Alterations in AdeS and AdeR regulatory proteins in 1-(1-naphthylmethyl)-piperazine responsive colistin resistance of Acinetobacter baumannii

References

• Sievert DM, Ricks P, Edwards JR, Schneider A, Patel J, Srinivasan A, Kallen A, Limbago B, Fridkin S. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009-2010. Infect Control Hosp Epidemiol. 2013;34(1):1–14.
   PubMed Web of Science ®Google Scholar
• Necati Hakyemez I, Kucukbayrak A, Tas T, Burcu Yikilgan A, Akkaya A, Yasayacak A, et al. Nosocomial Acinetobacter baumannii infections and changing antibiotic resistance. Pak J Med Sci. 2013;29(5):1245–1248.
   PubMed Web of Science ®Google Scholar
• Cai Y, Chai D, Wang R, Liang B, Bai N. Colistin resistance of Acinetobacter baumannii: clinical reports, mechanisms and antimicrobial strategies. J Antimicrob Chemother. 2012;67(7):1607–1615.
   PubMed Web of Science ®Google Scholar
• Izadpanah M, Khalili H. Antibiotic regimens for treatment of infections due to multidrug-resistant Gram-negative pathogens: an evidence-based literature review. J Res Pharm Pract. 2015;4(3):105–114.
   PubMed Web of Science ®Google Scholar
• Biswas S, Brunel J-M, Dubus J-C, Reynaud-Gaubert M, Rolain J-M. Colistin: an update on the antibiotic of the 21st century. Expert Rev Anti Infect Ther. 2012;10(8):917–934.
   PubMed Web of Science ®Google Scholar
• Koike M, Iida K, Matsuo T. Electron microscopic studies on mode of action of polymyxin. J Bacteriol. 1969;97(1):448–452.
   PubMed Web of Science ®Google Scholar
• Gales AC, Jones RN, Sader HS. Global assessment of the antimicrobial activity of polymyxin B against 54 731 clinical isolates of Gram-negative bacilli: report from the SENTRY antimicrobial surveillance programme (2001-2004). Clin Microbiol Infect. 2006;12(4):315–321.
   PubMed Web of Science ®Google Scholar
• Rodriguez CH, Hernan RC, Bombicino K, Karina B, Granados G, Gabriela G, Nastro M, Marcela N, Vay C, Carlos V, et al. Selection of colistin-resistant Acinetobacter baumannii isolates in postneurosurgical meningitis in an intensive care unit with high presence of heteroresistance to colistin. Diagn Microbiol Infect Dis. 2009;65(2):188–191.
   PubMed Web of Science ®Google Scholar
• Iacono M, Villa L, Fortini D, Bordoni R, Imperi F, Bonnal RJP, Sicheritz-Ponten T, De Bellis G, Visca P, Cassone A, et al. Whole-genome pyrosequencing of an epidemic multidrug-resistant Acinetobacter baumannii strain belonging to the European clone II group. Antimicrob Agents Chemother. 2008;52(7):2616–2625.
   PubMed Web of Science ®Google Scholar
• Olaitan AO, Morand S, Rolain JM. Mechanisms of polymyxin resistance: acquired and intrinsic resistance in bacteria. Front Microbiol. 2014;5:643
   PubMed Web of Science ®Google Scholar
• Poirel L, Jayol A, Nordmann P. Polymyxins: antibacterial activity, susceptibility testing, and resistance mechanisms encoded by plasmids or chromosomes. Clin Microbiol Rev. 2017;30(2):557–596.
   PubMed Web of Science ®Google Scholar
• Moffatt JH, Harper M, Harrison P, Hale JDF, Vinogradov E, Seemann T, Henry R, Crane B, St. Michael F, Cox AD, et al. Colistin resistance in Acinetobacter baumannii is mediated by complete loss of lipopolysaccharide production. Antimicrob Agents Chemother. 2010;54(12):4971–4977.
   PubMed Web of Science ®Google Scholar
• Hameed F, Khan MA, Muhammad H, Sarwar T, Bilal H, Rehman TU. Plasmid-mediated mcr-1 gene in Acinetobacter baumannii and Pseudomonas aeruginosa: first report from Pakistan. Rev Soc Bras Med Trop. 2019;52:e20190237
   PubMed Web of Science ®Google Scholar
• Fernando DM, Kumar A. Resistance-Nodulation-Division Multidrug Efflux Pumps in Gram-Negative Bacteria: Role in Virulence. Antibiotics (Basel). 2013;2(1):163–181.
