4,238
Views
14
CrossRef citations to date
0
Altmetric
Antimicrobial Agents

Novel tigecycline resistance mechanisms in Acinetobacter baumannii mediated by mutations in adeS, rpoB and rrf

ORCID Icon, , , , , , , ORCID Icon, , , , ORCID Icon & ORCID Icon show all
Pages 1404-1417 | Received 26 Apr 2021, Accepted 23 Jun 2021, Published online: 08 Jul 2021

References

  • Harding CM, Hennon SW, Feldman MF. Uncovering the mechanisms of Acinetobacter baumannii virulence. Nat Rev Microbiol. 2018 Feb;16(2):91–102.
  • Tacconelli E, Carrara E, Savoldi A, et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis. 2018 Mar;18(3):318–327.
  • Ni W, Han Y, Zhao J, et al. Tigecycline treatment experience against multidrug-resistant Acinetobacter baumannii infections: a systematic review and meta-analysis. Int J Antimicrob Agents. 2016;47(2):107–116.
  • Olson MW, Ruzin A, Feyfant E, et al. Functional, biophysical, and structural bases for antibacterial activity of tigecycline. Antimicrob Agents Chemother. 2006 Jun;50(6):2156–2166.
  • Gordon NC, Wareham DW. A review of clinical and microbiological outcomes following treatment of infections involving multidrug-resistant Acinetobacter baumannii with tigecycline. J Antimicrob Chemother. 2009 Apr;63(4):775–780.
  • He T, Wang R, Liu D, et al. Emergence of plasmid-mediated high-level tigecycline resistance genes in animals and humans. Nat Microbiol. 2019 Sep;4(9):1450–1456.
  • Gerson S, Nowak J, Zander E, et al. Diversity of mutations in regulatory genes of resistance-nodulation-cell division efflux pumps in association with tigecycline resistance in Acinetobacter baumannii. J Antimicrob Chemother. 2018 Jun 1;73(6):1501–1508.
  • Ruzin A, Keeney D, Bradford PA. AdeABC multidrug efflux pump is associated with decreased susceptibility to tigecycline in Acinetobacter calcoaceticus–Acinetobacter baumannii complex. J Antimicrob Chemother. 2007;59(5):1001–1004.
  • Sun JR, Perng CL, Chan MC, et al. A truncated AdeS kinase protein generated by ISAba1 insertion correlates with tigecycline resistance in Acinetobacter baumannii. PLoS One. 2012;7(11):e49534.
  • Yang YS, Chen HY, Hsu WJ, et al. Overexpression of AdeABC efflux pump associated with tigecycline resistance in clinical Acinetobacter nosocomialis isolates. Clin Microbiol Infect. 2019 Apr;25(4):512.e1–512.e6.
  • Chen Q, Li X, Zhou H, et al. Decreased susceptibility to tigecycline in Acinetobacter baumannii mediated by a mutation in trm encoding SAM-dependent methyltransferase. J Antimicrob Chemother. 2014 Jan;69(1):72–76.
  • Li X, Liu L, Ji J, et al. Tigecycline resistance in Acinetobacter baumannii mediated by frameshift mutation in plsC, encoding 1-acyl-sn-glycerol-3-phosphate acyltransferase. Eur J Clin Microbiol Infect Dis. 2015 Mar;34(3):625–631.
  • Wang L, Liu D, Lv Y, et al. Novel plasmid-mediated tet(X5) gene conferring resistance to tigecycline, eravacycline and omadacycline in clinical Acinetobacter baumannii. Antimicrob Agents Chemother. 2019 Dec 20;64(1):e01326–19.
  • Linkevicius M, Sandegren L, Andersson DI. Potential of tetracycline resistance proteins to evolve tigecycline resistance. Antimicrob Agents Chemother. 2016 Feb;60(2):789–796.
  • Foong WE, Wilhelm J, Tam HK, et al. Tigecycline efflux in Acinetobacter baumannii is mediated by TetA in synergy with RND-type efflux transporters. J Antimicrob Chemother. 2020 May 1;75(5):1135–1139.
  • Ma Z, Tao L, Bechthold A, et al. Overexpression of ribosome recycling factor is responsible for improvement of nucleotide antibiotic-toyocamycin in streptomyces diastatochromogenes 1628. Appl Microbiol Biotechnol. 2014 Jun;98(11):5051–5058.
  • Vivanco-Dominguez S, Bueno-Martinez J, Leon-Avila G, et al. Protein synthesis factors (RF1, RF2, RF3, RRF, and tmRNA) and peptidyl-tRNA hydrolase rescue stalled ribosomes at sense codons. J Mol Biol. 2012 Apr 13;417(5):425–439.
  • Duval M, Dar D, Carvalho F, et al. Hflxr, a homolog of a ribosome-splitting factor, mediates antibiotic resistance. Proc Natl Acad Sci U S A. 2018 Dec 26;115(52):13359–13364.
