Journal of Microbiology and Biotechnology

  • 제29권1호
  • /
  • Pages.1-10
  • /
  • 2019
  • /
  • 1017-7825(pISSN)
  • /
  • 1738-8872(eISSN)
한국미생물·생명공학회 (The Korean Society for Microbiology and Biotechnology)
권호 표지
DOI QR코드

DOI QR Code

Antimicrobial Agents That Inhibit the Outer Membrane Assembly Machines of Gram-Negative Bacteria

  • Choi, Umji (Department of Bioscience and Bioinformatics, Myongji University) ;
  • Lee, Chang-Ro (Department of Bioscience and Bioinformatics, Myongji University)
  • 투고 : 2018.04.02
  • 심사 : 2018.04.26
  • 발행 : 2019.01.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Gram-negative pathogens, such as Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter baumannii, pose a serious threat to public health worldwide, due to high rates of antibiotic resistance and the lack of development of novel antimicrobial agents targeting Gram-negative bacteria. The outer membrane (OM) of Gram-negative bacteria is a unique architecture that acts as a potent permeability barrier against toxic molecules, such as antibiotics. The OM is composed of phospholipids, lipopolysaccharide (LPS), outer membrane ${\beta}-barrel$ proteins (OMP), and lipoproteins. These components are synthesized in the cytoplasm or in the inner membrane, and are then selectively transported to the OM by the specific transport machines, including the Lol, BAM, and Lpt pathways. In this review, we summarize recent studies on the assembly systems of OM components and analyze studies for the development of inhibitors that target these systems. These analyses show that OM assembly machines have the potential to be a novel attractive drug target of Gram-negative bacteria.

