Efflux pump overexpression contributes to tigecycline heteroresistance in Salmonella enterica serovar Typhimurium

Frontiers in Cellular and Infection Microbiology

Volumn 7, Issue FEB, 2017, Pages

  Chen, Yi ^a   Hu, Daxing ^a   Zhang, Qijing ^b   Liao, Xiao Ping ^a   Liu, Ya Hong ^a   Sun, Jian ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

Efflux pump; Heteroresistance; Plasmid; Salmonella enterica serovar Typhimurium; Tigecycline

Indexed keywords

CIPROFLOXACIN; TIGECYCLINE; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CARRIER PROTEIN; MINOCYCLINE;

ACRB GENE; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; DNA MUTATION; DNA SEQUENCE; DRUG ACCUMULATION; ELECTROPORATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OQXAB GENE; RAMR GENE; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; UPREGULATION; ANALOGS AND DERIVATIVES; DRUG EFFECTS; GENETICS; MICROBIOLOGY; MULTIDRUG RESISTANCE; MUTATION; PLASMID; SALMONELLOSIS;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; MEMBRANE TRANSPORT PROTEINS; MINOCYCLINE; MUTATION; PLASMIDS; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SEQUENCE ANALYSIS, DNA;

EID: 85014728690     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2017.00037     Document Type: Article

References (47)