  • Hammerstrom TG, Beabout K, Clements TP, et al. Acinetobacter baumannii repeatedly evolves a hypermutator phenotype in response to tigecycline that effectively surveys evolutionary trajectories to resistance. PLoS One. 2015;10(10):e0140489.
  • Campbell EA, Korzheva N, Mustaev A, et al. Structural mechanism for rifampicin inhibition of bacterial rna polymerase. Cell. 2001 Mar 23;104(6):901–912.
  • Zaw MT, Emran NA, Lin Z. Mutations inside rifampicin-resistance determining region of rpoB gene associated with rifampicin-resistance in mycobacterium tuberculosis. J Infect Public Health. 2018 Sep–Oct;11(5):605–610.
  • Cui L, Isii T, Fukuda M, et al. An RpoB mutation confers dual heteroresistance to daptomycin and vancomycin in Staphylococcus aureus. Antimicrob Agents Chemother. 2010 Dec;54(12):5222–5233.
  • Zhou H, Zhang T, Yu D, et al. Genomic analysis of the multidrug-resistant Acinetobacter baumannii strain MDR-ZJ06 widely spread in China. Antimicrob Agents Chemother. 2011 Oct;55(10):4506–4512.
  • CLSI. Performance standards for antimicrobial susceptibility testing. 29th ed. Wayne (PA): Clinical and Laboratory Standards Institute. 2019. CLSI supplement M100. p. 1–282.
  • Deatherage DE, Barrick JE. Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol Biol. 2014;1151:165–188.
  • Amin IM, Richmond GE, Sen P, et al. A method for generating marker-less gene deletions in multidrug-resistant Acinetobacter baumannii. BMC Microbiol. 2013 Jul 13;13:158.
  • Hua X, Zhang L, Moran RA, et al. Cointegration as a mechanism for the evolution of a KPC-producing multidrug resistance plasmid in proteus mirabilis. Emerg Microbes Infect. 2020 Dec;9(1):1206–1218.
  • Tao Y, Wang Y, Huang S, et al. Metabolic-Activity-Based assessment of antimicrobial effects by D(2)O-labeled single-cell Raman microspectroscopy. Anal Chem. 2017 Apr 4;89(7):4108–4115.
  • Hua X, Liu L, Fang Y, et al. Colistin resistance in Acinetobacter baumannii MDR-ZJ06 revealed by a multiomics approach. Front Cell Infect Microbiol. 2017;7(45.
  • McClure R, Balasubramanian D, Sun Y, et al. Computational analysis of bacterial RNA-Seq data. Nucleic Acids Res. 2013;41(14):e140.
  • Robinson MD, McCarthy DJ, Smyth GK. Edger: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010 Jan 1;26(1):139–140.
  • Wickham H. Ggplot2: elegant graphics for data analysis. New York: Springer-Verlag; 2016.
  • Cao Q, Wang Y, Chen F, et al. A novel signal transduction pathway that modulates rhl quorum sensing and bacterial virulence in Pseudomonas aeruginosa. PLoS Pathog. 2014 Aug;10(8):e1004340.
  • Chang TY, Huang BJ, Sun JR, et al. Ader protein regulates adeABC expression by binding to a direct-repeat motif in the intercistronic spacer. Microbiol Res. 2016 Feb;183:60–67.
  • Xu Q, Hua X, He J, et al. The distribution of mutations and hotspots in transcription regulators of resistance-nodulation-cell division efflux pumps in tigecycline non-susceptible Acinetobacter baumannii in China. Int J Med Microbiol. 2020 Oct 24;310(8):151464.
  • Shi Y, Hua X, Xu Q, et al. Mechanism of eravacycline resistance in Acinetobacter baumannii mediated by a deletion mutation in the sensor kinase adeS, leading to elevated expression of the efflux pump AdeABC. Infect Genet Evol. 2020 Jun;80:104185.
  • Beabout K, Hammerstrom TG, Perez AM, et al. The ribosomal S10 protein is a general target for decreased tigecycline susceptibility. Antimicrob Agents Chemother. 2015 Sep;59(9):5561–5566.
  • Xu Q, Chen T, Yan B, et al. Dual role of gnaA in antibiotic resistance and virulence in Acinetobacter baumannii. Antimicrob Agents Chemother. 2019 Oct;63(10.
  • Zhou D, Tanzawa T, Lin J, et al. Structural basis for ribosome recycling by RRF and tRNA. Nat Struct Mol Biol. 2020 Jan;27(1):25–32.
  • Raj VS, Kaji H, Kaji A. Interaction of RRF and EF-G from E. coli and T. thermophilus with ribosomes from both origins–insight into the mechanism of the ribosome recycling step. RNA. 2005 Mar;11(3):275–284.