키워드

과제정보

연구 과제 주관 기관 : Advanced Biomass R&D Center (ABC), NRF

참고문헌

  1. Patel DS, Qi Y, Im W. 2017. Modeling and simulation of bacterial outer membranes and interactions with membrane proteins. Curr. Opin. Struct. Biol. 43: 131-140. https://doi.org/10.1016/j.sbi.2017.01.003
  2. May KL, Silhavy TJ. 2017. Making a membrane on the other side of the wall. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1862: 1386-1393. https://doi.org/10.1016/j.bbalip.2016.10.004
  3. Grabowicz M. 2018. Lipoprotein transport: greasing the machines of outer membrane biogenesis: re-examining lipoprotein transport mechanisms among diverse Gram-negative bacteria while exploring new discoveries and questions. BioEssays 40: e1700187 https://doi.org/10.1002/bies.201700187
  4. Typas A, Banzhaf M, van den Berg van Saparoea B, Verheul J, Biboy J, Nichols RJ, et al. 2010. Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143: 1097-1109. https://doi.org/10.1016/j.cell.2010.11.038
  5. Paradis-Bleau C, Markovski M, Uehara T, Lupoli TJ, Walker S, Kahne DE, et al. 2010. Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143: 1110-1120. https://doi.org/10.1016/j.cell.2010.11.037
  6. Liu R, Ochman H. 2007. Stepwise formation of the bacterial flagellar system. Proc. Natl. Acad. Sci. USA 104: 7116-7121. https://doi.org/10.1073/pnas.0700266104
  7. Hospenthal MK, Costa TRD, Waksman G. 2017. A comprehensive guide to pilus biogenesis in Gram-negative bacteria. Nat. Rev. Microbiol. 15: 365-379. https://doi.org/10.1038/nrmicro.2017.40
  8. Durand E, Nguyen VS, Zoued A, Logger L, Pehau-Arnaudet G, Aschtgen MS, et al. 2015. Biogenesis and structure of a type VI secretion membrane core complex. Nature 523: 555-560. https://doi.org/10.1038/nature14667
  9. Dong C, Beis K, Nesper J, Brunkan-Lamontagne AL, Clarke BR, Whitfield C, et al. 2006. Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 444: 226-229. https://doi.org/10.1038/nature05267
  10. Zeth K, Thein M. 2010. Porins in prokaryotes and eukaryotes: common themes and variations. Biochem. J. 431: 13-22. https://doi.org/10.1042/BJ20100371
  11. Lee CR, Lee JH, Park M, Park KS, Bae IK, Kim YB et al. 2017. Biology of Acinetobacter baumannii: pathogenesis, antibiotic resistance mechanisms, and prospective treatment options. Front. Cell. Infect. Microbiol. 7: 55.
  12. O'Shea R, Moser HE. 2008. Physicochemical properties of antibacterial compounds: implications for drug discovery. J. Med. Chem. 51: 2871-2878. https://doi.org/10.1021/jm700967e
  13. Lee CR, Cho IH, Jeong BC, Lee SH. 2013. Strategies to minimize antibiotic resistance. Int. J. Environ. Res. Public Health 10: 4274-4305. https://doi.org/10.3390/ijerph10094274
  14. Lee CR, Lee JH, Park KS, Jeon JH, Kim YB, Cha CJ, et al. 2017. Antimicrobial resistance of hypervirulent Klebsiella pneumoniae: epidemiology, hypervirulence-associated determinants, and resistance mechanisms. Front. Cell. Infect. Microbiol. 7: 483. https://doi.org/10.3389/fcimb.2017.00483
  15. Konovalova A, Silhavy TJ. 2015. Outer membrane lipoprotein biogenesis: Lol is not the end. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 370: 1679.
  16. Narita SI, Tokuda H. 2017. Bacterial lipoproteins; biogenesis, sorting and quality control. Biochim. Biophys. Acta 1862: 1414-1423. https://doi.org/10.1016/j.bbalip.2016.11.009
  17. Yamaguchi K, Yu F, Inouye M. 1988. A single amino acid determinant of the membrane localization of lipoproteins in E. coli. Cell 53: 423-432. https://doi.org/10.1016/0092-8674(88)90162-6
  18. Yakushi T, Masuda K, Narita S, Matsuyama S, Tokuda H. 2000. A new ABC transporter mediating the d etachment of lipid-modified proteins from membranes. Nat. Cell. Biol. 2: 212-218. https://doi.org/10.1038/35008635
  19. Yakushi T, Yokota N, Matsuyama S, Tokuda H. 1998. LolA-dependent release of a lipid-modified protein from the inner membrane of Escherichia coli requires nucleoside triphosphate. J. Biol. Chem. 273: 32576-32581. https://doi.org/10.1074/jbc.273.49.32576
  20. Mizutani M, Mukaiyama K, Xiao J, Mori M, Satou R, Narita S, et al. 2013. Functional differentiation of structurally similar membrane subunits of the ABC transporter LolCDE complex. FEBS Lett. 587: 23-29. https://doi.org/10.1016/j.febslet.2012.11.009
