Antibiotic adjuvants: an alternative approach to overcome multi-drug resistant Gram-negative bacteria

Reference

• AbuOun M, Stubberfield EJ, Duggett NA, Kirchner M, Dormer L, Nunez-Garcia J, Randall LP, Lemma F, Crook DW, Teale C, et al. 2017. mcr-1 and mcr-2 variant genes identified in Moraxella species isolated from pigs in Great Britain from 2014 to 2015. J Antimicrob Chemother. 72:2745–2749.
   PubMed Web of Science ®Google Scholar
• Alam MK, Alhhazmi A, DeCoteau JF, Luo Y, Geyer CR. 2016. RecA inhibitors potentiate antibiotic activity and block evolution of antibiotic resistance. Cell Chem Biol. 23:381–391.
   PubMed Web of Science ®Google Scholar
• Ayhan DH, Tamer YT, Akbar M, Bailey SM, Wong M, Daly SM, Greenberg DE, Toprak E. 2016. Sequence-specific targeting of bacterial resistance genes increases antibiotic efficacy. PLoS Biol. 14:e1002552.
   PubMed Web of Science ®Google Scholar
• Blair JM, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJ. 2015. Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol. 13:42–51.
   PubMed Web of Science ®Google Scholar
• Bonomo RA. 2017. β-Lactamases: a focus on current challenges. Cold Spring Harb Perspect Med. 7:a025239.
   PubMed Web of Science ®Google Scholar
• Borowiak M, Fischer J, Hammerl JA, Hendriksen RS, Szabo I, Malorny B. 2017. Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting Salmonella enterica subsp. enterica serovar Paratyphi B. J Antimicrob Chemother. 72:3317–3324.
   PubMed Web of Science ®Google Scholar
• Brochado AR, Telzerow A, Bobonis J, Banzhaf M, Mateus A, Selkrig J, Huth E, Bassler S, Zamarreno Beas J, Zietek M, et al. 2018. Species-specific activity of antibacterial drug combinations. Nature. 559:259–263.
   PubMed Web of Science ®Google Scholar
• Brown ED. 2015. Gram-negative resistance. ACS Infect Dis. 1:507.
   PubMed Web of Science ®Google Scholar
• Brown ED, Wright GD. 2016. Antibacterial drug discovery in the resistance era. Nature. 529:336–343.
   PubMed Web of Science ®Google Scholar
• Carattoli A, Villa L, Feudi C, Curcio L, Orsini S, Luppi A, Pezzotti G, Magistrali CF. 2017. Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Euro Surveill. 22:30589.
   PubMedGoogle Scholar
• Cardona ST, Choy M, Hogan AM. 2018. Essential two-component systems regulating cell envelope functions: opportunities for novel antibiotic therapies. J Membr Biol. 251:75–89.
   PubMed Web of Science ®Google Scholar
• Cornaglia G, Giamarellou H, Rossolini GM. 2011. Metallo-β-lactamases: a last frontier for β-lactams? Lancet Infect Dis. 11:381.
   PubMed Web of Science ®Google Scholar
• Czaplewski L, Bax R, Clokie M, Dawson M, Fairhead H, Fischetti VA, Foster S, Gilmore BF, Hancock REW, Harper D, et al. 2016. Alternatives to antibiotics-a pipeline portfolio review. Lancet Infect Dis. 16:239–251.
   PubMed Web of Science ®Google Scholar
• Daly SM, Sturge CR, Felder-Scott CF, Geller BL, Greenberg DE. 2017. MCR-1 inhibition with peptide-conjugated phosphorodiamidate morpholino oligomers restores sensitivity to polymyxin in Escherichia coli. MBio. 8:e01315–e01317.
   PubMed Web of Science ®Google Scholar
• Djoko K, Achard M, Phan M, Lo A, Miraula M, Prombhul S, Hancock S, Peters K, Sidjabat H, Harris P, et al. 2018. Copper ions and coordination complexes as novel carbapenem adjuvants. Antimicrob Agents Chemother. 62:AAC.02280–02217.
   Web of Science ®Google Scholar
• Domalaon R, Idowu T, Zhanel GG, Schweizer F. 2018a. Antibiotic hybrids: the next generation of agents and adjuvants against Gram-negative pathogens? Clin Microbiol Rev. 31:e00077–e00017.