1. Abouzeed, Y. M., Baucheron, S., and Cloeckaert, A. (2008). ramR mutations involved in efflux-mediated multidrug resistance in Salmonella enterica serovar Typhimurium. Antimicrob. Agents Chemother. 52, 2428-2434. doi: 10.1128/AAC.00084-08
2. Akiyama, T., Presedo, J., and Khan, A. A. (2013). The tetA gene decreases tigecycline sensitivity of Salmonella enterica isolates. Int. J. Antimicrob. Agents 42, 133-140. doi: 10.1016/j.ijantimicag.2013.04.017
3. Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L., and Leibler, S. (2004). Bacterial persistence as a phenotypic switch. Science 305, 1622-1625. doi: 10.1126/science.1099390
4. Dean, C. R., Visalli, M. A., Projan, S. J., Sum, P. E., and Bradford, P. A. (2003). Efflux-mediated resistance to tigecycline (GAR-936) in Pseudomonas aeruginosa PAO1. Antimicrob. Agents Chemother. 47, 972-978. doi: 10.1128/AAC.47.3.972-978.2003
5. Deresinski, S. (2009). Vancomycin heteroresistance and methicillin-resistant Staphylococcus aureus. J. Infect. Dis. 199, 605-609. doi: 10.1086/596630
6. Du, D., Wang, Z., James, N. R., Voss, J. E., Klimont, E., Ohene-Agyei, T., et al. (2014). Structure of the AcrAB-TolC multidrug efflux pump. Nature 509, 512-515. doi: 10.1038/nature13205
7. El-Halfawy, O. M., and Valvano, M. A. (2015). Antimicrobial heteroresistance: an emerging field in need of clarity. Clin. Microbiol. Rev. 28, 191-207. doi: 10.1128/CMR.00058-14
8. Fàbrega, A., Sánchez-Céspedes, J., Soto, S., and Vila, J. (2008). Quinolone resistance in the food chain. Int. J. Antimicrob. Agents 31, 307-315. doi: 10.1016/j.ijantimicag.2007.12.010
9. Falagas, M. E., Makris, G. C., Dimopoulos, G., and Matthaiou, D. K. (2008). Heteroresistance: a concern of increasing clinical significance? Clin. Microbiol. Infect. 14, 101-104. doi: 10.1111/j.1469-0691.2007.01912.x
10. Fluit, A. C., Florijn, A., Verhoef, J., and Milatovic, D. (2005). Presence of tetracycline resistance determinants and susceptibility to tigecycline and minocycline. Antimicrob. Agents Chemother. 49, 1636-1638. doi: 10.1128/AAC.49.4.1636-1638.2005
11. Gomes, D. M., Ward, K. E., and LaPlante, K. L. (2015). Clinical implications of vancomycin heteroresistant and intermediately susceptible Staphylococcus aureus. Pharmacother. 35, 424-432. doi: 10.1002/phar.1577
12. Hentschke, M., Christner, M., Sobottka, I., Aepfelbacher, M., and Rohde, H. (2010). Combined ramR mutation and presence of a Tn1721-associated tet(A) variant in a clinical isolate of Salmonella enterica serovar Hadar resistant to tigecycline. Antimicrob. Agents Chemother. 54, 1319-1322. doi: 10.1128/AAC.00993-09
13. Herrera, M., Di Gregorio, S., Fernandez, S., Posse, G., Mollerach, M., and Di Conza, J. (2016). In vitro selection of Staphylococcus aureus mutants resistant to tigecycline with intermediate susceptibility to vancomycin. Ann. Clin. Microbiol. Antimicrob. 15, 15. doi: 10.1186/s12941-016-0131-7
14. Hope, R., Warner, M., Mushtaq, S., Ward, M. E., Parsons, T., and Livermore, D. M. (2005). Effect of medium type, age and aeration on the MICs of tigecycline and classical tetracyclines. J. Antimicrob. Chemother. 56, 1042-1046. doi: 10.1093/jac/dki386
15. Horiyama, T., Nikaido, E., Yamaguchi, A., and Nishino, K. (2011). Roles of Salmonella multidrug efflux pumps in tigecycline resistance. J. Antimicrob. Chemother. 66, 105-110. doi: 10.1093/jac/dkq421
16. Hornsey, M., Ellington, M. J., Doumith, M., Scott, G., Livermore, D. M., and Woodford, N. (2010). Emergence of AcrAB-mediated tigecycline resistance in a clinical isolate of Enterobacter cloacae during ciprofloxacin treatment. Int. J. Antimicrob. Agents 35, 478-481. doi: 10.1016/j.ijantimicag.2010.01.011
17. Hung, K. H., Wang, M. C., Huang, A. H., Yan, J. J., and Wu, J. J. (2012). Heteroresistance to cephalosporins and penicillins in Acinetobacter baumannii. J. Clin. Microbiol. 50, 721-726. doi: 10.1128/JCM.05085-11
