Synergistic potential of Leu
Cefepime
/ pharmacology
Anti-Bacterial Agents
/ pharmacology
Microbial Sensitivity Tests
Cephalosporins
/ pharmacology
Methicillin-Resistant Staphylococcus aureus
/ drug effects
Drug Synergism
Biofilms
/ drug effects
Depsipeptides
/ pharmacology
Drug Resistance, Multiple, Bacterial
/ drug effects
Staphylococcal Infections
/ microbiology
Humans
Biofilm inhibition
Cefepime
Leu10-teixobactin
Methicillin-resistant Staphylococcus aureus (MRSA)
Synergistic activity
β-lactam potentiation
Journal
BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981
Informations de publication
Date de publication:
29 Oct 2024
29 Oct 2024
Historique:
received:
11
07
2024
accepted:
09
10
2024
medline:
30
10
2024
pubmed:
30
10
2024
entrez:
30
10
2024
Statut:
epublish
Résumé
Staphylococcus aureus (S. aureus) is a significant Gram-positive opportunistic pathogen behind many debilitating infections. β-lactam antibiotics are conventionally prescribed for treating S. aureus infections. However, the adaptability of S. aureus in evolving resistance to multiple β-lactams contributed to the persistence and spread of infections, exemplified in the emergence of methicillin-resistant S. aureus (MRSA). In the present study, we investigated the efficacies of the synthetic teixobactin analogue, Leu
Identifiants
pubmed: 39472779
doi: 10.1186/s12866-024-03577-x
pii: 10.1186/s12866-024-03577-x
doi:
Substances chimiques
Cefepime
807PW4VQE3
Anti-Bacterial Agents
0
Cephalosporins
0
Depsipeptides
0
teixobactin
LC730GUE72
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
442Subventions
Organisme : National Institute of Allergy and Infectious Diseases
ID : R01AI146241
Organisme : National Institute of Allergy and Infectious Diseases
ID : R01AI146241
Informations de copyright
© 2024. The Author(s).
Références
Craft KM, Nguyen JM, Berg LJ, Townsend SD. Methicillin-resistant Staphylococcus aureus (MRSA): antibiotic-resistance and the biofilm phenotype. MedChemComm. 2019;10(8).
Lee AS, de Lencastre H, Garau J, Kluytmans J, Malhotra-Kumar S, Peschel A et al. Methicillin-resistant Staphylococcus aureus. Nat Reviews Disease Primers. 2018;4(1).
Foster TJ. Antibiotic resistance in Staphylococcus aureus. Current status and future prospects. FEMS Microbiol Rev. 2017;41(3):430–49.
doi: 10.1093/femsre/fux007
pubmed: 28419231
Donlan RM, Biofilms. Microbial Life on surfaces. Emerg Infect Dis. 2002;8(9):881–90.
doi: 10.3201/eid0809.020063
pubmed: 12194761
pmcid: 2732559
Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents. 2010;35(4):322–32.
doi: 10.1016/j.ijantimicag.2009.12.011
pubmed: 20149602
Verderosa AD, Totsika M, Fairfull-Smith KE. Bacterial Biofilm Eradication agents: a current review. Front Chem. 2019;7.
Shalaby MAW, Dokla EME, Serya RAT, Abouzid KAM. Penicillin binding protein 2a: An overview and a medicinal chemistry perspective. European Journal of Medicinal Chemistry: Elsevier Masson SAS; 2020.
Hanaki H, Kuwahara-Arai K, Boyle-Vavra S, Daum RS, Labischinski H, Hiramatsu K. Activated cell-wall synthesis is associated with Vancomycin resistance in methicillin-resistant Staphylococcus aureus clinical strains Mu3 and Mu50. J Antimicrob Chemother. 1998;42(2):199–209.
doi: 10.1093/jac/42.2.199
pubmed: 9738837
De Rosa M, Verdino A, Soriente A, Marabotti A. The Odd couple(s): an overview of Beta-lactam antibiotics bearing more Than one Pharmacophoric Group. Int J Mol Sci. 2021;22(2):617.
doi: 10.3390/ijms22020617
pubmed: 33435500
pmcid: 7826672
Liu Y, Breukink E. The membrane steps of bacterial cell wall synthesis as antibiotic targets. Antibiotics: MDPI AG; 2016.
doi: 10.3390/antibiotics5030028
Nikolaidis I, Favini-Stabile S, Dessen A. Resistance to antibiotics targeted to the bacterial cell wall. Protein Sci. 2014;23(3).
