev. 2019;32(2):e00115-18.
   PubMed Web of Science ®Google Scholar
• Li R, Chen X, Zhou C, Dai QQ, Yang L. Recent advances in β-lactamase inhibitor chemotypes and inhibition modes. Eur J Med Chem. 2022;242:114677.
   PubMed Web of Science ®Google Scholar
• Le Terrier C, Gruenig V, Fournier C, Nordmann P, Poirel L. NDM-9 resistance to taniborbactam. Lancet Infect Dis. 2023;23(4):401–402.
   PubMed Web of Science ®Google Scholar
• Page MJ, Moher D, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, et al. Prisma 2020 explanation and elaboration: updated guidance and exemplars for reporting systematic reviews. BMJ. 2021;372:n160.
   PubMed Web of Science ®Google Scholar
• Chen C, Oelschlaeger P, Wang D, Xu H, Wang Q, Wang C, Zhao A, Yang KW. Structure and mechanism-guided design of dual serine/metallo-carbapenemase inhibitors. J Med Chem. 2022;65(8):5954–5974.
   PubMed Web of Science ®Google Scholar
• Brem J, Panduwawala T, Hansen JU, Hewitt J, Liepins E, Donets P, Espina L, Farley AJM, Shubin K, Campillos GG, et al. Imitation of β-lactam binding enables broad-spectrum metallo-β-lactamase inhibitors. Nat Chem. 2022;14(1):15–24.
   PubMed Web of Science ®Google Scholar
• Alcock BP, Huynh W, Chalil R, Smith KW, Raphenya AR, Wlodarski MA, Edalatmand A, Petkau A, Syed SA, Tsang KK, et al. CARD 2023: expanded curation, support for machine learning, and resistome prediction at the comprehensive antibiotic resistance database. Nucleic Acids Res. 2023;51(D1):D690–D699.
   PubMed Web of Science ®Google Scholar
• Hall BG. Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol. 2013;30(5):1229–1235.
   PubMed Web of Science ®Google Scholar
• Iwai S, Chai B, Sul WJ, Cole JR, Hashsham SA, Tiedje JM. Gene-targeted-metagenomics reveals extensive diversity of aromatic dioxygenase genes in the environment. Isme J. 2010;4(2):279–285.
   PubMed Web of Science ®Google Scholar
• Letunic I, Bork P. Interactive Tree of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49(W1):W293–W296.
   PubMed Web of Science ®Google Scholar
• Wang X, Lu M, Shi Y, Ou Y, Cheng X. Discovery of novel New Delhi metallo-β-lactamases-1 inhibitors by multistep virtual screening. PLoS One. 2015;10(3):e0118290.
   PubMed Web of Science ®Google Scholar
• Li GB, Abboud MI, Brem J, Someya H, Lohans CT, Yang SY, Spencer J, Wareham DW, McDonough MA, Schofield CJ. NMR-filtered virtual screening leads to non-metal chelating metallo-β-lactamase inhibitors. Chem Sci. 2017;8(2):928–937.
   PubMed Web of Science ®Google Scholar
• Spyrakis F, Celenza G, Marcoccia F, Santucci M, Cross S, Bellio P, Cendron L, Perilli M, Tondi D. Structure-based virtual screening for the discovery of novel inhibitors of New Delhi metallo-β-lactamase-1. ACS Med Chem Lett. 2018;9(1):45–50.
   PubMed Web of Science ®Google Scholar
• Shi C, Bao J, Sun Y, Kang X, Lao X, Zheng H. Discovery of baicalin as NDM-1 inhibitor: virtual screening, biological evaluation and molecular simulation. Bioorg Chem. 2019;88:102953.
   PubMed Web of Science ®Google Scholar
• Wang X, Yang Y, Gao Y, Niu X. Discovery of the novel inhibitor against New Delhi metallo-β-lactamase based on virtual screening and molecular modelling. Int J Mol Sci. 2020;21(10):3567.