18. Jenner, L., Starosta, A. L., Terry, D. S., Mikolajka, A., Filonava, L., Yusupov, M., et al. (2013). Structural basis for potent inhibitory activity of the antibiotic tigecycline during protein synthesis. Proc. Natl. Acad. Sci. U.S.A. 110, 3812-3816. doi: 10.1073/pnas.1216691110
19. Jiménez-Castellanos, J. C., Wan Ahmad Kamil, W. N., Cheung, C. H., Tobin, M. S., Brown, J., Isaac, S. G., et al. (2016). Comparative effects of overproducing the AraC-type transcriptional regulators MarA, SoxS, RarA and RamA on antimicrobial drug susceptibility in Klebsiella pneumoniae. J. Antimicrob. Chemother. 71, 1820-1825. doi: 10.1093/jac/dkw088
20. Keeney, D., Ruzin, A., and Bradford, P. A. (2007). RamA, a transcriptional regulator, and AcrAB, an RND-type efflux pump, are associated with decreased susceptibility to tigecycline in Enterobacter cloacae. Microb. Drug Resist. 13, 1-6. doi: 10.1089/mdr.2006.9990
21. Keeney, D., Ruzin, A., McAleese, F., Murphy, E., and Bradford, P. A. (2008). MarA-mediated overexpression of the AcrAB efflux pump results in decreased susceptibility to tigecycline in Escherichia coli. J. Antimicrob. Chemother. 61, 46-53. doi: 10.1093/jac/dkm397
22. Kehrenberg, C., Cloeckaert, A., Klein, G., and Schwarz, S. (2009). Decreased fluoroquinolone susceptibility in mutants of Salmonella serovars other than Typhimurium: detection of novel mutations involved in modulated expression of ramA and soxS. J. Antimicrob. Chemother. 64, 1175-1180. doi: 10.1093/jac/dkp347
23. Lee, H. Y., Chen, C. L., Wang, S. B., Su, L. H., Chen, S. H., Liu, S. Y., et al. (2011). Imipenem heteroresistance induced by imipenem in multidrug-resistant Acinetobacter baumannii: mechanism and clinical implications. Int. J. Antimicrob. Agents 37, 302-308. doi: 10.1016/j.ijantimicag.2010.12.015
24. Li, C., Sutherland, C. A., Nightingale, C. H., and Nicolau, D. P. (2004). Quantitation of tigecycline, a novel glycylcycline [corrected] by liquid chromatography. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 811, 225-229. doi: 10.1016/S1570-0232(04)00745-7
25. Li, L., Liao, X., Yang, Y., Sun, J., Li, L., Liu, B., et al. (2013). Spread of oqxAB in Salmonella enterica serotype Typhimurium predominantly by IncHI2 plasmids. J. Antimicrob. Chemother. 68, 2263-2268. doi: 10.1093/jac/dkt209
26. Liu, Y.-Y., Wang, Y., Walsh, T. R., Yi, L.-X., Zhang, R., Spencer, J., et al. (2016). 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. 16, 161-168. doi: 10.1016/S1473-3099(15)00424-7
27. Moore, M. R., Perdreau-Remington, F., and Chambers, H. F. (2003). Vancomycin treatment failure associated with heterogeneous vancomycin-intermediate Staphylococcus aureus in a patient with endocarditis and in the rabbit model of endocarditis. Antimicrob. Agents Chemother. 47, 1262-1266. doi: 10.1128/AAC.47.4.1262-1266.2003
28. Morand, B., and Mühlemann, K. (2007). Heteroresistance to penicillin in Streptococcus pneumoniae. Proc. Natl. Acad. Sci. U.S.A. 104, 14098-14103. doi: 10.1073/pnas.0702377104
29. Nikaido, E., Yamaguchi, A., and Nishino, K. (2008). AcrAB multidrug efflux pump regulation in Salmonella enterica serovar Typhimurium by RamA in response to environmental signals. J. Biol. Chem. 283, 24245-24253. doi: 10.1074/jbc.M804544200
30. Olliver, A., Vallé, M., Chaslus-Dancla, E., and Cloeckaert, A. (2004). Role of an acrR mutation in multidrug resistance of in vitro-selected fluoroquinolone-resistant mutants of Salmonella enterica serovar Typhimurium. FEMS Microbiol. Lett. 238, 267-272. doi: 10.1016/j.femsle.2004.07.046
31. Ong, C. T., Babalola, C. P., Nightingale, C. H., and Nicolau, D. P. (2005). Penetration, efflux and intracellular activity of tigecycline in human polymorphonuclear neutrophils (PMNs). J. Antimicrob. Chemother. 56, 498-501. doi: 10.1093/jac/dki260