Jubeh B, Breijyeh Z, Karaman R. Resistance of gram-positive bacteria to current antibacterial agents and overcoming approaches. Molecules: MDPI AG; 2020.
doi: 10.3390/molecules25122888
Bush K, Bradford PA. β-Lactams and β-Lactamase inhibitors: an overview. Cold Spring Harbor Perspect Med. 2016;6(8).
WHO bacterial priority pathogens list. 2024: Bacterial pathogens of public health importance to guide research, development and strategies to prevent and control antimicrobial resistance 2024 [ https://www.who.int/publications/i/item/9789240093461#:~:text=Notable%20among%20these%20are%20Gram,Pseudomonas%20aeruginosa%2C%20and%20Staphylococcus%20aureus
McCormick MH, McGuire JM, Pittenger GE, Pittenger RC, Stark WM. Vancomycin, a new antibiotic. I. Chemical and biologic properties. Antibiot Annual. 1955;3:606–11.
Karas JA, Chen F, Schneider-Futschik EK, Kang Z, Hussein M, Swarbrick J, et al. Synthesis and structure – activity relationships of teixobactin. Ann N Y Acad Sci. 2020;1459(1):86–105.
doi: 10.1111/nyas.14282
pubmed: 31792983
Ling LL, Schneider T, Peoples AJ, Spoering AL, Engels I, Conlon BP, et al. A new antibiotic kills pathogens without detectable resistance. Nature. 2015;517(7535):455–9.
doi: 10.1038/nature14098
pubmed: 25561178
pmcid: 7414797
Wen P-C, Vanegas JM, Rempe SB, Tajkhorshid E. Probing key elements of teixobactin–lipid II interactions in membranes. Chem Sci. 2018;9(34).
Velkov T, Swarbrick JD, Hussein MH, Schneider-Futschik EK, Hoyer D, Li J et al. The impact of backbone N-methylation on the structure-activity relationship of Leu10-teixobactin. J Pept Sci. 2019;25(9).
Hussein M, Karas JA, Schneider-Futschik EK, Chen F, Swarbrick J, Paulin OKA et al. The killing mechanism of Teixobactin against Methicillin-Resistant Staphylococcus aureus: an untargeted Metabolomics Study. mSystems. 2020;5(3).
Dien Bard J, Hindler JA, Gold HS, Limbago B. Rationale for eliminating Staphylococcus breakpoints for β-Lactam agents other than penicillin, Oxacillin or Cefoxitin, and Ceftaroline. Clin Infect Dis. 2014;58(9):1287–96.
doi: 10.1093/cid/ciu043
pubmed: 24457339
EUCAST. Clinical breakpoints - breakpoints and guidance.
Tyers M, Wright GD. Drug combinations: a strategy to extend the life of antibiotics in the 21st century. Nature Reviews Microbiology: Nature Publishing Group; 2019. pp. 141–55.
Lagatolla C, Mehat JW, La Ragione RM, Luzzati R, Di Bella S. Vitro and in vivo studies of Oritavancin and Fosfomycin synergism against Vancomycin-resistant Enterococcus faecium. Antibiotics. 2022;11(10):1334.
doi: 10.3390/antibiotics11101334
pubmed: 36289992
pmcid: 9598191
McGuinness WA, Malachowa N, Deleo FR. Vancomycin Resistance in Staphylococcus aureus. 2017.
Sanyal D, Greenwood D. An electronmicroscope study of glycopeptide antibiotic-resistant strains of Staphylococcus epidermidis. J Med Microbiol. 1993;39(3):204–10.
doi: 10.1099/00222615-39-3-204
pubmed: 8366519
Aslam J, Ali HM, Hussain S, Ahmad MZ, Siddique AB, Shahid M et al. Effectiveness of cephalosporins in hydrolysis and inhibition of Staphylococcus aureus and Escherichia coli biofilms. J Vet Sci. 2024;25(3).
