Polymyxin Resistance in Acinetobacter baumannii: Genetic Mutations and Transcriptomic Changes in Response to Clinically Relevant Dosage Regimens

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Cheah, Soon Ee ^a   Johnson, Matthew D ^a   Zhu, Yan ^a   Tsuji, Brian T ^b   Forrest, Alan ^b,c   Bulitta, Jurgen B ^a,d   Boyce, John D ^a   Nation, Roger L ^a   Li, Jian ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY AT BUFFALO   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d UNIVERSITY OF FLORIDA HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; PMRB PROTEIN, BACTERIA; POLYMYXIN; TRANSCRIPTION FACTOR;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTION; ANTIBIOTIC RESISTANCE; BACTERIAL COUNT; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; MICROBIAL VIABILITY; MICROBIOLOGY; MUTATION; TIME FACTOR;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; COLONY COUNT, MICROBIAL; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENOMICS; HUMANS; MICROBIAL VIABILITY; MUTATION; POLYMYXINS; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 84969940536     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep26233     Document Type: Article

References (48)

1. Walker, B. et al. Environment. Looming global-scale failures and missing institutions. Science 325, 1345-1346, doi: 10.1126/science.1175325 (2009).
2. Gales, A. C., Castanheira, M., Jones, R. N. & Sader, H. S. Antimicrobial resistance among Gram-negative bacilli isolated from Latin America: results from SENTRY Antimicrobial Surveillance Program (Latin America, 2008-2010). Diagn Microbiol Infect Dis 73, 354-360, doi: 10.1016/j.diagmicrobio.2012.04.007 (2012).
3. Sader, H. S., Farrell, D. J., Flamm, R. K. & Jones, R. N. Antimicrobial susceptibility of Gram-negative organisms isolated from patients hospitalized in intensive care units in United States and European hospitals (2009-2011). Diagn Microbiol Infect Dis, doi: 10.1016/j.diagmicrobio.2013.11.025 (2013).
4. Peleg, A. Y., Seifert, H. & Paterson, D. L. Acinetobacter baumannii: emergence of a successful pathogen. Clin Microbiol Rev 21, 538-582, doi: 10.1128/CMR.00058-07 (2008).
5. Nation, R. L., Velkov, T. & Li, J. Colistin and polymyxin B: peas in a pod, or chalk and cheese? Clin Infect Dis 59, 88-94, doi: 10.1093/cid/ciu213 (2014).
6. Nation, R. L. & Li, J. Colistin in the 21st century. Curr Opin Infect Dis 22, 535-543, doi: 10.1097/QCO.0b013e328332e672 (2009).
7. Zavascki, A. P., Goldani, L. Z., Li, J. & Nation, R. L. Polymyxin B for the treatment of multidrug-resistant pathogens: a critical review. J Antimicrob Chemother 60, 1206-1215, doi: 10.1093/jac/dkm357 (2007).
8. Jones, R. N. et al. Susceptibility rates in Latin American nations: report from a regional resistance surveillance program (2011). Braz J Infect Dis 17, 672-681, doi: 10.1016/j.bjid.2013.07.002 (2013).
9. Zhanel, G. G. et al. Antimicrobial susceptibility of 22746 pathogens from Canadian hospitals: results of the CANWARD 2007-11 study. J Antimicrob Chemother 68 Suppl 1, i7-22, doi: 10.1093/jac/dkt022 (2013).
10. Kim, S. Y., Shin, J., Shin, S. Y. & Ko, K. S. Characteristics of carbapenem-resistant Enterobacteriaceae isolates from Korea. Diagn Microbiol Infect Dis 76, 486-490, doi: 10.1016/j.diagmicrobio.2013.04.006 (2013).
11. Velkov, T., Thompson, P. E., Nation, R. L. & Li, J. Structure-activity relationships of polymyxin antibiotics. J Med Chem 53, 1898-1916, doi: 10.1021/jm900999h (2010).
12. Sampson, T. R. et al. Rapid killing of Acinetobacter baumannii by polymyxins is mediated by a hydroxyl radical death pathway. Antimicrob Agents Chemother 56, 5642-5649, doi: 10.1128/AAC.00756-12 (2012).
