Pentamidine sensitizes Gram-negative pathogens to antibiotics and overcomes acquired colistin resistance

Nature Microbiology

Volumn 2, Issue , 2017, Pages

  Stokes, Jonathan M ^a   Macnair, Craig R ^a   Ilyas, Bushra ^a   French, Shawn ^a   Côté, Jean Philippe ^a   Bouwman, Catrien ^b   Farha, Maya A ^a   Sieron, Arthur O ^a   Whitfield, Chris ^b   Coombes, Brian K ^a   Brown, Eric D ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; COLISTIN; PENTAMIDINE;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTION; ANIMAL; ANTIBIOTIC RESISTANCE; DISEASE MODEL; DRUG EFFECT; DRUG POTENTIATION; GRAM NEGATIVE BACTERIUM; METABOLISM; MICROBIOLOGY; PRECLINICAL STUDY; PROCEDURES;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; ANIMALS; ANTI-BACTERIAL AGENTS; COLISTIN; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; DRUG RESISTANCE, BACTERIAL; DRUG SYNERGISM; GRAM-NEGATIVE BACTERIA; PENTAMIDINE;

EID: 85014766280     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2017.28     Document Type: Article

References (44)

1. Nation, R. L. & Li, J. Colistin in the 21st century. Curr. Opin. Infect. Dis. 22, 535-543 (2009).
2. Liu, Y. Y. 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. 16, 161-168 (2016).
3. Needham, B. D. & Trent, M. S. Fortifying the barrier: the impact of lipid A remodelling on bacterial pathogenesis. Nat. Rev. Microbiol. 11, 467-481 (2013).
4. Brown, E. D. & Wright, G. D. Antibacterial drug discovery in the resistance era. Nature 529, 336-343 (2016).
5. Nikaido, H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67, 593-656 (2003).
6. Sands, M., Kron, M. A. & Brown, R. B. Pentamidine: a review. Rev. Infect. Dis. 7, 625-634 (1985).
7. Stokes, J. M., Davis, J. H., Mangat, C. S., Williamson, J. R. & Brown, E. D. Discovery of a small molecule that inhibits bacterial ribosome biogenesis. eLife 3, e03574 (2014).
8. Stokes, J. M. et al. Cold stress makes Escherichia coli susceptible to glycopeptide antibiotics by altering outer membrane integrity. Cell Chem. Biol. 23, 267-277 (2016).
9. Delcour, A. H. Outer membrane permeability and antibiotic resistance. Biochim. Biophys. Acta 1794, 808-816 (2009).
10. Nikaido, H. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264, 382-388 (1994).
11. Gill, E. E., Franco, O. L. & Hancock, R. E. Antibiotic adjuvants: diverse strategies for controlling drug-resistant pathogens. Chem. Biol. Drug Des. 85, 56-78 (2015).
12. Band, V. I. & Weiss, D. S. Mechanisms of antimicrobial peptide resistance in Gram-negative bacteria. Antibiotics 4, 18-41 (2015).
13. MacDonald, I. A. & Kuehn, M. J. Offense and defense: microbial membrane vesicles play both ways. Res. Microbiol. 163, 607-618 (2012).
14. Vaara, M. Agents that increase the permeability of the outer membrane. Microbiol. Rev. 56, 395-411 (1992).
15. Vaara, M. & Vaara, T. Polycations as outer membrane-disorganizing agents. Antimicrob. Agents Chemother. 24, 114-122 (1983).
16. David, S. A. Towards a rational development of anti-endotoxin agents: novel approaches to sequestration of bacterial endotoxins with small molecules. J. Mol. Recognit. 14, 370-387 (2001).
17. Sun, T. & Zhang, Y. Pentamidine binds to tRNA through non-specific hydrophobic interactions and inhibits aminoacylation and translation. Nucleic Acids Res. 36, 1654-1664 (2008).
18. Miletti, K. E. & Leibowitz, M. J. Pentamidine inhibition of group I intron splicing in Candida albicans correlates with growth inhibition. Antimicrob. Agents Chemother. 44, 958-966 (2000).
19. Zhu, W. et al. Antibacterial drug leads: DNA and enzyme multitargeting. J. Med. Chem. 58, 1215-1227 (2015).
20. Ofek, I. et al. Antibacterial synergism of polymyxin B nonapeptide and hydrophobic antibiotics in experimental Gram-negative infections in mice. Antimicrob. Agents Chemother. 38, 374-377 (1994).