Zervosen A, Sauvage E, Frère JM, Charlier P, Luxen A. Development of new drugs for an old target - the penicillin binding proteins. Molecules2012. pp. 12478–505.
Worthington RJ, Melander C. Overcoming resistance to β-Lactam antibiotics. J Org Chem. 2013;78(9):4207–13.
doi: 10.1021/jo400236f
pubmed: 23530949
pmcid: 3644377
Homma T, Nuxoll A, Gandt AB, Ebner P, Engels I, Schneider T, et al. Dual targeting of cell wall precursors by teixobactin leads to cell lysis. Antimicrob Agents Chemother. 2016;60(11):6510–7.
doi: 10.1128/AAC.01050-16
pubmed: 27550357
pmcid: 5075054
Farha MA, Leung A, Sewell EW, D’Elia MA, Allison SE, Ejim L, et al. Inhibition of WTA Synthesis Blocks the Cooperative Action of PBPs and sensitizes MRSA to β-Lactams. ACS Chem Biol. 2013;8(1):226–33.
doi: 10.1021/cb300413m
pubmed: 23062620
Foxley MA, Friedline AW, Jensen JM, Nimmo SL, Scull EM, King JB, et al. Efficacy of ampicillin against methicillin-resistant Staphylococcus aureus restored through synergy with branched poly(ethylenimine). J Antibiot. 2016;69(12):871–8.
doi: 10.1038/ja.2016.44
Campbell J, Singh AK, Santa Maria JP, Kim Y, Brown S, Swoboda JG, et al. Synthetic lethal compound combinations reveal a fundamental connection between wall teichoic acid and peptidoglycan biosyntheses in staphylococcus aureus. ACS Chem Biol. 2011;6(1):106–16.
doi: 10.1021/cb100269f
pubmed: 20961110
Brown S, Xia G, Luhachack LG, Campbell J, Meredith TC, Chen C, et al. Methicillin resistance in Staphylococcus aureus requires glycosylated wall teichoic acids. Proc Natl Acad Sci USA. 2012;109(46):18909–14.
doi: 10.1073/pnas.1209126109
pubmed: 23027967
pmcid: 3503181
Parmar A, Lakshminarayanan R, Iyer A, Goh ETL, To TY, Yam JKH, et al. Development of teixobactin analogues containing hydrophobic, non-proteogenic amino acids that are highly potent against multidrug-resistant bacteria and biofilms. Eur J Med Chem. 2023;261:115853.
doi: 10.1016/j.ejmech.2023.115853
pubmed: 37857144
Mann PA, Müller A, Wolff KA, Fischmann T, Wang H, Reed P, et al. Chemical Genetic Analysis and functional characterization of Staphylococcal Wall Teichoic Acid 2-Epimerases reveals unconventional antibiotic drug targets. PLoS Pathog. 2016;12(5):e1005585–e.
doi: 10.1371/journal.ppat.1005585
pubmed: 27144276
pmcid: 4856313
Naclerio GA, Onyedibe KI, Sintim HO. Lipoteichoic acid biosynthesis inhibitors as potent inhibitors of S. Aureus and E. faecalis growth and biofilm formation. Molecules. 2020;25(10):2277.
doi: 10.3390/molecules25102277
pubmed: 32408616
pmcid: 7287929
Ultee E, van der Aart LT, Zhang L, van Dissel D, Diebolder CA, van Wezel GP, et al. Teichoic acids anchor distinct cell wall lamellae in an apically growing bacterium. Commun Biology. 2020;3(1):314.
doi: 10.1038/s42003-020-1038-6
Li L, Cheung A, Bayer AS, Chen L, Abdelhady W, Kreiswirth BN, et al. The global Regulon sarA regulates β-Lactam Antibiotic Resistance in Methicillin-Resistant Staphylococcus aureus in Vitro and in endovascular infections. J Infect Dis. 2016;214(9):1421–9.