13. Deris, Z. Z. et al. A secondary mode of action of polymyxins against Gram-negative bacteria involves the inhibition of NADHquinone oxidoreductase activity. J Antibiot (Tokyo) 67, 147-151, doi: 10.1038/ja.2013.111 (2014).
14. Hale, J. D. & Hancock, R. E. Alternative mechanisms of action of cationic antimicrobial peptides on bacteria. Expert Rev Anti Infect Ther 5, 951-959, doi: 10.1586/14787210.5.6.951 (2007).
15. Hancock, R. E. & Chapple, D. S. Peptide antibiotics. Antimicrob Agents Chemother 43, 1317-1323 (1999).
16. Zhang, L., Dhillon, P., Yan, H., Farmer, S. & Hancock, R. E. Interactions of bacterial cationic peptide antibiotics with outer and cytoplasmic membranes of Pseudomonas aeruginosa. Antimicrob Agents Chemother 44, 3317-3321, doi: 10.1128/aac.44.12.3317-3321.2000 (2000).
17. Arroyo, L. A. et al. The pmrCAB operon mediates polymyxin resistance in Acinetobacter baumannii ATCC 17978 and clinical isolates through phosphoethanolamine modification of lipid A. Antimicrob Agents Chemother 55, 3743-3751, doi: 10.1128/AAC.00256-11 (2011).
18. Moffatt, J. H. et al. Insertion sequence ISAba11 is involved in colistin resistance and loss of lipopolysaccharide in Acinetobacter baumannii. Antimicrob Agents Chemother 55, 3022-3024 (2011).
19. Moffatt, J. H. et al. Colistin resistance in Acinetobacter baumannii is mediated by complete loss of lipopolysaccharide production. Antimicrob Agents Chemother 54, 4971-4977 (2010).
20. Chin, C. Y., Gregg, K. A., Napier, B. A., Ernst, R. K. & Weiss, D. S. A PmrB-regulated deacetylase required for lipid A modification and polymyxin resistance in Acinetobacter baumannii. Antimicrob Agents Chemother, doi: 10.1128/AAC.00515-15 (2015).
21. Park, Y. K., Choi, J. Y., Shin, D. & Ko, K. S. Correlation between overexpression and amino acid substitution of the PmrAB locus and colistin resistance in Acinetobacter baumannii. Int J Antimicrob Agents 37, 525-530 (2011).
22. Plachouras, D. et al. Population pharmacokinetic analysis of colistin methanesulfonate and colistin after intravenous administration in critically ill patients with infections caused by gram-negative bacteria. Antimicrob Agents Chemother 53, 3430-3436, doi: 10.1128/AAC.01361-08 (2009).
23. Garonzik, S. M. et al. Population pharmacokinetics of colistin methanesulfonate and formed colistin in critically ill patients from a multicenter study provide dosing suggestions for various categories of patients. Antimicrob Agents Chemother 55, 3284-3294 (2011).
24. Karaiskos, I. et al. Colistin population pharmacokinetics after application of a loading dose of 9 MU colistin methanesulfonate (CMS) in critically ill patients. Antimicrob Agents Chemother, doi: 10.1128/AAC.00554-15 (2015).
25. Sandri, A. M. et al. Population pharmacokinetics of intravenous polymyxin B in critically ill patients: implications for selection of dosage regimens. Clin Infect Dis 57, 524-531, doi: 10.1093/cid/cit334 (2013).
26. Gales, A. C., Reis, A. O. & Jones, R. N. Contemporary assessment of antimicrobial susceptibility testing methods for polymyxin B and colistin: review of available interpretative criteria and quality control guidelines. J Clin Microbiol 39, 183-190, doi: 10.1128/JCM.39.1.183-190.2001 (2001).
27. Adams, M. D. et al. Comparative genome sequence analysis of multidrug-resistant Acinetobacter baumannii. J Bacteriol 190, 8053-8064, doi: 10.1128/JB.00834-08 (2008).
28. Diancourt, L., Passet, V., Nemec, A., Dijkshoorn, L. & Brisse, S. The population structure of Acinetobacter baumannii: expanding multiresistant clones from an ancestral susceptible genetic pool. PLoS One 5, e10034, doi: 10.1371/journal.pone.0010034 (2010).