  21. Okuda S, Tokuda H. 2009. Model of mouth-to-mouth transfer of bacterial lipoproteins through inner membrane LolC, periplasmic LolA, and outer membrane LolB. Proc. Natl. Acad. Sci. USA 106: 5877-5882. https://doi.org/10.1073/pnas.0900896106
  22. Takeda K, Miyatake H, Yokota N, Matsuyama S, Tokuda H, Miki K. 2003. Crystal structures of bacterial lipoprotein localization factors, LolA and LolB. EMBO J. 22: 3199-3209. https://doi.org/10.1093/emboj/cdg324
  23. Hayashi Y, Tsurumizu R, Tsukahara J, Takeda K, Narita S, Mori M, et al. 2014. Roles of the protruding loop of factor B essential for the localization of lipoproteins (LolB) in the anchoring of bacterial triacylated proteins to the outer membrane. J. Biol. Chem. 289: 10530-10539. https://doi.org/10.1074/jbc.M113.539270
  24. Walther DM, Rapaport D, Tommassen J. 2009. Biogenesis of ${\beta}$-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence. Cell. Mol. Life Sci. 66: 2789-2804. https://doi.org/10.1007/s00018-009-0029-z
  25. Noinaj N, Rollauer SE, Buchanan SK. 2015. The ${\beta}$-barrel membrane protein insertase machinery from Gram-negative bacteria. Curr. Opin. Struct. Biol. 31: 35-42. https://doi.org/10.1016/j.sbi.2015.02.012
  26. Voulhoux R, Bos MP, Geurtsen J, Mols M, Tommassen J. 2003. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299: 262-265. https://doi.org/10.1126/science.1078973
  27. Kim S , Malinver ni J C, S liz P, S ilhavy T J, H ar rison S C, Kahne D. 2007. Structure and function of an essential component of the outer membrane protein assembly machine. Science 317: 961-964. https://doi.org/10.1126/science.1143993
  28. Misra R, Stikeleather R, Gabriele R. 2015. In vivo roles of BamA, BamB and BamD in the biogenesis of BamA, a core protein of the ${\beta}$-barrel assembly machine of Escherichia coli. J. Mol. Biol. 427: 1061-1074. https://doi.org/10.1016/j.jmb.2014.04.021
  29. Hagan CL, Westwood DB, Kahne D. 2013. Bam lipoproteins assemble BamA in vitro. Biochemistry 52: 6108-6113. https://doi.org/10.1021/bi400865z
  30. Sperandeo P, Martorana AM, Polissi A. 2017. The lipopolysaccharide transport (Lpt) machinery: a nonconventional transporter for lipopolysaccharide assembly at the outer membrane of Gram-negative bacteria. J. Biol. Chem. 292: 17981-17990. https://doi.org/10.1074/jbc.R117.802512
  31. Suits MD, Sperandeo P, Deho G, Polissi A, Jia Z. 2008. Novel structure of the conserved gram-negative lipopolysaccharide transport protein A and mutagenesis analysis. J. Mol. Biol. 380: 476-488. https://doi.org/10.1016/j.jmb.2008.04.045
  32. Merten JA, Schultz KM, Klug CS. 2012. Concentration-dependent oligomerization and oligomeric arrangement of LptA. Protein Sci. 21: 211-218. https://doi.org/10.1002/pro.2004
  33. Freinkman E, Okuda S, Ruiz N, Kahne D. 2012. Regulated assembly of the transenvelope protein complex required for lipopolysaccharide export. Biochemistry 51: 4800-4806. https://doi.org/10.1021/bi300592c
  34. Okuda S, Freinkman E, Kahne D. 2012. Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 338: 1214-1217. https://doi.org/10.1126/science.1228984
  35. Tran AX, Dong C, Whitfield C. 2010. Structure and functional analysis of LptC, a conserved membrane protein involved in the lipopolysaccharide export pathway in Escherichia coli. J. Biol. Chem. 285: 33529-33539. https://doi.org/10.1074/jbc.M110.144709
  36. Laguri C, Sperandeo P, Pounot K, Ayala I, Silipo A, Bougault CM, et al. 2017. Interaction of lipopolysaccharides at intermolecular sites of the periplasmic Lpt transport assembly. Sci. Rep. 7: 9715. https://doi.org/10.1038/s41598-017-10136-0
  37. Schultz KM, Lundquist TJ, Klug CS. 2017. Lipopolysaccharide binding to the periplasmic protein LptA. Protein Sci. 26: 1517-1523. https://doi.org/10.1002/pro.3177
  38. Freinkman E, Chng SS, Kahne D. 2011. The complex that inserts lipopolysaccharide into the bacterial outer membrane forms a two-protein plug-and-barrel. Proc. Natl. Acad. Sci. USA 108: 2486-2491. https://doi.org/10.1073/pnas.1015617108