   PubMed Web of Science ®Google Scholar
• Domalaon R, Sanchak Y, Koskei L, Lyu Y, Zhanel G, Arthur G, Schweizer F. 2018b. Short proline-rich lipopeptide potentiates minocycline and rifampin against multidrug- and extensively drug-resistant Pseudomonas aeruginosa. Antimicrobial Agents Chemother. 62:e02374–e02317.
   PubMed Web of Science ®Google Scholar
• Durand-Réville TF, Guler S, Comita-Prevoir J, Chen B, Bifulco N, Huynh H, Lahiri S, Shapiro AB, McLeod SM, Carter NM, et al. 2017. ETX2514 is a broad-spectrum β-lactamase inhibitor for the treatment of drug-resistant Gram-negative bacteria including Acinetobacter baumannii. Nat Microbiol. 2:17104.
   PubMed Web of Science ®Google Scholar
• Ehmann DE, Jahić H, Ross PL, Gu R-F, Hu J, Kern G, Walkup GK, Fisher SL. 2012. Avibactam is a covalent, reversible, non-β-lactam β-lactamase inhibitor. Proc Natl Acad Sci USA. 109:11663–11668.
   PubMed Web of Science ®Google Scholar
• Ejim L, Farha MA, Falconer SB, Wildenhain J, Coombes BK, Tyers M, Brown ED, Wright GD. 2011. Combinations of antibiotics and nonantibiotic drugs enhance antimicrobial efficacy. Nat Chem Biol. 7:348.
   PubMed Web of Science ®Google Scholar
• El-Halfawy O, Klett J, Ingram R, Loutet S, Murphy M, Martín-Santamaría S, Valvano M. 2017. Antibiotic capture by bacterial lipocalins uncovers an extracellular mechanism of intrinsic antibiotic resistance. MBio. 8:e00225–e00217.
   PubMed Web of Science ®Google Scholar
• Findlay B, Zhanel GG, Schweizer F. 2012. Neomycin-phenolic conjugates: polycationic amphiphiles with broad-spectrum antibacterial activity, low hemolytic activity and weak serum protein binding. Bioorg Med Chem Lett. 22:1499–1503.
   PubMed Web of Science ®Google Scholar
• Flemming HC, Wingender J. 2010. The biofilm matrix. Nat Rev Microbiol. 8:623–633.
   PubMed Web of Science ®Google Scholar
• Forget AL, Kowalczykowski SC. 2012. Single-molecule imaging of DNA pairing by recA reveals a 3-dimensional homology search. Nature. 482:423–427.
   PubMed Web of Science ®Google Scholar
• Gorityala BK, Guchhait G, Fernando DM, Deo S, McKenna SA, Zhanel GG, Kumar A, Schweizer F. 2016. Adjuvants based on hybrid antibiotics overcome resistance in Pseudomonas aeruginosa and enhance fluoroquinolone efficacy. Angew Chem Int Ed. 55:555–559.
   PubMed Web of Science ®Google Scholar
• Guchhait G, Altieri A, Gorityala B, Yang X, Findlay B, Zhanel GG, Mookherjee N, Schweizer F. 2015. Amphiphilic tobramycins with immunomodulatory properties. Angew Chem Int Ed. 54:6278–6282.
   PubMed Web of Science ®Google Scholar
• Haeili M, Javani A, Moradi J, Jafari Z, Feizabadi MM, Babaei E. 2017. MgrB alterations mediate colistin resistance in Klebsiella pneumoniae isolates from Iran. Front Microbiol. 8:2470.
   PubMed Web of Science ®Google Scholar
• Haynes K, Abdali N, Jhawar V, Zgurskaya H, Parks J, Green A, Baudry J, Rybenkov V, Smith J, Walker J. 2017. Identification and structure-activity relationships of novel compounds that potentiate the activities of antibiotics in Escherichia coli. J Med Chem. 60:6205–6219.
   PubMed Web of Science ®Google Scholar
• Heng J, Zhao Y, Liu M, Liu Y, Fan J, Wang X, Zhao Y, Zhang XC. 2015. Substrate-bound structure of the E. coli multidrug resistance transporter MdfA. Cell Res. 25:1060.
   PubMed Web of Science ®Google Scholar
• Hobbs JK, Miller K, O'Neill AJ, Chopra I. 2008. Consequences of daptomycin-mediated membrane damage in Staphylococcus aureus. J Antimicrob Chemother. 62:1003.
   PubMed Web of Science ®Google Scholar
• Hoffman JL. 1978. Biosynthesis of S-N6-methyladenosylhomocysteine, an inhibitor of RNA methyltransferases. J Biol Chem. 253:2905–2907.