29. Bergen, P. J. et al. Comparison of once-, twice- and thrice-daily dosing of colistin on antibacterial effect and emergence of resistance: studies with Pseudomonas aeruginosa in an in vitro pharmacodynamic model. J Antimicrob Chemother 61, 636-642, doi: 10.1093/jac/dkm511 (2008).
30. Mohamed, A. F. et al. Application of a loading dose of colistin methanesulfonate in critically ill patients: population pharmacokinetics, protein binding, and prediction of bacterial kill. Antimicrob Agents Chemother 56, 4241-4249, doi: 10.1128/aac.06426-11 (2012).
31. Henry, R. et al. The transcriptomic response of Acinetobacter baumannii to colistin and doripenem alone and in combination in an in vitro pharmacokinetics/pharmacodynamics model. J Antimicrob Chemother 70, 1303-1313, doi: 10.1093/jac/dku536 (2015).
32. Garrison, E. & Marth, G. Haplotype-based variant detection from short-read sequencing. Preprint at arXiv:1207.3907v2 [q-bio.GN] (2012).
33. Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43, e47, doi: 10.1093/nar/gkv007 (2015).
34. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57, 289-300 (1995).
35. Jones, P. et al. Inter ProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236-1240, doi: 10.1093/bioinformatics/btu031 (2014).
36. Le Cao, K. A., Boitard, S. & Besse, P. Sparse PLS discriminant analysis: biologically relevant feature selection and graphical displays for multiclass problems. BMC bioinformatics 12, 253, doi: 10.1186/1471-2105-12-253 (2011).
37. Li, L., Stoeckert, C. J. Jr. & Roos, D. S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome res 13, 2178-2189, doi: 10.1101/gr.1224503 (2003).
38. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15, 550, doi: 10.1186/s13059-014-0550-8 (2014).
39. Drusano, G. L. et al. Interaction of drug- and granulocyte-mediated killing of Pseudomonas aeruginosa in a murine pneumonia model. J Infect Dis 210, 1319-1324, doi: 10.1093/infdis/jiu237 (2014).
40. Drusano, G. L. et al. Saturability of granulocyte kill of Pseudomonas aeruginosa in a murine model of pneumonia. Antimicrob Agents Chemother 55, 2693-2695, doi: 10.1128/AAC.01687-10 (2011).
41. Nation, R. L. et al. Framework for optimisation of the clinical use of colistin and polymyxin B: the Prato polymyxin consensus. Lancet Infect Dis 15, 225-234, doi: 10.1016/s1473-3099(14)70850-3 (2015).
42. Adams, M. D. et al. Resistance to colistin in Acinetobacter baumannii associated with mutations in the PmrAB two-component system. Antimicrob Agents Chemother 53, 3628-3634, doi: 10.1128/AAC.00284-09 (2009).
43. Falagas, M. E., Rafailidis, P. I. & Matthaiou, D. K. Resistance to polymyxins: Mechanisms, frequency and treatment options. Drug Resist Updat 13, 132-138, doi: 10.1016/j.drup.2010.05.002 (2010).
44. Kim, K. S., Rao, N. N., Fraley, C. D. & Kornberg, A. Inorganic polyphosphate is essential for long-term survival and virulence factors in Shigella and Salmonella spp. Proc Natl Acad Sci USA 99, 7675-7680, doi: 10.1073/pnas.112210499 (2002).
45. Maifiah, M. H. M. et al. In interscience conference of antimicrobial agents and chemotherapy (San Diego, 2015).
46. Abdul Rahim, N. et al. Synergistic killing of NDM-producing MDR Klebsiella pneumoniae by two 'old' antibiotics-polymyxin B and chloramphenicol. J Antimicrob Chemother 70, 2589-2597, doi: 10.1093/jac/dkv135 (2015).
47. Li, J. et al. Antibiograms of multidrug-resistant clinical Acinetobacter baumannii: promising therapeutic options for treatment of infection with colistin-resistant strains. Clin Infect Dis 45, 594-598, doi: 10.1086/520658 (2007).
48. Deris, Z. Z. et al. The combination of colistin and doripenem is synergistic against Klebsiella pneumoniae at multiple inocula and suppresses colistin resistance in an in vitro pharmacokinetic/pharmacodynamic model. Antimicrob Agents Chemother 56, 5103-5112, doi: 10.1128/AAC.01064-12 (2012).