   PubMedGoogle Scholar
• Delmar JA, Su C-C, Yu EW. Bacterial multidrug efflux transporters. Annu Rev Biophys. 2014;43(1):93–117.
   PubMedGoogle Scholar
• Magnet S, Courvalin P, Lambert T. Resistance-nodulation-cell division-type efflux pump involved in aminoglycoside resistance in Acinetobacter baumannii strain BM4454. Antimicrob Agents Chemother. 2001;45(12):3375–3380.
   PubMed Web of Science ®Google Scholar
• Marchand I, Damier-Piolle L, Courvalin P, Lambert T. Expression of the RND-type efflux pump AdeABC in Acinetobacter baumannii is regulated by the AdeRS two-component system. Antimicrob Agents Chemother. 2004;48(9):3298–3304.
   PubMed Web of Science ®Google Scholar
• Coyne S, Courvalin P, Périchon B. Efflux-mediated antibiotic resistance in Acinetobacter spp. Antimicrob Agents Chemother. 2011;55(3):947–953.
   PubMed Web of Science ®Google Scholar
• Dijkshoorn L, Nemec A, Seifert H. An increasing threat in hospitals: multidrug-resistant Acinetobacter baumannii. Nat Rev Microbiol. 2007;5(12):939–951.
   PubMed Web of Science ®Google Scholar
• Chang T-Y, Huang B-J, Sun J-R, Perng C-L, Chan M-C, Yu C-P, Chiueh T-S. AdeR protein regulates adeABC expression by binding to a direct-repeat motif in the intercistronic spacer. Microbiol. Res. 2016;183:60–67.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Lari AR, Ardebili A, Hashemi A. AdeR-AdeS mutations & overexpression of the AdeABC efflux system in ciprofloxacin-resistant Acinetobacter baumannii clinical isolates. Indian J Med Res. 2018;147(4):413–421.
   PubMedGoogle Scholar
• Montana S, Vilacoba E, Traglia GM, Almuzara M, Pennini M, Fernandez A, et al. Genetic Variability of AdeRS Two-Component System Associated with Tigecycline Resistance in XDR-Acinetobacter baumannii Isolates. Curr Microbiol. 2015;71(1):76–82.
   PubMed Web of Science ®Google Scholar
• Yoon EJ, Courvalin P, Grillot-Courvalin C. RND-type efflux pumps in multidrug-resistant clinical isolates of Acinetobacter baumannii: major role for AdeABC overexpression and AdeRS mutations. Antimicrob Agents Chemother. 2013;57(7):2989–2995.
   PubMed Web of Science ®Google Scholar
• Hornsey M, Ellington MJ, Doumith M, Thomas CP, Gordon NC, Wareham DW, Quinn J, Lolans K, Livermore DM, Woodford N, et al. AdeABC-mediated efflux and tigecycline MICs for epidemic clones of Acinetobacter baumannii. J Antimicrob Chemother. 2010;65(8):1589–1593.
   PubMed Web of Science ®Google Scholar
• Sun J-R, Perng C-L, Chan M-C, Morita Y, Lin J-C, Su C-M, Wang W-Y, Chang T-Y, Chiueh T-S. A truncated AdeS kinase protein generated by ISAba1 insertion correlates with tigecycline resistance in Acinetobacter baumannii. PloS One. 2012;7(11):e49534.
   PubMed Web of Science ®Google Scholar
• Damier-Piolle L, Magnet S, Brémont S, Lambert T, Courvalin P. AdeIJK, a resistance-nodulation-cell division pump effluxing multiple antibiotics in Acinetobacter baumannii. Antimicrob Agents Chemother. 2008;52(2):557–562.
   PubMed Web of Science ®Google Scholar
• Coyne S, Guigon G, Courvalin P, Périchon B. Screening and quantification of the expression of antibiotic resistance genes in Acinetobacter baumannii with a microarray. Antimicrob Agents Chemother. 2010;54(1):333–340.