   PubMed Web of Science ®Google Scholar
• Jammal J, Zaknoon F, Kaneti G, Goldberg K, Mor A. 2015. Sensitization of Gram-negative bacteria to rifampin and OAK combinations. Sci Rep. 5:9216.
   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. 2014. Aspergillomarasmine A overcomes metallo-β-lactamase antibiotic resistance. Nature. 510:503–506.
   PubMed Web of Science ®Google Scholar
• Klein M, Kimmelman LJ. 1947. The correlation between the inhibition of drug resistance and synergism in streptomycin and penicillin. J Bacteriol. 54:363.
   PubMed Web of Science ®Google Scholar
• Kupferschmidt K. 2016. Resistance fighters. Science. 352:758–761.
   PubMed Web of Science ®Google Scholar
• Lahiri SD, Mangani S, Jahić H, Benvenuti M, Durand-Reville TF, De Luca F, Ehmann DE, Rossolini GM, Alm RA, Docquier J-D. 2015. 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. 10:591–600.
   PubMed Web of Science ®Google Scholar
• Lamers R, Cavallari J, Burrows L. 2013. The efflux inhibitor phenylalanine-arginine beta-naphthylamide (PAβN) permeabilizes the outer membrane of Gram-negative bacteria. PloS One. 8:e60666.
   PubMed Web of Science ®Google Scholar
• Ling LL, Schneider T, Peoples AJ, Spoering AL, Engels I, Conlon BP, Mueller A, Schaberle TF, Hughes DE, Epstein S, et al. 2015. A new antibiotic kills pathogens without detectable resistance. Nature. 517:455–459.
   PubMed Web of Science ®Google Scholar
• Liu Y-Y, Wang Y, Walsh TR, Yi L-X, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, et al. 2016. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis. 16:161–168.
   PubMed Web of Science ®Google Scholar
• Liu Y, Ding S, Dietrich R, Märtlbauer E, Zhu K. 2017. A biosurfactant-inspired heptapeptide with improved specificity to kill MRSA. Angew Chem Int Ed. 56:1486–1490.
   PubMed Web of Science ®Google Scholar
• Liu Y, Li R, Xiao X, Wang Z. 2019. Molecules that inhibit bacterial resistance enzymes. Molecules. 24:43.
   Web of Science ®Google Scholar
• Livermore DM, Mushtaq S, Warner M, Woodford N. 2014. Comparative in vitro activity of sulfametrole/trimethoprim and sulfamethoxazole/trimethoprim and other agents against multiresistant Gram-negative bacteria. J Antimicrob Chemother. 69:1050–1056.
   PubMed Web of Science ®Google Scholar
• Lyu Y, Yang X, Goswami S, Gorityala B, Idowu T, Domalaon R, Zhanel G, Shan A, Schweizer F. 2017. Amphiphilic tobramycin-lysine conjugates sensitize multidrug resistant Gram-negative bacteria to rifampicin and minocycline. J Med Chem. 60:3684–3702.
   PubMed Web of Science ®Google Scholar
• Maiden M, Hunt A, Zachos M, Gibson J, Hurwitz M, Mulks M, Waters C. 2018. Triclosan is an aminoglycoside adjuvant for eradication of Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother. 62:AAC.00146–00118.
   Google Scholar
• Mansour SC, Pena OM, Hancock RE. 2014. Host defense peptides: front-line immunomodulators. Trends Immunol. 35:443–450.
   PubMed Web of Science ®Google Scholar
• Mo Y, Lorenzo M, Farghaly S, Kaur K, Housman ST. 2019. What's new in the treatment of multidrug-resistant Gram-negative infections? Diagn Microbiol Infect Dis. 93:171–181.
   PubMed Web of Science ®Google Scholar
• Moellering RC Jr, Eliopoulos GM, Allan JD. 1986. Beta-lactam/aminoglycoside combinations: interactions and their mechanisms. Am J Med. 80:30–34.
   PubMed Web of Science ®Google Scholar
• Morici P, Florio W, Rizzato C, Ghelardi E, Tavanti A, Rossolini GM, Lupetti A. 2017. Synergistic activity of synthetic N-terminal peptide of human lactoferrin in combination with various antibiotics against carbapenem-resistant Klebsiella pneumoniae strains. Eur J Clin Microbiol Infect Dis. 36:1739–1748.