  39. Gu Y, Stansfeld PJ, Zeng Y, Dong H, Wang W, Dong C. 2015. Lipopolysaccharide is inserted into the outer membrane through an intramembrane hole, a lumen gate, and the lateral opening of LptD. Structure 23: 496-504. https://doi.org/10.1016/j.str.2015.01.001
  40. Li X, Gu Y, Dong H, Wang W, Dong C. 2015. Trapped lipopolysaccharide and LptD intermediates reveal lipopolysaccharide translocation steps across the Escherichia coli outer membrane. Sci. Rep. 5: 11883. https://doi.org/10.1038/srep11883
  41. Sperandeo P, Martorana AM, Polissi A. 2017. Lipopolysaccharide biogenesis and transport at the outer membrane of Gram-negative bacteria. Biochim. Biophys. Acta 1862: 1451-1460. https://doi.org/10.1016/j.bbalip.2016.10.006
  42. Chng SS, Xue M, Garner RA, Kadokura H, Boyd D, Beckwith J, et al. 2012. Disulfide rearrangement triggered by translocon assembly controls lipopolysaccharide export. Science 337: 1665-1668. https://doi.org/10.1126/science.1227215
  43. Chng SS, Ruiz N, Chimalakonda G, Silhavy TJ, Kahne D. 2010. Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane. Proc. Natl. Acad. Sci. USA 107: 5363-5368. https://doi.org/10.1073/pnas.0912872107
  44. Chimalakonda G, Ruiz N, Chng SS, Garner RA, Kahne D, Silhavy TJ. 2011. Lipoprotein LptE is required for the assembly of LptD by the beta-barrel assembly machine in the outer membrane of Escherichia coli. Proc. Natl. Acad. Sci. USA 108: 2492-2497. https://doi.org/10.1073/pnas.1019089108
  45. Malojcic G, Andres D, Grabowicz M, George AH, Ruiz N, Silhavy TJ, et al. 2014. LptE binds to and alters the physical state of LPS to catalyze its assembly at the cell surface. Proc. Natl. Acad. Sci. USA 111: 9467-9472. https://doi.org/10.1073/pnas.1402746111
  46. Malinverni JC, Silhavy TJ. 2009. An ABC transport system that maintains lipid a symmetry in the gram-negative outer membrane. Proc. Natl. Acad. Sci. USA 106: 8009-8014. https://doi.org/10.1073/pnas.0903229106
  47. Ekiert DC, Bhabha G, Isom GL, Greenan G, Ovchinnikov S, Henderson IR, et al. 2017. Architectures of lipid transport systems for the bacterial outer membrane. Cell 169: 273-285 e217. https://doi.org/10.1016/j.cell.2017.03.019
  48. Ruiz N, Wu T, Kahne D, Silhavy TJ. 2006. Probing the barrier function of the outer membrane with chemical conditionality. ACS Chem. Biol. 1: 385-395. https://doi.org/10.1021/cb600128v
  49. Dekker N. 2000. Outer-membrane phospholipase A: known structure, unknown biological function. Mol. Microbiol. 35: 711-717. https://doi.org/10.1046/j.1365-2958.2000.01775.x
  50. Bishop RE, Gibbons HS, Guina T, Trent MS, Miller SI, Raetz CR. 2000. Transfer of palmitate from phospholipids to lipid A in outer membranes of gram-negative bacteria. EMBO J. 19: 5071-5080. https://doi.org/10.1093/emboj/19.19.5071
  51. Chong ZS, Woo WF, Chng SS. 2015. Osmoporin OmpC forms a complex with MlaA to maintain outer membrane lipid asymmetry in Escherichia coli. Mol. Microbiol. 98: 1133-1146. https://doi.org/10.1111/mmi.13202
  52. Dalebroux ZD, Edrozo MB, Pfuetzner RA, Ressl S, Kulasekara BR, Blanc MP et al. 2015. Delivery of cardiolipins to the Salmonella outer membrane is necessary for survival within host tissues and virulence. Cell. Host Microbe 17: 441-451. https://doi.org/10.1016/j.chom.2015.03.003
  53. Ito H, Ura A, Oyamada Y, Yoshida H, Yamagishi J, Narita S et al. 2007. A new screening method to identify inhibitors of the Lol (localization of lipoproteins) system, a novel antibacterial target. Microbiol. Immunol. 51: 263-270. https://doi.org/10.1111/j.1348-0421.2007.tb03906.x
  54. Pathania R, Zlitni S, Barker C, Das R, Gerritsma DA, Lebert J, et al. 2009. Chemical genomics in Escherichia coli identifies an inhibitor of bacterial lipoprotein targeting. Nat. Chem. Biol. 5: 849-856. https://doi.org/10.1038/nchembio.221
  55. Barker CA, Allison SE, Zlitni S, Nguyen ND, Das R, Melacini G, et al. 2013. Degradation of MAC13243 and studies of the interaction of resulting thiourea compounds with the lipoprotein targeting chaperone LolA. Bioorg. Med. Chem. Lett. 23: 2426-2431. https://doi.org/10.1016/j.bmcl.2013.02.005
  56. Iwai N, Nagai K, Wachi M. 2002. Novel S-benzylisothiourea compound that induces spherical cells in Escherichia coli probably by acting on a rod-shape-determining protein(s) other than penicillin-binding protein 2. Biosci. Biotechnol. Biochem. 66: 2658-2662. https://doi.org/10.1271/bbb.66.2658