   PubMed Web of Science ®Google Scholar
• Brindisi M, Brogi S, Giovani S, Gemma S, Lamponi S, De Luca F, Novellino E, Campiani G, Docquier JD, Butini S. Targeting clinically-relevant metallo-β-lactamases: from high-throughput docking to broad-spectrum inhibitors. J Enzyme Inhib Med Chem. 2016;31(sup1):98–109.
   PubMed Web of Science ®Google Scholar
• Thomas PW, Spicer T, Cammarata M, Brodbelt JS, Hodder P, Fast W. An altered zinc-binding site confers resistance to a covalent inactivator of New Delhi metallo-β-lactamase-1 (NDM-1) discovered by high-throughput screening. Bioorg Med Chem. 2013;21(11):3138–3146.
   PubMed Web of Science ®Google Scholar
• Betts JW, Phee LM, Abdul Momin MHF, Umland K-D, Brem J, Schofield CJ, Wareham DW. In vitro and in vivo activity of ML302F: a thioenolate inhibitor of VIM-subfamily metallo β-lactamases. Med Chem Commun. 2016;7(1):190–193.
   Google Scholar
• Cain R, Brem J, Zollman D, McDonough MA, Johnson RM, Spencer J, Makena A, Abboud MI, Cahill S, Lee SY, et al. In silico fragment-based design identifies subfamily B1 metallo-β-lactamase inhibitors. J Med Chem. 2018;61(3):1255–1260.
   PubMed Web of Science ®Google Scholar
• Caburet J, Boucherle B, Bourdillon S, Simoncelli G, Verdirosa F, Docquier JD, Moreau Y, Krimm I, Crouzy S, Peuchmaur M. A fragment-based drug discovery strategy applied to the identification of NDM-1 β-lactamase inhibitors. Eur J Med Chem. 2022;240:114599.
   PubMed Web of Science ®Google Scholar
• Vella P, Hussein WM, Leung EWW, Clayton D, Ollis DL, Mitić N, Schenk G, McGeary RP. The identification of new metallo-β-lactamase inhibitor leads from fragment-based screening. Bioorg Med Chem Lett. 2011;21(11):3282–3285.
   PubMed Web of Science ®Google Scholar
• Christopeit T, Leiros HK. Fragment-based discovery of inhibitor scaffolds targeting the metallo-β-lactamases NDM-1 and VIM-2. Bioorg Med Chem Lett. 2016;26(8):1973–1977.
   PubMed Web of Science ®Google Scholar
• Yang Y, Guo Y, Zhou Y, Gao Y, Wang X, Wang J, Niu X. Discovery of a novel natural allosteric inhibitor that targets NDM-1 against Escherichia coli. Front Pharmacol. 2020;11:581001.
   PubMed Web of Science ®Google Scholar
• Somboro AM, Osei Sekyere J, Amoako DG, Kumalo HM, Khan R, Bester LA, Essack SY. In vitro potentiation of carbapenems with tannic acid against carbapenemase-producing enterobacteriaceae: exploring natural products as potential carbapenemase inhibitors. J Appl Microbiol. 2019;126(2):452–467.
   PubMed Web of Science ®Google Scholar
• Davies DT, Leiris S, Sprynski N, Castandet J, Lozano C, Bousquet J, Zalacain M, Vasa S, Dasari PK, Pattipati R, et al. ANT2681: SAR studies leading to the identification of a metallo-β-lactamase inhibitor with potential for clinical use in combination with meropenem for the treatment of infections caused by NDM-producing Enterobacteriaceae. ACS Infect Dis. 2020;6(9):2419–2430.
   PubMed Web of Science ®Google Scholar
• Leiris S, Coelho A, Castandet J, Bayet M, Lozano C, Bougnon J, Bousquet J, Everett M, Lemonnier M, Sprynski N, et al. SAR studies leading to the identification of a novel series of metallo-β-lactamase inhibitors for the treatment of carbapenem-resistant enterobacteriaceae infections that display efficacy in an animal infection model. ACS Infect Dis. 2019;5(1):131–140.