   PubMed Web of Science ®Google Scholar
• Morones-Ramirez JR, Winkler JA, Spina CS, Collins JJ. 2013. Silver enhances antibiotic activity against Gram-negative bacteria. Sci Transl Med. 5:190ra181.
   Web of Science ®Google Scholar
• O'Neill J. 2016. Tackling drug-resistant infections globally: final report and recommendations. (Review on Antimicrobial Resistance, London). https://amr-review.org/sites/default/files/160518_Final%20paper_with%20cover.pdf (2019/3/30).
   Google Scholar
• Oh E, Zhang Q, Jeon B. 2014. Target optimization for peptide nucleic acid (PNA)-mediated antisense inhibition of the CmeABC multidrug efflux pump in Campylobacter jejuni. J Antimicrob Chemother. 69:375.
   PubMed Web of Science ®Google Scholar
• Pader V, Hakim S, Painter KL, Wigneshweraraj S, Clarke TB, Edwards AM. 2016. Staphylococcus aureus inactivates daptomycin by releasing membrane phospholipids. Nat Microbiol. 2:16194.
   PubMed Web of Science ®Google Scholar
• Papp-Wallace KM, Endimiani A, Taracila MA, Bonomo RA. 2011. Carbapenems: past, present, and future. Antimicrob Agents Chemother. 55:4943.
   PubMed Web of Science ®Google Scholar
• Pendleton JN, Gorman SP, Gilmore BF. 2013. Clinical relevance of the ESKAPE pathogens. Expert Rev anti Infect Ther. 11:297–308.
   PubMed Web of Science ®Google Scholar
• Ramirez MS, Tolmasky ME. 2010. Aminoglycoside modifying enzymes. Drug Resist Updat. 13:151–171.
   PubMed Web of Science ®Google Scholar
• Reading C, Cole M. 1977. Clavulanic acid: a beta-lactamase-inhibiting beta-lactam from Streptomyces clavuligerus. Antimicrob Agents Chemother. 11:852–857.
   PubMed Web of Science ®Google Scholar
• Richter MF, Drown BS, Riley AP, Garcia A, Shirai T, Svec RL, Hergenrother PJ. 2017. Predictive compound accumulation rules yield a broad-spectrum antibiotic. Nature. 545:299–304.
   PubMed Web of Science ®Google Scholar
• Robbel L, Marahiel MA. 2010. Daptomycin, a bacterial lipopeptide synthesized by a nonribosomal machinery. J Biol Chem. 285:27501–27508.
   PubMed Web of Science ®Google Scholar
• Roy R, Tiwari M, Donelli G, Tiwari V. 2018. Strategies for combating bacterial biofilms: a focus on anti-biofilm agents and their mechanisms of action. Virulence. 9:522–554.
   PubMed Web of Science ®Google Scholar
• Shakya T, Stogios P, Waglechner N, Evdokimova E, Ejim L, Blanchard J, Mcarthur A, Savchenko A, Wright G. 2011. A small molecule discrimination map of the antibiotic resistance kinome. Chem Biol. 18:1591–1601.
   PubMed Web of Science ®Google Scholar
• Shen Y, Zhou H, Xu J, Wang Y, Zhang Q, Walsh TR, Shao B, Wu C, Hu Y, Yang L, et al. 2018. Anthropogenic and environmental factors associated with high incidence of mcr-1 carriage in humans across China. Nat Microbiol. 3:1054–1062.
   PubMed Web of Science ®Google Scholar
• Sjuts H, Vargiu AV, Kwasny SM, Nguyen ST, Kim H-S, Ding X, Ornik AR, Ruggerone P, Bowlin TL, Nikaido H, et al. 2016. Molecular basis for inhibition of AcrB multidrug efflux pump by novel and powerful pyranopyridine derivatives. Proc Natl Acad Sci USA. 113:3509–3514.
   PubMed Web of Science ®Google Scholar
• Smith PA, Koehler MFT, Girgis HS, Yan D, Chen Y, Chen Y, Crawford JJ, Durk MR, Higuchi RI, Kang J, et al. 2018. Optimized arylomycins are a new class of Gram-negative antibiotics. Nature. 561:189–194.
   PubMed Web of Science ®Google Scholar
• Sohlenkamp C, Geiger O. 2016. Bacterial membrane lipids: diversity in structures and pathways. FEMS Microbiol Rev. 40:133–159.
