A shared mechanism of multidrug resistance in laboratory-evolved uropathogenic Escherichia coli

References

• Nikaido H. Multidrug resistance in bacteria. Annu Rev Biochem. 2009;78(1):119–17. doi: 10.1146/annurev.biochem.78.082907.145923
   PubMedGoogle Scholar
• Blair JM, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJ. Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol. 2015;13(1):42–51. doi: 10.1038/nrmicro3380
   PubMed Web of Science ®Google Scholar
• Micali S, Isgro G, Bianchi G, et al. Cranberry and recurrent cystitis: more than marketing? Crit Rev Food Sci Nutr. 2014;54(8):1063–1075. doi: 10.1080/10408398.2011.625574
   PubMed Web of Science ®Google Scholar
• Flores-Mireles AL, Walker JN, Caparon M, et al. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 2015;13(5):269–284. doi: 10.1038/nrmicro3432
   PubMed Web of Science ®Google Scholar
• Connell I, Agace W, Klemm P, et al. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc Natl Acad Sci, USA. 1996;93(18):9827–9832. doi: 10.1073/pnas.93.18.9827
   PubMed Web of Science ®Google Scholar
• Terlizzi ME, Gribaudo G, Maffei ME. UroPathogenic Escherichia coli (UPEC) infections: virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies. Front Microbiol. 2017;8:1566. doi: 10.3389/fmicb.2017.01566
   PubMed Web of Science ®Google Scholar
• Mobley HL, Green DM, Trifillis AL, et al. Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun. 1990;58(5):1281–1289. doi: 10.1128/iai.58.5.1281-1289.1990
   PubMed Web of Science ®Google Scholar
• Hooton TM. Clinical practice. Uncomplicated urinary tract infection. N Engl J Med. 2012;366(11):1028–1037. doi: 10.1056/NEJMcp1104429
   PubMed Web of Science ®Google Scholar
• Kot B. Antibiotic resistance among uropathogenic Escherichia coli. Pol J Microbiol. 2019;68(4):403–415. doi: 10.33073/pjm-2019-048
   PubMed Web of Science ®Google Scholar
• Habibi A, Khameneie MK. Antibiotic resistance properties of uropathogenic Escherichia coli isolated from pregnant women with history of recurrent urinary tract infections. Trop J Pharm Res. 2016;15(8):1745–1750. doi: 10.4314/tjpr.v15i8.21
   Web of Science ®Google Scholar
• Peck KR, Kim MJ, Choi JY, et al. In vitro time-kill studies of antimicrobial agents against blood isolates of imipenem-resistant Acinetobacter baumannii, including colistin- or tigecycline-resistant isolates. J Med Microbiol. 2012;61(Pt 3):353–360. doi: 10.1099/jmm.0.036939-0
   PubMed Web of Science ®Google Scholar
• Elshikh M, Ahmed S, Funston S, et al. Resazurin-based 96-well plate microdilution method for the determination of minimum inhibitory concentration of biosurfactants. Biotechnol Lett. 2016;38(6):1015–1019. doi: 10.1007/s10529-016-2079-2
   PubMed Web of Science ®Google Scholar
• Bankevich A, Nurk S, Antipov D, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–477. doi: 10.1089/cmb.2012.0021
   PubMed Web of Science ®Google Scholar
• Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformat. 2014;30(14):2068–2069. doi: 10.1093/bioinformatics/btu153
   Google Scholar
• Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformat. 2014;30(15):2114–2120. doi: 10.1093/bioinformatics/btu170
   Google Scholar
• Han Y, Lee EJ. Detecting salmonella type II flagella production by transmission electron microscopy and immunocytochemistry. J Microbiol. 2020;58(4):245–251. doi: 10.1007/s12275-020-9297-y
   PubMed Web of Science ®Google Scholar
• Vega-Hernández R, Ochoa SA, Valle-Rios R, et al. Flagella, type I fimbriae and curli of uropathogenic Escherichia coli promote the release of proinflammatory cytokines in a coculture system. Microorgan. 2021;9(11):2233. doi: 10.3390/microorganisms9112233
   PubMed Web of Science ®Google Scholar
• Garofalo CK, Hooton TM, Martin SM, et al. Escherichia coli from urine of female patients with urinary tract infections is competent for intracellular bacterial community formation. Infect Immun. 2007;75(1):52–60. doi: 10.1128/IAI.01123-06