   PubMed Web of Science ®Google Scholar
• Grigorenko VG, Khrenova MG, Andreeva IP, Rubtsova MY, Lev AI, Novikova TS, Detusheva EV, Fursova NK, Dyatlov IA, Egorov AM. Drug repurposing of the unithiol: inhibition of metallo-β-lactamases for the treatment of carbapenem-resistant Gram-negative bacterial infections. Int J Mol Sci. 2022;23(3):1834..
   PubMed Web of Science ®Google Scholar
• Liu Y, Yang K, Jia Y, Wang Z. Repurposing peptidomimetic as potential inhibitor of New Delhi metallo-β-lactamases in Gram-negative bacteria. ACS Infect Dis. 2019;5(12):2061–2066.
   PubMed Web of Science ®Google Scholar
• Muteeb G, Alsultan A, Farhan M, Aatif M. Risedronate and methotrexate are high-affinity inhibitors of New Delhi metallo-β-lactamase-1 (NDM-1): a drug repurposing approach. Molecules. 2022;27(4):1283.
   PubMed Web of Science ®Google Scholar
• Sychantha D, Rotondo CM, Tehrani K, Martin NI, Wright GD. Aspergillomarasmine a inhibits metallo-β-lactamases by selectively sequestering Zn2. J Biol Chem. 2021;297(2):100918.
   PubMed Web of Science ®Google Scholar
• King AM, Reid-Yu SA, Wang W, King DT, De Pascale G, Strynadka NC, Walsh TR, Coombes BK, Wright GD. Aspergillomarasmine A overcomes metallo-β-lactamase antibiotic resistance. Nature. 2014;510(7506):503–506.
   PubMed Web of Science ®Google Scholar
• Rotondo CM, Sychantha D, Koteva K, Wright GD. Suppression of β-lactam resistance by aspergillomarasmine A is influenced by both the metallo-β-lactamase target and the antibiotic partner. Antimicrob Agents Chemother. 2020;64(4):e01386–19.
   PubMed Web of Science ®Google Scholar
• Zhang J, Wang S, Wei Q, Guo Q, Bai Y, Yang S, Song F, Zhang L, Lei X. Synthesis and biological evaluation of aspergillomarasmine A derivatives as novel NDM-1 inhibitor to overcome antibiotics resistance. Bioorg Med Chem. 2017;25(19):5133–5141.
   PubMed Web of Science ®Google Scholar
• Koteva K, King AM, Capretta A, Wright GD. Total synthesis and activity of the metallo-β-lactamase inhibitor aspergillomarasmine. Angew Chem Int Ed Engl. 2016;55(6):2210–2212.
   PubMed Web of Science ®Google Scholar
• Bergstrom A, Katko A, Adkins Z, Hill J, Cheng Z, Burnett M, Yang H, Aitha M, Mehaffey MR, Brodbelt JS, et al. Probing the interaction of aspergillomarasmine A with metallo-β-lactamases NDM-1, VIM-2, and IMP-7. ACS Infect Dis. 2018;4(2):135–145.
   PubMed Web of Science ®Google Scholar
• Albu SA, Koteva K, King AM, Al-Karmi S, Wright GD, Capretta A. Total synthesis of aspergillomarasmine A and related compounds: a sulfamidate approach enables exploration of structure-activity relationships. Angew Chem Int Ed Engl. 2016;55(42):13259–13262.
   PubMed Web of Science ®Google Scholar
• Yoshizumi A, Ishii Y, Livermore DM, Woodford N, Kimura S, Saga T, Harada S, Yamaguchi K, Tateda K. 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. 2013;19(5):992–995.
   PubMed Web of Science ®Google Scholar
• Aoki N, Ishii Y, Tateda K, Saga T, Kimura S, Kikuchi Y, Kobayashi T, Tanabe Y, Tsukada H, Gejyo F, et al. Efficacy of calcium-EDTA as an inhibitor for metallo-β-lactamase in a mouse model of Pseudomonas aeruginosa pneumonia. Antimicrob Agents Chemother. 2010;54(11):4582–4588.