   PubMed Web of Science ®Google Scholar
• Stoesser N, Mathers AJ, Moore CE, Day NP, Crook DW. 2016. Colistin resistance gene mcr-1 and pHNSHP45 plasmid in human isolates of Escherichia coli and Klebsiella pneumoniae. Lancet Infect Dis. 16:285–286.
   PubMed Web of Science ®Google Scholar
• Stokes JM, MacNair CR, Ilyas B, French S, Cote JP, Bouwman C, Farha MA, Sieron AO, Whitfield C, Coombes BK, Brown ED. 2017. Pentamidine sensitizes Gram-negative pathogens to antibiotics and overcomes acquired colistin resistance. Nat Microbiol. 2:17028.
   PubMed Web of Science ®Google Scholar
• Suga T, Ishii T, Iwatsuki M, Yamamoto T, Nonaka K, Masuma R, Matsui H, Hanaki H, Omura S, Shiomi K. 2012. Aranorosin circumvents arbekacin-resistance in MRSA by inhibiting the bifunctional enzyme AAC(6')/APH(2″). J Antibiot. 65:527.
   PubMed Web of Science ®Google Scholar
• Sully EK, Geller BL, Li L, Moody CM, Bailey SM, Moore AL, Wong M, Nordmann P, Daly SM, Sturge CR, Greenberg DE. 2017. Peptide-conjugated phosphorodiamidate morpholino oligomer (PPMO) restores carbapenem susceptibility to NDM-1-positive pathogens in vitro and in vivo. J Antimicrob Chemother. 72:782.
   PubMed Web of Science ®Google Scholar
• Suresh G, Das RK, Kaur BS, Rouissi T, Avalos RA, Chorfi Y, Godbout S. 2018. Alternatives to antibiotics in poultry feed: molecular perspectives. Crit Rev Microbiol. 44:318–335.
   PubMed Web of Science ®Google Scholar
• Swick MC, Morgan-Linnell SK, Carlson KM, Zechiedrich L. 2011. Expression of multidrug efflux pump genes acrAB-tolC, mdfA, and norE in Escherichia coli clinical isolates as a function of fluoroquinolone and multidrug resistance. Antimicrob Agents Chemother. 55:921–924.
   PubMed Web of Science ®Google Scholar
• Taylor PL, Rossi L, De Pascale G, Wright GD. 2012. A forward chemical screen identifies antibiotic adjuvants in Escherichia coli. ACS Chem Biol. 7:1547–1555.
   PubMed Web of Science ®Google Scholar
• Unnikrishnan A, Papaemmanuil E, Beck D, Deshpande NP, Verma A, Kumari A, Woll PS, Richards LA, Knezevic K, Chandrakanthan V, et al. 2017. Integrative genomics identifies the molecular basis of resistance to azacitidine therapy in myelodysplastic syndromes. Cell Rep. 20:572–585.
   PubMed Web of Science ®Google Scholar
• Velkov T, Dai C, Ciccotosto GD, Cappai R, Hoyer D, Li J. 2018. Polymyxins for Cns infections: pharmacology and neurotoxicity. Pharmacol Ther. 181:85–90.
   PubMed Web of Science ®Google Scholar
• Velkov T, Gallardo-Godoy A, Swarbrick J, Blaskovich M, Elliott A, Han M, Thompson P, Roberts K, Huang J, Becker B, et al. 2018. Structure, function, and biosynthetic origin of octapeptin antibiotics active against extensively drug-resistant Gram-negative bacteria. Cell Chem Biol. 25:380–391.
   PubMed Web of Science ®Google Scholar
• Walsh TR, Weeks J, Livermore DM, Toleman MA. 2011. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect Dis. 11:355–362.
   PubMed Web of Science ®Google Scholar
• Wang M, Wang P, Tu L, Zhu S, Zhang L, Li Z, Zhang Q, Yuan D, Zhang X. 2016. Multi-omics maps of cotton fibre reveal epigenetic basis for staged single-cell differentiation. Nucleic Acids Res. 44:4067–4079.
   PubMed Web of Science ®Google Scholar
• Wang X, Wang Y, Zhou Y, Li J, Yin W, Wang S, Zhang S, Shen J, Shen Z, Wang Y. 2018. Emergence of a novel mobile colistin resistance gene, mcr-8, in NDM-producing Klebsiella pneumoniae. Emerg Microbes Infect. 7:122.