21. Clifton, L. A. et al. Effect of divalent cation removal on the structure of Gramnegative bacterial outer membrane models. Langmuir 31, 404-412 (2014).
22. Olaitan, A. O., Morand, S. & Rolain, J. M. Mechanisms of polymyxin resistance: acquired and intrinsic resistance in bacteria. Front. Microbiol. 5, 643 (2014).
23. Bystrova, O. V. et al. Structural studies on the core and the O-polysaccharide repeating unit of Pseudomonas aeruginosa immunotype 1 lipopolysaccharide. Eur. J. Biochem. 269, 2194-2203 (2002).
24. Schoenbach, E. B. & Greenspan, E. M. The pharmacology, mode of action and therapeutic potentialities of stilbamidine, pentamidine, propamidine and other aromatic diamidines: a review. Medicine (Baltimore) 27, 327-377 (1948).
25. Amos, H. & Vollmayer, E. Effect of pentamidine on the growth of Escherichia coli. J. Bacteriol. 73, 172-177 (1957).
26. Ando, M. et al. In situ potentiometric method to evaluate bacterial outer membrane-permeabilizing ability of drugs: example using antiprotozoal diamidines. J. Microbiol. Methods 91, 497-500 (2012).
27. Yeung, K. T., Chan, M. & Chan, C. K. The safety of i.v. pentamidine administered in an ambulatory setting. Chest 110, 136-140 (1996).
28. Ejim, L. et al. Combinations of antibiotics and nonantibiotic drugs enhance antimicrobial efficacy. Nat. Chem. Biol. 7, 348-350 (2011).
29. Dijkshoorn, L., Nemec, A. & Seifert, H. An increasing threat in hospitals:multidrugresistant Acinetobacter baumannii. Nat. Rev. Microbiol. 5, 939-951 (2007).
30. Qureshi, Z. A. et al. Colistin-resistant Acinetobacter baumannii: beyond carbapenem resistance. Clin. Infect. Dis. 60, 1295-1303 (2015).
31. Napier, B. A. et al. Clinical use of colistin induces cross-resistance to host antimicrobials in Acinetobacter baumannii. mBio 4, e00021-13 (2013).
32. Du, H., Chen, L., Tang, Y. W. & Kreiswirth, B. N. Emergence of the mcr-1 colistin resistance gene in carbapenem-resistant enterobacteriaceae. Lancet Infect. Dis. 16, 287-288 (2016).
33. Baba, T. et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006.0008 (2006).
34. Mangat, C. S., Bharat, A., Gehrke, S. S. & Brown, E. D. Rank ordering plate data facilitates data visualization and normalization in high-throughput screening. J. Biomol. Screen. 19, 1314-1320 (2014).
35. French, S. et al. A robust platform for chemical genomics in bacterial systems. Mol. Biol. Cell. 27, 1015-1025 (2016).
36. Ihaka, R. & Gentleman, R. R: a language for data analysis and graphics. J. Comp. Graph. Stat. 5, 299-314 (1996).
37. Keseler, I. M. et al. Ecocyc: fusing model organism databases with systems biology. Nucleic Acids Res. 41, D605-D612 (2013).
38. Karp, P. D. Pathway databases: a case study in computational symbolic theories. Science 293, 2040-2044 (2001).
39. Karp, P. D. et al. Pathway Tools version 19.0 update: software for pathway/ genome informatics and systems biology. Brief. Bioinform. 17, 877-890 (2016).
40. Odds, F. C. Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52, 1 (2003).
41. Hasman, H. et al. Detection of mcr-1 encoding plasmid-mediated colistinresistant Escherichia coli isolates from human bloodstream infection and imported chicken meat, Denmark 2015. Euro Surveill. 20, 30085 (2015).
42. Groisman, E. A. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183, 1835-1842 (2001).
43. O'Neill, A. J., Cove, J. H. & Chopra, I. Mutation frequencies for resistance to fusidic acid and rifampicin in Staphylococcus aureus. J. Antimicrob. Chemother. 47, 647-650 (2001).
44. Mariam, D. H., Mengistu, Y., Hoffner, S. E. & Andersson, D. I. Effect of rpoB mutations conferring rifampin resistance on fitness of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 48, 1289-1294 (2004).