   PubMed Web of Science ®Google Scholar
• Rosenfeld N, Bouchier C, Courvalin P, Périchon B. Expression of the resistance-nodulation-cell division pump AdeIJK in Acinetobacter baumannii is regulated by AdeN, a TetR-type regulator. Antimicrob Agents Chemother. 2012;56(5):2504–2510.
   PubMed Web of Science ®Google Scholar
• Coyne S, Rosenfeld N, Lambert T, Courvalin P, Perichon B. Overexpression of resistance-nodulation-cell division pump AdeFGH confers multidrug resistance in Acinetobacter baumannii. Antimicrob Agents Chemother. 2010;54(10):4389–4393.
   PubMed Web of Science ®Google Scholar
• Lomovskaya O, Warren MS, Lee A, Galazzo J, Fronko R, Lee M, Blais J, Cho D, Chamberland S, Renau T, et al. Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: novel agents for combination therapy. Antimicrob Agents Chemother. 2001;45(1):105–116.
   PubMed Web of Science ®Google Scholar
• Pannek S, Higgins PG, Steinke P, Jonas D, Akova M, Bohnert JA, Seifert H, Kern WV. Multidrug efflux inhibition in Acinetobacter baumannii: comparison between 1-(1-naphthylmethyl)-piperazine and phenyl-arginine-beta-naphthylamide. J Antimicrob Chemother. 2006;57(5):970–974.
   PubMed Web of Science ®Google Scholar
• Anes J, Sivasankaran SK, Muthappa DM, Fanning S, Srikumar S. Exposure to Sub-inhibitory Concentrations of the Chemosensitizer 1-(1-Naphthylmethyl)-Piperazine Creates Membrane Destabilization in Multi-Drug Resistant Klebsiella pneumoniae. Front Microbiol. 2019;10:92.
   PubMed Web of Science ®Google Scholar
• Vargiu AV, Nikaido H. Multidrug binding properties of the AcrB efflux pump characterized by molecular dynamics simulations. Proc Natl Acad Sci USA. 2012;109(50):20637–20642.
   PubMed Web of Science ®Google Scholar
• Nikaido H. Structure and mechanism of RND-type multidrug efflux pumps. Adv Enzymol Relat Areas Mol Biol. 2011;77:1–60.
   PubMedGoogle Scholar
• Ardehali SH, Azimi T, Fallah F, Owrang M, Aghamohammadi N, Azimi L. Role of efflux pumps in reduced susceptibility to tigecycline in Acinetobacter baumannii. New Microbes New Infect. 2019;30:100547.
   PubMedGoogle Scholar
• Baron SA, Rolain JM. Efflux pump inhibitor CCCP to rescue colistin susceptibility in mcr-1 plasmid-mediated colistin-resistant strains and Gram-negative bacteria. J Antimicrob Chemother. 2018;73(7):1862–1871.
   PubMed Web of Science ®Google Scholar
• Ni W, Li Y, Guan J, Zhao J, Cui J, Wang R, Liu Y. Effects of Efflux Pump Inhibitors on Colistin Resistance in Multidrug-Resistant Gram-Negative Bacteria. Antimicrob Agents Chemother. 2016;60(5):3215–3218.
   PubMed Web of Science ®Google Scholar
• Xing L, Barnie P, Su Z, Xu H. Development of Efflux Pumps and Inhibitors (EPIs) in A. baumanii. Clin. Microbiol. 2014;3:1.
   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. 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. 2016;16(2):161–168.
   PubMed Web of Science ®Google Scholar
• Carretto E, Brovarone F, Russello G, Nardini P, El-Bouseary MM, Aboklaish AF, Walsh TR, Tyrrell JM. Clinical validation of sensitest colistin, a broth microdilution-based method to evaluate colistin MICs. J Clin Microbiol. 2018;56(4): e01523–17.
   PubMed Web of Science ®Google Scholar
• Pérez-Varela M, Corral J, Aranda J, Barbé J. Roles of efflux pumps from different superfamilies in the surface-associated motility and virulence of Acinetobacter baumannii ATCC 17978. Antimicrob Agents Chemother. 2019;63(3): e02190–18.
   PubMed Web of Science ®Google Scholar
• Leus IV, Weeks JW, Bonifay V, Smith L, Richardson S, Zgurskaya HI. Substrate specificities and efflux efficiencies of RND efflux pumps of Acinetobacter baumannii. J Bacteriol. 2018;200(13):e00049–18.