   PubMed Web of Science ®Google Scholar
• Walters MS, Lane MC, Vigil PD, et al. Kinetics of uropathogenic Escherichia coli metapopulation movement during urinary tract infection. MBio. 2012;3(1). doi: 10.1128/mBio.00303-11
   PubMed Web of Science ®Google Scholar
• Beggs GA, Brennan RG, Arshad M. MarR family proteins are important regulators of clinically relevant antibiotic resistance. Protein Sci. 2020;29(3):647–653. doi: 10.1002/pro.3769
   PubMed Web of Science ®Google Scholar
• Reyes-Fernández EZ, Schuldiner S. Acidification of cytoplasm in Escherichia coli provides a strategy to cope with stress and facilitates development of antibiotic resistance. Sci Rep. 2020;10(1):1–13. doi: 10.1038/s41598-020-66890-1
   PubMed Web of Science ®Google Scholar
• Martin RG, Jair KW, Wolf RE, et al. Autoactivation of the marRAB multiple antibiotic resistance operon by the MarA transcriptional activator in Escherichia coli. J Bacteriol. 1996;178(8):2216–2223. doi: 10.1128/jb.178.8.2216-2223.1996
   PubMed Web of Science ®Google Scholar
• Ma D, Alberti M, Lynch C, et al. The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol Microbiol. 1996;19(1):101–112. doi: 10.1046/j.1365-2958.1996.357881.x
   PubMed Web of Science ®Google Scholar
• Fralick JA. Evidence that TolC is required for functioning of the Mar/AcrAB efflux pump of Escherichia coli. J Bacteriol. 1996;178(19):5803–5805. doi: 10.1128/jb.178.19.5803-5805.1996
   PubMed Web of Science ®Google Scholar
• Sulavik MC, Houseweart C, Cramer C, et al. Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes. Antimicrob Agents Chemother. 2001;45(4):1126–1136. doi: 10.1128/AAC.45.4.1126-1136.2001
   PubMed Web of Science ®Google Scholar
• Nikaido H. Antibiotic resistance caused by gram-negative multidrug efflux pumps. Clin Infect Dis. 1998;27(Supplement_1):S32–S41. doi: 10.1086/514920
   PubMedGoogle Scholar
• Aiba H, Mizuno T. Phosphorylation of a bacterial activator protein, OmpR, by a protein kinase, EnvZ, stimulates the transcription of the ompF and ompC genes in Escherichia coli. FEBS Lett. 1990;261(1):19–22. doi: 10.1016/0014-5793(90)80626-T
   PubMed Web of Science ®Google Scholar
• Cai SJ, Inouye M. Inouye M EnvZ-OmpR interaction and osmoregulation in Escherichia coli. J Biol Chem. 2002;277(27):24155–24161. doi: 10.1074/jbc.M110715200
   PubMed Web of Science ®Google Scholar
• Lan C-Y, Igo MM. Differential expression of the OmpF and OmpC porin proteins in Escherichia coli K-12 depends upon the level of active OmpR. J Bacteriol. 1998;180(1):171–174. doi: 10.1128/JB.180.1.171-174.1998
   PubMed Web of Science ®Google Scholar
• Brigitte Roux B. The binding of antibiotics in OmpF porin. Structure. 2013;21(1):76–87.
   PubMed Web of Science ®Google Scholar
• Ferenci T, Phan K. How porin heterogeneity and trade-offs affect the antibiotic susceptibility of gram-negative bacteria. Genes (Basel). 2015;6(4):1113–1124. doi: 10.3390/genes6041113
   PubMed Web of Science ®Google Scholar
• Chetri S, Singha M, Bhowmik D, et al. Transcriptional response of OmpC and OmpF in Escherichia coli against differential gradient of carbapenem stress. BMC Res Notes. 2019;12(1). doi: 10.1186/s13104-019-4177-4
   PubMedGoogle Scholar
• Choi U, Lee C-R. Distinct roles of outer membrane porins in antibiotic resistance and membrane integrity in Escherichia coli. Front Microbiol. 2019;10:953. doi: 10.3389/fmicb.2019.00953
   PubMedGoogle Scholar
• Uehara T, Dinh T, Bernhardt TG. LytM-domain factors are required for daughter cell separation and rapid ampicillin-induced lysis in Escherichia coli. J Bacteriol. 2009;191(16):5094–5107. doi: 10.1128/JB.00505-09
   PubMed Web of Science ®Google Scholar
• Tsang M-J, Yakhnina AA, Bernhardt TG, et al. NlpD links cell wall remodeling and outer membrane invagination during cytokinesis in Escherichia coli. PloS Genet. 2017;13(7):e1006888. doi: 10.1371/journal.pgen.1006888
   PubMed Web of Science ®Google Scholar