   PubMed Web of Science ®Google Scholar
• Wang Y, Tian G-B, Zhang R, Shen Y, Tyrrell JM, Huang X, Zhou H, Lei L, Li H-Y, Doi Y, et al. 2017. Prevalence, risk factors, outcomes, and molecular epidemiology of mcr-1-positive Enterobacteriaceae in patients and healthy adults from China: an epidemiological and clinical study. Lancet Infect Dis. 17:390–399.
   PubMed Web of Science ®Google Scholar
• World Health Organization. 2017. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. https://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf (2019/3/30).
   Google Scholar
• Worthington RJ, Blackledge MS, Melander C. 2013. Small-molecule inhibition of bacterial two-component systems to combat antibiotic resistance and virulence. Future Med Chem. 5:1265–1284.
   PubMed Web of Science ®Google Scholar
• Wright GD. 2016. Antibiotic adjuvants: rescuing antibiotics from resistance. Trends Microbiol. 24:862–871.
   PubMed Web of Science ®Google Scholar
• Xavier BB, Lammens C, Ruhal R, Kumar-Singh S, Butaye P, Goossens H, Malhotra-Kumar S. 2016. Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Euro Surveill. 21:30280.
   Google Scholar
• Yang X, Goswami S, Gorityala BK, Domalaon R, Lyu Y, Kumar A, Zhanel GG, Schweizer FM. 2017a. A tobramycin vector enhances synergy and efficacy of efflux pump inhibitors against multidrug-resistant Gram-negative bacteria. J Med Chem. 60:3913–3932.
   PubMed Web of Science ®Google Scholar
• Yang X, Lu J, Ying M, Mu J, Li P, Liu Y. 2017b. Docking and molecular dynamics studies on triclosan derivatives binding to FabI. J Mol Model. 23:25.
   PubMed Web of Science ®Google Scholar
• Yang YQ, Li YX, Lei CW, Zhang AY, Wang HN. 2018. Novel plasmid-mediated colistin resistance gene mcr-7.1 in Klebsiella pneumoniae. J Antimicrob Chemother. 73:1791–1795.
   PubMed Web of Science ®Google Scholar
• Yenn TW, Khan MA, Syuhada NA, Ring LC, Ibrahim D, Tan WN. 2017. Stigmasterol: an adjuvant for beta lactam antibiotics against beta-lactamase positive clinical isolates. Steroids. 128:68–71.
   PubMed Web of Science ®Google Scholar
• Yin W, Li H, Shen Y, Liu Z, Wang S, Shen Z, Zhang R, Walsh TR, Shen J, Wang Y. 2017. Novel plasmid-mediated colistin resistance gene mcr-3 in Escherichia coli. MBio. 8:e00543–e00517.
   PubMed Web of Science ®Google Scholar
• Yoon E-J, Chabane YN, Goussard S, Snesrud E, Courvalin P, Dé E, Grillot-Courvalin C. 2015. Contribution of resistance-nodulation-cell division efflux systems to antibiotic resistance and biofilm formation in Acinetobacter baumannii. MBio. 6:e00309–e00315.
   PubMed Web of Science ®Google Scholar
• Zhanel GG, Lawrence CK, Adam H, Schweizer F, Zelenitsky S, Zhanel M, Lagacé-Wiens PRS, Walkty A, Denisuik A, Golden A, et al. 2018. Imipenem-Relebactam and Meropenem-Vaborbactam: Two Novel Carbapenem-β-Lactamase Inhibitor Combinations. Drugs. 78:65–98.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Liu S, Wang T, Li H, Tang S, Wang J, Wang Y, Deng X. 2018. Pterostilbene, a potential MCR-1 inhibitor that enhances the efficacy of polymyxin B. Antimicrob Agents Chemother. 62:AAC.02146–02117.
   Web of Science ®Google Scholar
• Zipperer A, Konnerth MC, Laux C, Berscheid A, Janek D, Weidenmaier C, Burian M, Schilling NA, Slavetinsky C, Marschal M, et al. 2016. Human commensals producing a novel antibiotic impair pathogen colonization. Nature. 535:511–516.
   PubMed Web of Science ®Google Scholar
• Zurawski DV, Reinhart AA, Alamneh YA, Pucci MJ, Si YZ, Abu-Taleb R, Shearer JP, Demons ST, Tyner SD, Lister T. 2017. SPR741, an antibiotic adjuvant, potentiates the in vitro and in vivo activity of rifampin against clinically relevant extensively drug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother. 61:01239–01217.
   PubMed Web of Science ®Google Scholar