doi: 10.1093/infdis/jiw386
pubmed: 27543672
pmcid: 5079373
Peng Q, Tang X, Dong W, Sun N, Yuan W. A review of Biofilm formation of Staphylococcus aureus and its regulation mechanism. Antibiotics. 2022;12(1):12.
doi: 10.3390/antibiotics12010012
pubmed: 36671212
pmcid: 9854888
Zhu X, Liu D, Singh AK, Drolia R, Bai X, Tenguria S et al. Tunicamycin mediated inhibition of Wall Teichoic Acid affects Staphylococcus aureus and Listeria monocytogenes cell morphology, Biofilm formation and virulence. Front Microbiol. 2018;9.
Gross M, Cramton SE, Götz F, Peschel A. Key role of Teichoic Acid Net Charge in Staphylococcus aureus colonization of Artificial surfaces. Infect Immun. 2001;69(5):3423–6.
doi: 10.1128/IAI.69.5.3423-3426.2001
pubmed: 11292767
pmcid: 98303
Swoboda JG, Campbell J, Meredith TC, Walker S. Wall teichoic acid function, biosynthesis, and inhibition. ChemBioChem2010. pp. 35–45.
Darnell RL, Knottenbelt MK, Todd Rose FO, Monk IR, Stinear TP, Cook GM et al. Genomewide profiling of the Enterococcus faecalis transcriptional response to Teixobactin reveals CroRS as an essential Regulator of Antimicrobial Tolerance. mSphere. 2019;4(3).
Ferrer-González E, Kaul M, Parhi AK, LaVoie EJ, Pilch DS. β-Lactam antibiotics with a High Affinity for PBP2 Act synergistically with the FtsZ-Targeting Agent TXA707 against Methicillin-Resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2017;61(9).
Jordan S, Hutchings MI, Mascher T. Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol Rev. 2008;32(1):107–46.
doi: 10.1111/j.1574-6976.2007.00091.x
pubmed: 18173394
Utaida S, Dunman PM, Macapagal D, Murphy E, Projan SJ, Singh VK, et al. Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology. 2003;149(10):2719–32.
doi: 10.1099/mic.0.26426-0
pubmed: 14523105
Mitchell SJ, Verma D, Griswold KE, Bailey-Kellogg C. Building blocks and blueprints for bacterial autolysins. PLoS Comput Biol. 2021;17(4).
Kluj RM, Ebner P, Adamek M, Ziemert N, Mayer C, Borisova M. Recovery of the peptidoglycan turnover product released by the Autolysin atl in Staphylococcus aureus involves the Phosphotransferase System Transporter MurP and the Novel 6-phospho-N-acetylmuramidase MupG. Front Microbiol. 2018;9.
Weinstein MP, Patel JB, Burnhman C-A, Zimmer BL. Clinical and Laboratory Standards Institute Methods for Dilution Antimicrobial susceptibility tests for Bacteria that grow aerobically standard, approval CDM-A. M07 methods for. dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; 2018.
Clinical L, Standards I. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. 30th ed2020.
Howden BP, McEvoy CRE, Allen DL, Chua K, Gao W, Harrison PF et al. Evolution of multidrug resistance during staphylococcus aureus infection involves mutation of the essential two component regulator WalKR. PLoS Pathog. 2011;7(11).
Chua KYL, Seemann T, Harrison PF, Monagle S, Korman TM, Johnson PDR et al. The dominant Australian community-acquired methicillin-resistant Staphylococcus aureus clone ST93-IV [2B] is highly virulent and genetically distinct. PLoS ONE. 2011;6(10).
Doern CD. When does 2 plus 2 equal 5? A review of antimicrobial synergy testing. J Clin Microbiol. 2014;52(12):4124–8.
doi: 10.1128/JCM.01121-14
pubmed: 24920779
pmcid: 4313275
Kowalska-Krochmal B, Dudek-Wicher R. The minimum inhibitory concentration of antibiotics: methods, interpretation, clinical relevance. Pathogens. 2021;10(2):1–21.
doi: 10.3390/pathogens10020165
Motyl M, Dorso K, Barrett J, Giacobbe R. Basic microbiological techniques used in Antibacterial Drug Discovery. Curr Protocols Pharmacol. 2005;31(1).