   PubMed Web of Science ®Google Scholar
• Zhang E, Wang MM, Huang SC, Xu SM, Cui DY, Bo YL, Bai PY, Hua YG, Xiao CL, Qin S. Nota analogue: A first dithiocarbamate inhibitor of metallo-β-lactamases. Bioorg Med Chem Lett. 2018;28(2):214–221.
   PubMed Web of Science ®Google Scholar
• Somboro AM, Tiwari D, Bester LA, Parboosing R, Chonco L, Kruger HG, Arvidsson PI, Govender T, Naicker T, Essack SY. NOTA: a potent metallo-β-lactamase inhibitor. J Antimicrob Chemother. 2015;70(5):1594–1596.
   PubMed Web of Science ®Google Scholar
• Chen AY, Thomas PW, Stewart AC, Bergstrom A, Cheng Z, Miller C, Bethel CR, Marshall SH, Credille CV, Riley CL, et al. Dipicolinic acid derivatives as inhibitors of New Delhi metallo-β-lactamase-1. J Med Chem. 2017;60(17):7267–7283.
   PubMed Web of Science ®Google Scholar
• Chen AY, Thomas PW, Cheng Z, Xu NY, Tierney DL, Crowder MW, Fast W, Cohen SM. Investigation of dipicolinic acid isosteres for the inhibition of metallo-β-lactamases. ChemMedChem. 2019;14(13):1271–1282.
   PubMed Web of Science ®Google Scholar
• Lomovskaya O, Tsivkovski R, Nelson K, Rubio-Aparicio D, Sun D, Totrov M, Dudley MN. Spectrum of β-lactamase inhibition by the cyclic boronate QPX7728, an ultrabroad-spectrum β-lactamase inhibitor of serine and metallo-β-lactamases: enhancement of activity of multiple antibiotics against isogenic strains expressing single β-lactamases. Antimicrob Agents Chemother. 2020;64(6):e00212-20.
   PubMed Web of Science ®Google Scholar
• Nelson K, Rubio-Aparicio D, Sun D, Dudley M, Lomovskaya O. In vitro activity of the ultrabroad-spectrum-β-lactamase inhibitor QPX7728 against carbapenem-resistant enterobacterales with varying intrinsic and acquired resistance mechanisms. Antimicrob Agents Chemother. 2020;64(8):e00757-20.
   PubMed Web of Science ®Google Scholar
• Nelson K, Rubio-Aparicio D, Tsivkovski R, Sun D, Totrov M, Dudley M, Lomovskaya O. In vitro activity of the ultra-broad-spectrum β-lactamase inhibitor QPX7728 in combination with meropenem against clinical isolates of carbapenem-resistant Acinetobacter baumannii. Antimicrob Agents Chemother. 2020;64(11):e01406-20.
   PubMed Web of Science ®Google Scholar
• Tsivkovski R, Totrov M, Lomovskaya O. Biochemical characterization of QPX7728, a new ultrabroad-spectrum β-lactamase inhibitor of serine and metallo-β-lactamases. Antimicrob Agents Chemother. 2020;64(6):e00130-20.
   PubMed Web of Science ®Google Scholar
• Lomovskaya O, Rubio-Aparicio D, Nelson K, Sun D, Tsivkovski R, Castanheira M, Lindley J, Loutit J, Dudley M. In vitro activity of the ultrabroad-spectrum β-lactamase inhibitor QPX7728 in combination with multiple β-lactam antibiotics against Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2021;65(6):e00210-21.
   PubMed Web of Science ®Google Scholar
• Lomovskaya O, Rubio-Aparicio D, Tsivkovski R, Loutit J, Dudley M. The ultrabroad-spectrum β-lactamase inhibitor QPX7728 restores the potency of multiple oral β-lactam antibiotics against β-lactamase-producing strains of resistant enterobacterales. Antimicrob Agents Chemother. 2022;66(2):e0216821.
   PubMed Web of Science ®Google Scholar
• Krajnc A, Brem J, Hinchliffe P, Calvopiña K, Panduwawala TD, Lang PA, Kamps J, Tyrrell JM, Widlake E, Saward BG, et al. Bicyclic boronate VNRX-5133 inhibits metallo- and serine-β-lactamases. J Med Chem. 2019;62(18):8544–8556.