  57. McLeod SM, Fleming PR, MacCormack K, McLaughlin RE, Whiteaker JD, Narita S, et al. 2015. Small-molecule inhibitors of gram-negative lipoprotein trafficking discovered by phenotypic screening. J. Bacteriol. 197: 1075-1082. https://doi.org/10.1128/JB.02352-14
  58. Nayar AS, Dougherty TJ, Ferguson KE, Granger BA, McWilliams L, Stacey C, et al. 2015. Novel antibacterial targets and compounds revealed by a high-throughput cell wall reporter assay. J. Bacteriol. 197: 1726-1734. https://doi.org/10.1128/JB.02552-14
  59. Nickerson NN, Jao CC, Xu Y, Quinn J, Skippington E, Alexander MK, et al. 2018. A novel inhibitor of the LolCDE ABC transporter essential for lipoprotein trafficking in Gram-negative bacteria. Antimicrob. Agents Chemother. 62: 4.
  60. Sun D, Cohen S, Mani N, Murphy C, Rothstein DM. 2002. A pathway-specific cell based screening system to detect bacterial cell wall inhibitors. J. Antibiot. (Tokyo) 55: 279-287. https://doi.org/10.7164/antibiotics.55.279
  61. Tam C, Missiakas D. 2005. Changes in lipopolysaccharide structure induce the ${\sigma}^E$-dependent response of Escherichia coli. Mol. Microbiol. 55: 1403-1412. https://doi.org/10.1111/j.1365-2958.2005.04497.x
  62. Lima S, Guo MS, Chaba R, Gross CA, Sauer RT. 2013. Dual molecular signals mediate the bacterial response to outer-membrane stress. Science 340: 837-841. https://doi.org/10.1126/science.1235358
  63. Gronenberg LS, Kahne D. 2010. Development of an activity assay for discovery of inhibitors of lipopolysaccharide transport. J. Am. Chem. Soc. 132: 2518-2519. https://doi.org/10.1021/ja910361r
  64. Sherman DJ, Okuda S, Denny WA, Kahne D. 2013. Validation of inhibitors of an ABC transporter required to transport lipopolysaccharide to the cell surface in Escherichia coli. Bioorg. Med. Chem. 21: 4846-4851. https://doi.org/10.1016/j.bmc.2013.04.020
  65. Parker LL, Piwnica-Worms H. 1992. Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science 257: 1955-1957. https://doi.org/10.1126/science.1384126
  66. Kokryakov VN, Harwig SS, Panyutich EA, Shevchenko AA, Aleshina GM, Shamova OV, et al. 1993. Protegrins: leukocyte antimicrobial peptides that combine features of corticostatic defensins and tachyplesins. FEBS Lett. 327: 231-236. https://doi.org/10.1016/0014-5793(93)80175-T
  67. Steinberg DA, Hurst MA, Fujii CA, Kung AH, Ho JF, Cheng FC, et al. 1997. Protegrin-1: a broad-spectrum, rapidly microbicidal peptide with in vivo activity. Antimicrob. Agents Chemother. 41: 1738-1742. https://doi.org/10.1128/AAC.41.8.1738
  68. Srinivas N, Jetter P, Ueberbacher BJ, Werneburg M, Zerbe K, Steinmann J, et al. 2010. Peptidomimetic antibiotics target outer-membrane biogenesis in Pseudomonas aeruginosa. Science 327: 1010-1013. https://doi.org/10.1126/science.1182749
  69. Andolina G, Bencze LC, Zerbe K, Muller M, Steinmann J, Kocherla H, et al. 2018. A peptidomimetic antibiotic interacts with the periplasmic domain of LptD from Pseudomonas aeruginosa. ACS Chem. Biol. 13: 666-675. https://doi.org/10.1021/acschembio.7b00822
  70. Schmidt J, Patora-Komisarska K, Moehle K, Obrecht D, Robinson JA. 2013. Structural studies of ${\beta}$-hairpin peptidomimetic antibiotics that target LptD in Pseudomonas sp. Bioorg. Med. Chem. 21: 5806-5810. https://doi.org/10.1016/j.bmc.2013.07.013
  71. Vetterli SU, Moehle K, Robinson JA. 2016. Synthesis and antimicrobial activity against Pseudomonas aeruginosa of macrocyclic ${\beta}$-hairpin peptidomimetic antibiotics containing N-methylated amino acids. Bioorg. Med. Chem. 24: 6332-6339. https://doi.org/10.1016/j.bmc.2016.05.027
  72. Zerbe K, Moehle K, Robinson JA. 2017. Protein epitope mimetics: from new antibiotics to supramolecular synthetic vaccines. Acc. Chem. Res. 50: 1323-1331. https://doi.org/10.1021/acs.accounts.7b00129
  73. Urfer M, Bogdanovic J, Lo Monte F, Moehle K, Zerbe K, Omasits U, et al. 2016. A peptidomimetic antibiotic targets outer membrane proteins and disrupts selectively the outer membrane in Escherichia coli. J. Biol. Chem. 291: 1921-1932. https://doi.org/10.1074/jbc.M115.691725