Hussein M, Hu X, Paulin OKA, Crawford S, Tony Zhou Q, Baker M, et al. Polymyxin B combinations with FDA-approved non-antibiotic phenothiazine drugs targeting multi-drug resistance of Gram-negative pathogens. Comput Struct Biotechnol J. 2020;18:2247–58.
doi: 10.1016/j.csbj.2020.08.008
pubmed: 32952938
pmcid: 7481501
Siqueira VLD, Cardoso RF, Caleffi-Ferracioli KR, de Lima Scodro RB, Fernandez MA, Fiorini A, et al. Structural changes and differentially expressed genes in Pseudomonas aeruginosa exposed to Meropenem-Ciprofloxacin Combination. Antimicrob Agents Chemother. 2014;58(7):3957–67.
doi: 10.1128/AAC.02584-13
pubmed: 24798291
pmcid: 4068605
Jonckheere S, De Neve N, Verbeke J, De Decker K, Brandt I, Boel A et al. Target-controlled infusion of Cefepime in critically ill patients. Antimicrob Agents Chemother. 2019;64(1).
Van der Auwera P, Santella PJ. Pharmacokinetics of cefepime: a review. J Antimicrob Chemother. 1993;32(suppl B):103–15.
doi: 10.1093/jac/32.suppl_B.103
pubmed: 8150753
Alshareef F, Review B. Protocol to Evaluate Antibacterial Activity MIC, FIC and Time Kill Method. 2021.
Petersen PJ, Jones CH, Bradford PA. In vitro antibacterial activities of tigecycline and comparative agents by time-kill kinetic studies in fresh Mueller-Hinton broth. Diagn Microbiol Infect Dis. 2007;59(3):347–9.
doi: 10.1016/j.diagmicrobio.2007.05.013
pubmed: 17662552
Belley A, Neesham-Grenon E, Arhin FF, McKay GA, Parr TR, Moeck G. Assessment by Time-kill methodology of the synergistic effects of Oritavancin in Combination with other Antimicrobial agents against Staphylococcus aureus. Antimicrob Agents Chemother. 2008;52(10).
Yadav R, Bulitta JB, Schneider EK, Shin BS, Velkov T, Nation RL et al. Aminoglycoside concentrations required for synergy with carbapenems against Pseudomonas aeruginosa determined via mechanistic studies and modeling. Antimicrob Agents Chemother. 2017;61(12).
Kang YR, Chung DR, Ko J-H, Huh K, Cho SY, Kang C-I, et al. Comparing the synergistic and Antagonistic Interactions of Ciprofloxacin and levofloxacin combined with rifampin against drug-resistant Staphylococcus aureus: a time–kill assay. Antibiotics. 2023;12(4):711.
doi: 10.3390/antibiotics12040711
pubmed: 37107077
pmcid: 10135007
Montero MM, Domene Ochoa S, López-Causapé C, Luque S, Sorlí L, Campillo N et al. Time-kill evaluation of antibiotic combinations containing ceftazidime-avibactam against extensively drug-resistant Pseudomonas aeruginosa and their potential role against Ceftazidime-Avibactam-Resistant isolates. Microbiol Spectr. 2021;9(1).
Olivier FAB, Hilsenstein V, Weerasinghe H, Weir A, Hughes S, Crawford S et al. The escape of Candida albicans from macrophages is enabled by the fungal toxin candidalysin and two host cell death pathways. Cell Rep. 2022;40(12).
Mohamed AMT, Chan H, Luhur J, Bauda E, Gallet B, Morlot C, et al. Chromosome segregation and Peptidoglycan Remodeling are coordinated at a highly stabilized septal pore to maintain bacterial Spore Development. Dev Cell. 2021;56(1):36–e515.
doi: 10.1016/j.devcel.2020.12.006
pubmed: 33383000
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402–8.
doi: 10.1006/meth.2001.1262
pubmed: 11846609