   PubMed Web of Science ®Google Scholar
• Hamrick JC, Docquier JD, Uehara T, Myers CL, Six DA, Chatwin CL, John KJ, Vernacchio SF, Cusick SM, Trout REL, et al. VNRX-5133 (taniborbactam), a broad-spectrum inhibitor of serine- and metallo-β-lactamases, restores activity of cefepime in enterobacterales and Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2020;64(3):e01963-19.
   PubMed Web of Science ®Google Scholar
• Weide T, Saldanha SA, Minond D, Spicer TP, Fotsing JR, Spaargaren M, Frère JM, Bebrone C, Sharpless KB, Hodder PS, et al. NH-1,2,3-triazole-based inhibitors of the VIM-2 metallo-β-lactamase: synthesis and structure-activity studies. ACS Med Chem Lett. 2010;1(4):150–154.
   PubMed Web of Science ®Google Scholar
• Wade N, Tehrani K, Brüchle NC, van Haren MJ, Mashayekhi V, Martin NI. Mechanistic investigations of metallo-β-lactamase inhibitors: strong zinc binding is not required for potent enzyme inhibition. ChemMedChem. 2021;16(10):1651–1659.
   PubMed Web of Science ®Google Scholar
• Torelli NJ, Akhtar A, DeFrees K, Jaishankar P, Pemberton OA, Zhang X, Johnson C, Renslo AR, Chen Y. Active-site druggability of carbapenemases and broad-spectrum inhibitor discovery. ACS Infect Dis. 2019;5(6):1013–1021.
   PubMed Web of Science ®Google Scholar
• Dai Q, Yan Y, Ning X, Li G, Yu J, Deng J, Yang L, Li GB. Ancphore: a versatile tool for anchor pharmacophore steered drug discovery with applications in discovery of new inhibitors targeting metallo-β-lactamases and indoleamine/tryptophan 2,3-dioxygenases. Acta Pharm Sin B. 2021;11(7):1931–1946.
   PubMed Web of Science ®Google Scholar
• Legru A, Verdirosa F, Hernandez JF, Tassone G, Sannio F, Benvenuti M, Conde PA, Bossis G, Thomas CA, Crowder MW, et al. 1,2,4-Triazole-3-thione compounds with a 4-ethyl alkyl/aryl sulfide substituent are broad-spectrum metallo-β-lactamase inhibitors with re-sensitization activity. Eur J Med Chem. 2021;226:113873.
   PubMed Web of Science ®Google Scholar
• Gavara L, Sevaille L, De Luca F, Mercuri P, Bebrone C, Feller G, Legru A, Cerboni G, Tanfoni S, Baud D, et al. 4-Amino-1,2,4-triazole-3-thione-derived schiff bases as metallo-β-lactamase inhibitors. Eur J Med Chem. 2020;208:112720.
   PubMed Web of Science ®Google Scholar
• Yang SK, Kang JS, Oelschlaeger P, Yang KW. Azolylthioacetamide: a highly promising scaffold for the development of metallo-β-lactamase inhibitors. ACS Med Chem Lett. 2015;6(4):455–460.
   PubMed Web of Science ®Google Scholar
• Xiang Y, Chang YN, Ge Y, Kang JS, Zhang YL, Liu XL, Oelschlaeger P, Yang KW. Azolylthioacetamides as a potent scaffold for the development of metallo-β-lactamase inhibitors. Bioorg Med Chem Lett. 2017;27(23):5225–5229.
   PubMed Web of Science ®Google Scholar
• Liu XL, Xiang Y, Chen C, Yang KW. Azolylthioacetamides as potential inhibitors of New Delhi metallo-β-lactamase-1 (NDM-1). J Antibiot (Tokyo)). 2019;72(2):118–121.
