Generation of persister cells of Pseudomonas aeruginosa and Staphylococcus aureus by chemical treatment and evaluation of their susceptibility to membrane-targeting agents

Frontiers in Microbiology

Volumn 8, Issue OCT, 2017, Pages

  Grassi, Lucia ^a   Di Luca, Mariagrazia ^b,c   Maisetta, Giuseppantonio ^a   Rinaldi, Andrea C ^d   Esin, Semih ^a   Trampuz, Andrej ^b   Batoni, Giovanna ^a  

^a UNIVERSITY OF PISA   (Italy)

^b BERLIN INSTITUTE OF HEALTH   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d UNIVERSITY OF CAGLIARI   (Italy)

Author keywords

Antimicrobial peptides; Induction of persistence; Isothermal microcalorimetry; Persisters; Pseudomonas aeruginosa; Staphylococcus aureus

Indexed keywords

CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; CIPROFLOXACIN; COLISTIN; DAPTOMYCIN; GENTAMICIN; LEVOFLOXACIN; MEMBRANE AFFECTING AGENT; MEROPENEM; OXIDOREDUCTASE;

ARTICLE; BACTERIAL CELL; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CELL DENSITY; CHEMOSENSITIVITY; CONTROLLED STUDY; ENZYME ACTIVITY; FLOW CYTOMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIMIT OF DETECTION; METABOLIC ACTIVATION; MICROCALORIMETRY; MINIMUM BACTERICIDAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PERSISTER CELL; PHENOTYPE; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; THERMOGENESIS;

EID: 85030641280     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.01917     Document Type: Article

References (45)