• Connell I, Agace W, Klemm P, et al. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc Natl Acad Sci USA. 1996;93(18):9827–9832. doi: 10.1073/pnas.93.18.9827
   PubMed Web of Science ®Google Scholar
• Schwan WR, Shibata S, Aizawa S-I, et al. The two-component response regulator RcsB regulates type 1 piliation in Escherichia coli. J Bacteriol. 2007;189(19):7159–7163. doi: 10.1128/JB.00705-07
   PubMed Web of Science ®Google Scholar
• Vila J, Soto SM. Salicylate increases the expression of marA and reduces in vitro biofilm formation in uropathogenic Escherichia coli by decreasing type 1 fimbriae expression. Virulence. 2012;3(3):280–285. doi: 10.4161/viru.19205
   PubMed Web of Science ®Google Scholar
• Rentschler AE, Lovrich SD, Fitton R, et al. OmpR regulation of the uropathogenic Escherichia coli fimB gene in an acidic/high osmolality environment. Microbiology. 2013;159(Pt_2):316–327. doi: 10.1099/mic.0.059386-0
   PubMedGoogle Scholar
• Olliver A, Vallé M, Chaslus-Dancla E, et al. Role of an acrR mutation in multidrug resistance of in vitro-selected fluoroquinolone-resistant mutants of salmonella enterica serovar typhimurium. FEMS Microbiol Lett. 2004;238(1):267–272. doi: 10.1111/j.1574-6968.2004.tb09766.x
   PubMed Web of Science ®Google Scholar
• Chetri S, Das BJ, Bhowmik D, et al. Transcriptional response of mar, sox and rob regulon against concentration gradient carbapenem stress within Escherichia coli isolated from hospital acquired infection. BMC Res Notes. 2020;13(1). doi: 10.1186/s13104-020-04999-2
   PubMed Web of Science ®Google Scholar
• Wales A, Davies R. Co-selection of resistance to antibiotics, biocides and heavy metals, and its relevance to foodborne pathogens. Antibiotics. 2015;4(4):567–604. doi: 10.3390/antibiotics4040567
   Google Scholar
• Adler M, Anjum M, Andersson DI, et al. Combinations of mutations in envZ, ftsI, mrdA, acrB and acrR can cause high-level carbapenem resistance in Escherichia coli. J Antimicrob Chemother. 2016;71(5):1188–1198. doi: 10.1093/jac/dkv475
   PubMed Web of Science ®Google Scholar
• Meier S, Weber R, Zbinden R, et al. Extended-spectrum beta-lactamase-producing gram-negative pathogens in community-acquired urinary tract infections: an increasing challenge for antimicrobial therapy. Infection. 2011;39(4):333–340. doi: 10.1007/s15010-011-0132-6
   PubMed Web of Science ®Google Scholar
• Li M, Liu Q, Teng Y, et al. The resistance mechanism of Escherichia coli induced by ampicillin in laboratory. Infect Drug Resist. 2019;12:2853–2863. doi: 10.2147/IDR.S221212
   PubMed Web of Science ®Google Scholar
• Merchel Piovesan Pereira B, Wang X, Tagkopoulos I. Biocide-induced emergence of antibiotic resistance in Escherichia coli. Front Microbiol. 2021;12:640923. doi: 10.3389/fmicb.2021.640923
   PubMedGoogle Scholar
• Alekshun MN, Kim YS, Levy SB. Mutational analysis of MarR, the negative regulator of marRAB expression in Escherichia coli, suggests the presence of two regions required for DNA binding. Mol Microbiol. 2002;35(6):1394–1404. doi: 10.1046/j.1365-2958.2000.01802.x
   Web of Science ®Google Scholar
• Ruiz C, Levy SB. Many chromosomal genes modulate MarA-mediated multidrug resistance in Escherichia coli. Antimicrob Agents Chemother. 2010;54(5):2125–2134. doi: 10.1128/AAC.01420-09
   PubMed Web of Science ®Google Scholar
• Sharma P, Haycocks JRJ, Middlemiss AD, et al. The multiple antibiotic resistance operon of enteric bacteria controls DNA repair and outer membrane integrity. Nat Commun. 2017;8(1). doi: 10.1038/s41467-017-01405-7
   Google Scholar
• Chubiz LM, Rao CV. Role of the mar-sox-rob regulon in regulating outer membrane porin expression. J Bacteriol. 2011;193(9):2252–2260. doi: 10.1128/JB.01382-10
   PubMed Web of Science ®Google Scholar
• McOsker CC, Fitzpatrick PM. Nitrofurantoin: mechanism of action and implications for resistance development in common uropathogens. J Antimicrob Chemother. 1994;33(suppl A):23–30. doi: 10.1093/jac/33.suppl_A.23
   PubMedGoogle Scholar