   PubMed Web of Science ®Google Scholar
• Feng L, Yang KW, Zhou LS, Xiao JM, Yang X, Zhai L, Zhang YL, Crowder MW. N-heterocyclic dicarboxylic acids: Broad-spectrum inhibitors of metallo-β-lactamases with co-antibacterial effect against antibiotic-resistant bacteria. Bioorg Med Chem Lett. 2012;22(16):5185–5189.
   PubMed Web of Science ®Google Scholar
• Shin WS, Bergstrom A, Bonomo RA, Crowder MW, Muthyala R, Sham YY. Discovery of 1-hydroxypyridine-2(1h)-thione-6-carboxylic acid as a first-in-class low-cytotoxic nanomolar metallo β-lactamase inhibitor. ChemMedChem. 2017;12(11):845–849.
   PubMed Web of Science ®Google Scholar
• Hinchliffe P, Tanner CA, Krismanich AP, Labbé G, Goodfellow VJ, Marrone L, Desoky AY, Calvopiña K, Whittle EE, Zeng F, et al. Structural and kinetic studies of the potent inhibition of metallo-β-lactamases by 6-phosphonomethylpyridine-2-carboxylates. Biochemistry. 2018;57(12):1880–1892.
   PubMed Web of Science ®Google Scholar
• Wang Q, He Y, Lu R, Wang WM, Yang KW, Fan HM, Jin Y, Blackburn GM. Thermokinetic profile of NDM-1 and its inhibition by small carboxylic acids. Biosci Rep. 2018;38(2):BSR20180244.
   PubMedGoogle Scholar
• Shi XF, Wang MM, Huang SC, Han JX, Chu WC, Xiao C, Zhang E, Qin S. H(2)depda: an acyclic adjuvant potentiates meropenem activity in vitro against metallo-β-lactamase-producing enterobacterales. Eur J Med Chem. 2019;167:367–376.
   PubMed Web of Science ®Google Scholar
• Jackson AC, Zaengle-Barone JM, Puccio EA, Franz KJ. A cephalosporin prochelator inhibits new delhi metallo-β-lactamase 1 without removing zinc. ACS Infect Dis. 2020;6(5):1264–1272.
   PubMed Web of Science ®Google Scholar
• Thomas CA, Cheng Z, Yang K, Hellwarth E, Yurkiewicz CJ, Baxter FM, Fullington SA, Klinsky SA, Otto JL, Chen AY, et al. Probing the mechanisms of inhibition for various inhibitors of metallo-β-lactamases VIM-2 and NDM-1. J Inorg Biochem. 2020;210:111123.
   PubMed Web of Science ®Google Scholar
• Gao H, Li JQ, Kang PW, Chigan JZ, Wang H, Liu L, Xu YS, Zhai L, Yang KW. N-acylhydrazones confer inhibitory efficacy against New Delhi metallo-β-lactamase-1. Bioorg Chem. 2021;114:105138.
   PubMed Web of Science ®Google Scholar
• Li JQ, Sun LY, Jiang Z, Chen C, Gao H, Chigan JZ, Ding HH, Yang KW. Diaryl-substituted thiosemicarbazone: a potent scaffold for the development of New Delhi metallo-β-lactamase-1 inhibitors. Bioorg Chem. 2021;107:104576.
   PubMed Web of Science ®Google Scholar
• Klingler FM, Wichelhaus TA, Frank D, Cuesta-Bernal J, El-Delik J, Müller HF, Sjuts H, Göttig S, Koenigs A, Pos KM, et al. Approved drugs containing thiols as inhibitors of metallo-β-lactamases: strategy to combat multidrug-resistant bacteria. J Med Chem. 2015;58(8):3626–3630.
   PubMed Web of Science ®Google Scholar
• Wachino J, 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. 2016;60(7):4274–4282.
   PubMed Web of Science ®Google Scholar
• Brem J, van Berkel SS, Zollman D, Lee SY, Gileadi O, McHugh PJ, Walsh TR, McDonough MA, Schofield CJ. Structural basis of metallo-β-lactamase inhibition by captopril stereoisomers. Antimicrob Agents Chemother. 2016;60(1):142–150.