  • Ryoji M, Karpen JW, Kaji A. Further characterization of ribosome releasing factor and evidence that it prevents ribosomes from reading through a termination codon. J Biol Chem. 1981 Jun 10;256(11):5798–5801.
  • Antunes LC, Imperi F, Towner KJ, et al. Genome-assisted identification of putative iron-utilization genes in Acinetobacter baumannii and their distribution among a genotypically diverse collection of clinical isolates. Res Microbiol. 2011 Apr;162(3):279–284.
  • Penwell WF, Actis LA. Isolation and Characterization of the Acinetobactin and baumannoferrin siderophores produced by Acinetobacter baumannii. Methods Mol Biol. 2019;1946:259–270.
  • Zimbler DL, Penwell WF, Gaddy JA, et al. Iron acquisition functions expressed by the human pathogen Acinetobacter baumannii. Biometals. 2009 Feb;22(1):23–32.
  • Jenner L, Starosta AL, Terry DS, et al. Structural basis for potent inhibitory activity of the antibiotic tigecycline during protein synthesis. Proc Natl Acad Sci U S A. 2013 Mar 5;110(10):3812–3816.
  • Ishino T, Atarashi K, Uchiyama S, et al. Interaction of ribosome recycling factor and elongation factor EF-G with E. coli ribosomes studied by the surface plasmon resonance technique. Genes Cells. 2000 Dec;5(12):953–963.
  • Yoshida T, Uchiyama S, Nakano H, et al. Solution structure of the ribosome recycling factor from aquifex aeolicus. Biochemistry. 2001 Feb 27;40(8):2387–2396.
  • Tupin A, Gualtieri M, Roquet-Banères F, et al. Resistance to rifampicin: at the crossroads between ecological, genomic and medical concerns. Int J Antimicrob Agents. 2010 Jun;35(6):519–523.
  • Thapa B, Tribuddharat C, Rugdeekha S, et al. Rifampin resistance in carbapenem-resistant Acinetobacter baumannii in Siriraj hospital, Thailand. NMCJ. 2009 Dec;11(4):232–237.
  • Matsuo M, Hishinuma T, Katayama Y, et al. Mutation of RNA polymerase beta subunit (rpoB) promotes hVISA-to-VISA phenotypic conversion of strain Mu3. Antimicrob Agents Chemother. 2011 Sep;55(9):4188–4195.
  • Wang C, Fang R, Zhou B, et al. Evolution of resistance mechanisms and biological characteristics of rifampicin-resistant Staphylococcus aureus strains selected in vitro. BMC Microbiol. 2019 Sep 18;19(1):220.
  • Zhou H, Zhang L, Xu Q, et al. The mismatch repair system (mutS and mutL) in Acinetobacter baylyi ADP1. BMC Microbiol. 2020 Feb 28;20(1):40.
  • Pérez-Varela M, Corral J, Vallejo JA, et al. Mutations in the β-subunit of the RNA polymerase impair the surface-associated motility and virulence of Acinetobacter baumannii. Infect Immun. 2017 Aug;85(8):e00327–17.
  • Ramos JL, Martinez-Bueno M, Molina-Henares AJ, et al. The TetR family of transcriptional repressors. Microbiol Mol Biol Rev. 2005 Jun;69(2):326–356.
  • Trebosc V, Gartenmann S, Royet K, et al. A novel genome-editing platform for drug-resistant Acinetobacter baumannii reveals an AdeR-unrelated tigecycline resistance mechanism. Antimicrob Agents Chemother. 2016 Dec;60(12):7263–7271.
  • Richmond GE, Evans LP, Anderson MJ, et al. The Acinetobacter baumannii two-component system AdeRS regulates genes required for multidrug efflux, biofilm formation, and virulence in a strain-specific manner. mBio. 2016 Apr 19;7(2):e00430–16.
  • Geisinger E, Mortman NJ, Vargas-Cuebas G, et al. A global regulatory system links virulence and antibiotic resistance to envelope homeostasis in Acinetobacter baumannii. PLoS Pathog. 2018 May;14(5):e1007030.
  • Leblanc SK, Oates CW, Raivio TL. Characterization of the induction and cellular role of the BaeSR two-component envelope stress response of Escherichia coli. J Bacteriol. 2011 Jul;193(13):3367–3375.
  • Sun F, Li C, Jeong D, et al. In the Staphylococcus aureus two-component system sae, the response regulator SaeR binds to a direct repeat sequence and DNA binding requires phosphorylation by the sensor kinase SaeS. J Bacteriol. 2010 Apr;192(8):2111–2127.
  • Muller C, Plésiat P, Jeannot K. A two-component regulatory system interconnects resistance to polymyxins, aminoglycosides, fluoroquinolones, and β-lactams inPseudomonas aeruginosa. Antimicrob Agents Chemother. 2011 Mar;55(3):1211–1221.