   PubMed Web of Science ®Google Scholar
• Krahn T, Wibberg D, Maus I, Winkler A, Pühler A, Poirel L, Schlüter A. Complete genome sequence of acinetobacter baumannii CIP 70.10, a susceptible reference strain for comparative genome analyses. Genome Announc. 2015;3(4): e00850–15.
   PubMedGoogle Scholar
• Bonnin RA, Poirel L, Nordmann P. AbaR-type transposon structures in Acinetobacter baumannii. J Antimicrob Chemother. 2012;67(1):234–236.
   PubMed Web of Science ®Google Scholar
• Lu PL, Chang JC, Hsu HT, Chen JH, Chen FJ, Lin SF, Siu LK. One tube multiplex PCR for simple screening of SCCmec I-V types of methicillin-resistant staphylococcus aureus. J Chemother. 2008;20(6):690–696.
   PubMed Web of Science ®Google Scholar
• Hujer KM, Hujer AM, Hulten EA, Bajaksouzian S, Adams JM, Donskey CJ, Ecker DJ, Massire C, Eshoo MW, Sampath R, et al. Analysis of antibiotic resistance genes in multidrug-resistant Acinetobacter sp. isolates from military and civilian patients treated at the Walter Reed Army Medical Center. Antimicrob Agents Chemother. 2006;50(12):4114–4123.
   PubMed Web of Science ®Google Scholar
• Brosius J, Palmer ML, Kennedy PJ, Noller HF. Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci USA. 1978;75(10):4801–4805.
   PubMed Web of Science ®Google Scholar
• Moazzen Z, Eslami G, Hashemi A, Yousefi Nojookambari N. Efflux Pump Inhibitor Carbonyl Cyanide 3-Chlorophenylhydrazone (CCCP) Effect on the Minimum Inhibitory Concentration of Ciprofloxacin in Acinetobacter baumannii Strains. Arch Clin Infect Dis. 2018; 13(2):e59644.
   Web of Science ®Google Scholar
• Kuo HY, Chang KC, Kuo JW, Yueh HW, Liou ML. Imipenem: a potent inducer of multidrug resistance in Acinetobacter baumannii. Int J Antimicrob Agents. 2012;39(1):33–38.
   PubMed Web of Science ®Google Scholar
• Ma Z, Cai SX, Tong WC, Ruan SC, Wang H. [Role of the AdeABC efflux pump in carbapenems resistance of clinical isolates of Acinetobacter baumannii]. Nan Fang Yi Ke Da Xue Xue Bao. 2011;31(8):1378–1381.
   PubMedGoogle Scholar
• Park YK, Ko KS. Effect of carbonyl cyanide 3-chlorophenylhydrazone (CCCP) on killing Acinetobacter baumannii by colistin. J Microbiol. 2015;53(1):53–59.
   PubMed Web of Science ®Google Scholar
• Machado D, Antunes J, Simões A, Perdigão J, Couto I, McCusker M, Martins M, Portugal I, Pacheco T, Batista J, et al. Contribution of efflux to colistin heteroresistance in a multidrug resistant Acinetobacter baumannii clinical isolate. J Med Microbiol. 2018;67(6):740–749.
   PubMed Web of Science ®Google Scholar
• D’Souza R, Pinto NA, Phuong NL, Higgins PG, Vu TN, Byun J-H, et al. Phenotypic and Genotypic Characterization of Acinetobacter spp. Panel Strains: A Cornerstone to Facilitate Antimicrobial Development. Front Microbiol. 2019;10:559.
   PubMed Web of Science ®Google Scholar
• Rumbo C, Gato E, López M, Ruiz de Alegría C, Fernández-Cuenca F, Martínez-Martínez L, Vila J, Pachón J, Cisneros JM, Rodríguez-Baño J, et al. Contribution of efflux pumps, porins, and β-lactamases to multidrug resistance in clinical isolates of Acinetobacter baumannii. Antimicrob Agents Chemother. 2013;57(11):5247–5257.
   PubMed Web of Science ®Google Scholar
• Gerson S, Nowak J, Zander E, Ertel J, Wen Y, Krut O, Seifert H, Higgins PG. 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;73(6):1501–1508.
   PubMed Web of Science ®Google Scholar