   PubMed Web of Science ®Google Scholar
• Yusof Y, Tan DTC, Arjomandi OK, Schenk G, McGeary RP. Captopril analogues as metallo-β-lactamase inhibitors. Bioorg Med Chem Lett. 2016;26(6):1589–1593.
   PubMed Web of Science ®Google Scholar
• Tehrani KHME, Martin NI. Thiol-containing metallo-β-lactamase inhibitors resensitize resistant Gram-negative bacteria to meropenem. ACS Infect Dis. 2017;3(10):711–717.
   PubMed Web of Science ®Google Scholar
• Ma G, Wang S, Wu K, Zhang W, Ahmad A, Hao Q, Lei X, Zhang H. Structure-guided optimization of D-captopril for discovery of potent NDM-1 inhibitors. Bioorg Med Chem. 2021;29:115902.
   PubMed Web of Science ®Google Scholar
• 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. 2010;54(9):3625–3629.
   PubMed Web of Science ®Google Scholar
• Livermore DM, 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. 2013;68(1):153–158.
   PubMed Web of Science ®Google Scholar
• Yamada K, Yanagihara K, Kaku N, Harada Y, Migiyama Y, Nagaoka K, Morinaga Y, Nakamura S, Imamura Y, Miyazaki T, et al. 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. 2013;42(3):238–243.
   PubMed Web of Science ®Google Scholar
• Hiraiwa Y, Morinaka A, Fukushima T, Kudo T. Metallo-β-lactamase inhibitory activity of 3-alkyloxy and 3-amino phthalic acid derivatives and their combination effect with carbapenem. Bioorg Med Chem. 2013;21(18):5841–5850.
   PubMed Web of Science ®Google Scholar
• 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. 2014;24(20):4891–4894.
   PubMed Web of Science ®Google Scholar
• Li N, Xu Y, Xia Q, Bai C, Wang T, Wang L, He D, Xie N, Li L, Wang J, et al. Simplified captopril analogues as NDM-1 inhibitors. Bioorg Med Chem Lett. 2014;24(1):386–389.
   PubMed Web of Science ®Google Scholar
• Parkova A, Lucic A, Krajnc A, Brem J, Calvopiña K, Langley GW, McDonough MA, Trapencieris P, Schofield CJ. Broad spectrum β-lactamase inhibition by a thioether substituted bicyclic boronate. ACS Infect Dis. 2020;6(6):1398–1404.
   PubMed Web of Science ®Google Scholar
• Everett M, Sprynski N, Coelho A, Castandet J, Bayet M, Bougnon J, Lozano C, Davies DT, Leiris S, Zalacain M, et al. Discovery of a novel metallo-β-lactamase inhibitor that potentiates meropenem activity against carbapenem-resistant Enterobacteriaceae. Antimicrob Agents Chemother. 2018;62(5):e00074-18.
   PubMed Web of Science ®Google Scholar
• Zalacain M, Lozano C, Llanos A, Sprynski N, Valmont T, De Piano C, Davies D, Leiris S, Sable C, Ledoux A, et al. Novel specific metallo-β-lactamase inhibitor ANT2681 restores meropenem activity to clinically effective levels against NDM-positive Enterobacterales. Antimicrob Agents Chemother. 2021;65(6):e00203-21.
   PubMed Web of Science ®Google Scholar
• González MM, Kosmopoulou M, Mojica MF, Castillo V, Hinchliffe P, Pettinati I, Brem J, Schofield CJ, Mahler G, Bonomo RA, et al. Bisthiazolidines: a substrate-mimicking scaffold as an inhibitor of the NDM-1 carbapenemase. ACS Infect Dis. 2015;1(11):544–554.
   PubMed Web of Science ®Google Scholar
• Hinchliffe P, González MM, Mojica MF, González JM, Castillo V, Saiz C, Kosmopoulou M, Tooke CL, Llarrull LI, Mahler G, et al. Cross-class metallo-β-lactamase inhibition by bisthiazolidines reveals multiple binding modes. Proc Natl Acad Sci U S A. 2016;113(26):E3745–3754.