피인용 문헌

  1. First Description of Colistin and Tigecycline-Resistant Acinetobacter baumannii Producing KPC-3 Carbapenemase in Portugal vol.7, pp.4, 2019, https://doi.org/10.3390/antibiotics7040096
  2. Distinct Roles of Outer Membrane Porins in Antibiotic Resistance and Membrane Integrity in Escherichia coli vol.10, 2019, https://doi.org/10.3389/fmicb.2019.00953
  3. Characterization of Streptomyces Isolates Associated with Estuarine Fish Chanos chanos and Profiling of Their Antibacterial Metabolites-Crude-Extract vol.2020, 2020, https://doi.org/10.1155/2020/8851947
  4. Carbon based membranes with modified properties: thermal, morphological, mechanical and antimicrobial vol.27, pp.3, 2019, https://doi.org/10.1007/s10570-019-02861-8
  5. Bimetallic gold-silver nanoparticles mediate bacterial killing by disrupting the actin cytoskeleton MreB vol.12, pp.6, 2019, https://doi.org/10.1039/c9nr10700b
  6. Periplasmic Targets for the Development of Effective Antimicrobials against Gram-Negative Bacteria vol.6, pp.9, 2020, https://doi.org/10.1021/acsinfecdis.0c00384
  7. Amphiphilic Aminoglycosides as Medicinal Agents vol.21, pp.19, 2019, https://doi.org/10.3390/ijms21197411
  8. Membrane-Targeting Triphenylphosphonium Functionalized Ciprofloxacin for Methicillin-Resistant Staphylococcus aureus (MRSA) vol.9, pp.11, 2019, https://doi.org/10.3390/antibiotics9110758
  9. Transcriptional Responses of Pseudomonas aeruginosa to Inhibition of Lipoprotein Transport by a Small Molecule Inhibitor vol.202, pp.24, 2019, https://doi.org/10.1128/jb.00452-20
  10. Outer membrane protein A (OmpA) as a potential therapeutic target for Acinetobacter baumannii infection vol.27, pp.1, 2019, https://doi.org/10.1186/s12929-020-0617-7
  11. Partial Purification and Characterization of Bacteriocin-Like Inhibitory Substances Produced by Streptomyces sp. Isolated from the Gut of Chanos chanos vol.2021, 2019, https://doi.org/10.1155/2021/7190152
  12. Improved Antibacterial Activity of Water-Soluble Nanoformulated Kaempferol and Combretastatin Polyphenolic Compounds vol.2021, 2021, https://doi.org/10.1155/2021/5682182
  13. Iron-Rich Conditions Induce OmpA and Virulence Changes of Acinetobacter baumannii vol.12, 2019, https://doi.org/10.3389/fmicb.2021.725194
  14. TAM mediates adaptation of carbapenem-resistant Klebsiella pneumoniae to antimicrobial stress during host colonization and infection vol.17, pp.2, 2021, https://doi.org/10.1371/journal.ppat.1009309
  15. Emerging peptide antibiotics with therapeutic potential vol.9, 2019, https://doi.org/10.1016/j.medidd.2020.100078
  16. The assembly of β‐barrel membrane proteins by BAM and SAM vol.115, pp.3, 2021, https://doi.org/10.1111/mmi.14666
  17. Effective Small Molecule Antibacterials from a Novel Anti-Protein Secretion Screen vol.9, pp.3, 2019, https://doi.org/10.3390/microorganisms9030592
  18. Interest of Homodialkyl Neamine Derivatives against Resistant P. aeruginosa, E. coli, and β-Lactamases-Producing Bacteria-Effect of Alkyl Chain Length on the Interaction with LPS vol.22, pp.16, 2019, https://doi.org/10.3390/ijms22168707
  19. Peptides Affecting the Outer Membrane Lipid Asymmetry System (MlaA-OmpC/F) Reduce Avian Pathogenic Escherichia coli (APEC) Colonization in Chickens vol.87, pp.17, 2021, https://doi.org/10.1128/aem.00567-21
  20. Core Oligosaccharide Portion of Lipopolysaccharide Plays Important Roles in Multiple Antibiotic Resistance in Escherichia coli vol.65, pp.10, 2019, https://doi.org/10.1128/aac.00341-21
  21. Novel Small Molecule Growth Inhibitor Affecting Bacterial Outer Membrane Reduces Extraintestinal Pathogenic Escherichia coli (ExPEC) Infection in Avian Model vol.9, pp.2, 2021, https://doi.org/10.1128/spectrum.00006-21
  22. A review of medicinal plants used in the Brazilian Cerrado for the treatment of fungal and bacterial infections vol.31, 2019, https://doi.org/10.1016/j.hermed.2021.100523