32. Pérez, A., Poza, M., Aranda, J., Latasa, C., Medrano, F. J., Tomás, M., et al. (2012). Effect of transcriptional activators SoxS, RobA, and RamA on expression of multidrug efflux pump AcrAB-TolC in Enterobacter cloacae. Antimicrob. Agents Chemother. 56, 6256-6266. doi: 10.1128/AAC.01085-12
33. Pournaras, S., Kristo, I., Vrioni, G., Ikonomidis, A., Poulou, A., Petropoulou, D., et al. (2010). Characteristics of meropenem heteroresistance in Klebsiella pneumoniae carbapenemase (KPC)-producing clinical isolates of K. pneumoniae. J. Clin. Microbiol. 48, 2601-2604. doi: 10.1128/JCM.02134-09
34. Ruzin, A., Keeney, D., and Bradford, P. A. (2007). AdeABC multidrug efflux pump is associated with decreased susceptibility to tigecycline in Acinetobacter calcoaceticus-Acinetobacter baumannii complex. J. Antimicrob. Chemother. 59, 1001-1004. doi: 10.1093/jac/dkm058
35. Sánchez-Romero, M. A., and Casadesús, J. (2014). Contribution of phenotypic heterogeneity to adaptive antibiotic resistance. Proc. Natl. Acad. Sci. U.S.A. 111, 355-360. doi: 10.1073/pnas.1316084111
36. Smith, S. I., Seriki, A., and Ajayi, A. (2016). Typhoidal and non-typhoidal Salmonella infections in Africa. Eur. J. Clin. Microbiol. Infect. Dis. 35, 1913-1922. doi: 10.1007/s10096-016-2760-3
37. Stein, G. E., and Babinchak, T. (2013). Tigecycline: an update. Diagn. Microbiol. Infect. Dis. 75, 331-336. doi: 10.1016/j.diagmicrobio.2012.12.004
38. Sun, Y., Dai, M., Hao, H., Wang, Y., Huang, L., Almofti, Y. A., et al. (2011). The role of RamA on the development of ciprofloxacin resistance in Salmonella enterica serovar Typhimurium. PLoS ONE 6:e23471. doi: 10.1371/journal.pone.0023471
39. Taneja, N., and Kaur, H. (2016). Insights into Newer Antimicrobial Agents Against Gram-negative Bacteria. Microbiol. Insights 9, 9-19. doi: 10.4137/MBI.S29459
40. Tang, H. J., Chen, C. C., and Ko, W. C. (2016). Tigecycline therapy for bacteremia and aortitis caused by Salmonella enterica serotype Choleraesuis: a case report. J. Microbiol. Immunol. Infect. 49, 131-133. doi: 10.1016/j.jmii.2012.01.011
41. Veleba, M., De Majumdar, S., Hornsey, M., Woodford, N., and Schneiders, T. (2013). Genetic characterization of tigecycline resistance in clinical isolates of Enterobacter cloacae and Enterobacter aerogenes. J. Antimicrob. Chemother. 68, 1011-1018. doi: 10.1093/jac/dks530
42. Veleba, M., Higgins, P. G., Gonzalez, G., Seifert, H., and Schneiders, T. (2012). Characterization of RarA, a Novel AraC family multidrug resistance regulator in Klebsiella pneumoniae. Antimicrob. Agents Chemother. 56, 4450-4458. doi: 10.1128/AAC.00456-12
43. Wong, M. H., Chan, E. W., and Chen, S. (2015). Evolution and dissemination of OqxAB-like efflux pumps, an emerging quinolone resistance determinant among members of Enterobacteriaceae. Antimicrob. Agents Chemother. 59, 3290-3297. doi: 10.1128/AAC.00310-15
44. Yao, X., Doi, Y., Zeng, L., Lv, L., and Liu, J.-H. (2016). Carbapenem-resistant and colistin-resistant Escherichia coli co-producing NDM-9 and MCR-1. Lancet Infect. Dis. 16, 288-289. doi: 10.1016/S1473-3099(16)00057-8
45. Zheng, J., Cui, S., and Meng, J. (2009). Effect of transcriptional activators RamA and SoxS on expression of multidrug efflux pumps AcrAB and AcrEF in fluoroquinolone-resistant Salmonella Typhimurium. J. Antimicrob. Chemother. 63, 95-102. doi: 10.1093/jac/dkn448
46. Zheng, J., Tian, F., Cui, S., Song, J., Zhao, S., Brown, E. W., et al. (2011). Differential gene expression by RamA in ciprofloxacin-resistant Salmonella Typhimurium. PLoS ONE 6:e22161. doi: 10.1371/journal.pone.0022161
47. Zhong, X., Xu, H., Chen, D., Zhou, H., Hu, X., and Cheng, G. (2014). First emergence of acrAB and oqxAB mediated tigecycline resistance in clinical isolates of Klebsiella pneumoniae pre-dating the use of tigecycline in a Chinese hospital. PLoS ONE 9:e115185. doi: 10.1371/journal.pone.0115185