   PubMed Web of Science ®Google Scholar
• Rossi MA, Martinez V, Hinchliffe P, Mojica MF, Castillo V, Moreno DM, Smith R, Spellberg B, Drusano GL, Banchio C, et al. 2-Mercaptomethyl-thiazolidines use conserved aromatic-S interactions to achieve broad-range inhibition of metallo-β-lactamases. Chem Sci. 2021;12(8):2898–2908.
   PubMed Web of Science ®Google Scholar
• Yang KW, Feng L, Yang SK, Aitha M, LaCuran AE, Oelschlaeger P, Crowder MW. New β-phospholactam as a carbapenem transition state analog: synthesis of a broad-spectrum inhibitor of metallo-β-lactamases. Bioorg Med Chem Lett. 2013;23(21):5855–5859.
   PubMed Web of Science ®Google Scholar
• Lassaux P, Hamel M, Gulea M, Delbrück H, Mercuri PS, Horsfall L, Dehareng D, Kupper M, Frère JM, Hoffmann K, et al. Mercaptophosphonate compounds as broad-spectrum inhibitors of the metallo-β-lactamases. J Med Chem. 2010;53(13):4862–4876.
   PubMed Web of Science ®Google Scholar
• Liu S, Zhou Y, Niu X, Wang T, Li J, Liu Z, Wang J, Tang S, Wang Y, Deng X. Magnolol restores the activity of meropenem against NDM-1-producing escherichia coli by inhibiting the activity of metallo-β-lactamase. Cell Death Discov. 2018;4:28.
   PubMed Web of Science ®Google Scholar
• Guo Y, Yang Y, Xu X, Li L, Zhou Y, Jia G, Wei L, Yu Q, Wang J. Metallo-β-lactamases inhibitor fisetin attenuates meropenem resistance in NDM-1-producing Escherichia coli. Eur J Med Chem. 2022;231:114108.
   PubMed Web of Science ®Google Scholar
• Romero E, Oueslati S, Benchekroun M, D'Hollander ACA, Ventre S, Vijayakumar K, Minard C, Exilie C, Tlili L, Retailleau P, et al. Azetidinimines as a novel series of non-covalent broad-spectrum inhibitors of β-lactamases with submicromolar activities against carbapenemases KPC-2 (class A), NDM-1 (class B) and OXA-48 (class D). Eur J Med Chem. 2021;219:113418.
   PubMed Web of Science ®Google Scholar
• Naas T, Oueslati S, Bonnin RA, Dabos ML, Zavala A, Dortet L, Retailleau P, Iorga BI. Beta-lactamase database (BLDB) - structure and function. J Enzyme Inhib Med Chem. 2017;32(1):917–919.
   PubMed Web of Science ®Google Scholar
• Piccirilli A, Segatore B, Brisdelli F, Amicosante G, Perilli M. Potent inhibitory activity of taniborbactam towards NDM-1 and NDM-1(Q119X) mutants, and in vitro activity of cefepime/taniborbactam against mbls producing enterobacterales. Int J Antimicrob Agents. 2021;57(1):106228.
   PubMed Web of Science ®Google Scholar
• 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. 2013;57(1):101–109.
   PubMed Web of Science ®Google Scholar
• Lomovskaya O, Tsivkovski R, Totrov M, Dressel D, Castanheira M, Dudley M. New boronate drugs and evolving NDM-mediated β-lactam resistance. Antimicrob Agents Chemother. 2023;67(9):e0057923.
   PubMed Web of Science ®Google Scholar
• Qin Y, Duan X, Peng Y, Rui Y. Rapid detection of a novel B1-β-lactamase gene, blaAFM-1 using a loop-mediated isothermal amplification (LAMP) assay. Ann Clin Microbiol Antimicrob. 2021;20(1):80.
   PubMed Web of Science ®Google Scholar
• Teufel F, Almagro Armenteros JJ, Johansen AR, Gíslason MH, Pihl SI, Tsirigos KD, Winther O, Brunak S, von Heijne G, Nielsen H. SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol. 2022;40(7):1023–1025.
   PubMed Web of Science ®Google Scholar