1. 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
2. Batoni, G., Casu, M., Giuliani, A., Luca, V., Maisetta, G., Mangoni, M. L., et al. (2016). Rational modification of a dendrimeric peptide with antimicrobial activity: consequences on membrane-binding and biological properties. Amino Acids 48, 887-900. doi: 10.1007/s00726-015-2136-5
3. Braissant, O., Wirz, D., Göpfert, B., and Daniels, A. U. (2010). Use of isothermal microcalorimetry to monitor microbial activities. FEMS Microbiol. Lett. 303, 1-8. doi: 10.1111/j.1574-6968.2009.01819.x
4. Brauner, A., Fridman, O., Gefen, O., and Balaban, N. Q. (2016). Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nat. Rev. Microbiol. 14, 320-330. doi: 10.1038/nrmicro.2016.34
5. Briers, Y., Walmagh, M., Grymonprez, B., Biebl, M., Pirnay, J., Defraine, V., et al. (2014). Art-175 is highly antibacterial against multidrug-resistant strains and persisters of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 58, 3774-3784. doi: 10.1128/AAC.02668-14
6. Cañas-Duarte, S. J., Restrepo, S., and Pedraza, J. M. (2014). Novel protocol for persister cells isolation. PLOS ONE 9:e88660. doi: 10.1371/journal.pone.0088660
7. Chen, X., Zhang, M., Zhou, C., Kallenbach, N. R., and Ren, D. (2011). Control of bacterial persister cells by Trp/Arg containing antimicrobial peptides. Appl. Environ. Microbiol. 14, 4878-4885. doi: 10.1128/AEM.02440-10
8. Chowdhury, N., Wood, T. L., Martinez-Vazquez, M., Garcia-Contreras, R., and Wood, T. K. (2016). DNA-crosslinker cisplatin eradicates bacterial persister cells. Biotechnol. Bioeng. 113, 1984-1992. doi: 10.1002/bit.25963
9. Conlon, B. P. (2014). Staphylococcus aureus chronic and relapsing infections: evidence of a role for persister cells. Bioessays 36, 991-996. doi: 10.1002/bies.201400080
10. Conlon, B. P., Nakayasu, E. S., Fleck, L. E., LaFleur, M. D., Isabella, V. M., Coleman, K., et al. (2013). Activated ClpP kills persisters and eradicates a chronic biofilm infection. Nature 503, 365-370. doi: 10.1038/nature12790
11. Conlon, B. P., Rowe, S. E., Gandt, A. B., Nuxoll, A. S., Donegan, N. P., Zalis, E. A., et al. (2016). Persister formation in Staphylococcus aureus is associated with ATP depletion. Nat. Microbiol. 1:16051. doi: 10.1038/nmicrobiol.2016.51
12. Cui, P., Niu, H., Shi, W., Zhang, S., Zhang, H., Margolick, J., et al. (2016). Disruption of membrane by colistin kills uropathogenic Escherichia coli persisters and enhances killing of other antibiotics. Antimicrob. Agents Chemother. 60, 6867-6871. doi: 10.1128/AAC.01481-16
13. Di Luca, M., Navari, E., Esin, S., Menichini, M., Barnini, S., Trampuz, A., et al. (2017). Detection of biofilms in biopsies from chronic rhinosinusitis patients: in vitro biofilm forming ability and antimicrobial susceptibility testing in biofilm mode of growth of isolated bacteria. Adv. Exp. Med. Biol. doi: 10.1007/5584_2017_34 [Epub ahead of print].
14. Dörr, T., Lewis, K., and Vulic, M. (2009). SOS response induces persistence to fluoroquinolones in Escherichia coli. PLOS Genet. 5:e1000760. doi: 10.1371/journal.pgen.1000760
15. European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID) (2000). EUCAST definitive document E.Def 1.2, May 2000: terminology relating to methods for the determination of susceptibility of bacteria to antimicrobial agents. Clin. Microbiol. Infect. 6, 503-508. doi: 10.1046/j.1469-0691.2000.00149.x
16. Fauvart, M., De Groote, V. N., and Michiels, J. (2011). Role of persister cells in chronic infections: clinical relevance and perspective on anti-persister therapies. J. Med. Microbiol. 60, 699-709. doi: 10.1099/jmm.0.030932-0
17. Gefen, O., and Balaban, N. Q. (2009). The importance of being persistent: heterogeneity of bacterial populations under antibiotic stress. FEMS Microbiol. Rev. 33, 704-717. doi: 10.1111/j.1574-6976.2008.00156.x
18. Gefen, O., Gabay, C., Mumcuoglu, M., Engel, G., and Balaban, N. Q. (2008). Single-cell protein induction dynamics reveals a period of vulnerability to antibiotics in persister bacteria. Proc. Natl. Acad. Sci. U.S.A. 105, 6145-6149. doi: 10.1073/pnas.0711712105
19. Grassi, L., Maisetta, G., Maccari, G., Esin, S., and Batoni, G. (2017). Analogs of the frog-skin antimicrobial peptide Temporin 1Tb exhibit a wider spectrum of activity and a stronger antibiofilm potential as compared to the parental peptide. Front. Chem. 5:24. doi: 10.3389/fchem.2017.00024
20. Han, H. M., Gopal, M., and Park, Y. (2016). Design and membrane-disruption mechanism of charge-enriched AMPs exhibiting cell selectivity, high-salt resistance, and anti-biofilm properties. Amino Acids 48, 505-522. doi: 10.3389/fchem.2017.00024
21. Henry, T. C., and Brynildsen, M. P. (2016). Development of persister-FACSeq: a method to massively parallelize quantification of persister physiology and its heterogeneity. Sci. Rep. 6:25100. doi: 10.1038/srep25100
22. Jõers, A., Kaldalu, N., and Tenson, T. (2010). The frequency of persisters in Escherichia coli reflects the kinetics of awakening from dormancy. J. Bacteriol. 192, 3379-3384. doi: 10.1128/JB.00056-10
23. Jung, S., Mysliwy, J., Spudy, B., Lorenzen, I., Reiss, K., Gelhaus, C., et al. (2011). Human ß-defensin 2 and ß-defensin 3 chimeric peptides reveal the structural basis of the pathogen specificity of their parent molecules. Antimicrob. Agents Chemother. 55, 954-960. doi: 10.1128/AAC.00872-10
24. Keren, I., Kaldalu, N., Spoering, A., Wang, Y., and Lewis, K. (2004). Persister cells and tolerance to antimicrobials. FEMS Microbiol. Lett. 230, 13-18. doi: 10.1016/S0378-1097(03)00856-5
25. Keren, I., Minami, S., Rubin, E., and Lewis, K. (2011). Characterization and transcriptome analysis of Mycobacterium tuberculosis persisters. mBio 2:e00100-11. doi: 10.1128/mBio.00100-11
26. Kim, J. S., Heo, P., Yang, T. J., Lee, K. S., Cho, D. H., Kim, B. T., et al. (2011). Selective killing of bacterial persisters by a single chemical compound without affecting normal antibiotic-sensitive cells. Antimicrob. Agents Chemother. 55, 5380-5383. doi: 10.1128/AAC.00708-11
27. Kwan, B. W., Chowdhury, N., and Wood, T. K. (2015). Combatting bacterial infections by killing persister cells with mitomycin C. Environ. Microbiol. 17, 4406-4414. doi: 10.1111/1462-2920.12873
28. Kwan, B. W., Valenta, J. A., Benedik, M. J., and Wood, T. K. (2013). Arrested protein synthesis increases persister-like cell formation. Antimicrob. Agents Chemother. 57, 1468-1473. doi: 10.1128/AAC.02135-12
29. Lechner, S., Lewis, K., and Bertram, R. (2012). Staphylococcus aureus persisters tolerant to bactericidal antibiotics. J. Mol. Microbiol. Biotechnol. 22, 235-244. doi: 10.1159/000342449
30. Levin, B. R., and Rozen, D. E. (2006). Non-inherited antibiotic resistance. Nat. Rev. Microbiol. 4, 556-562. doi: 10.1038/nrmicro1445
31. Lewis, K. (2001). Riddle of biofilm resistance. Antimicrob. Agents Chemother. 45, 999-1007. doi: 10.1128/AAC.45.4.999-1007.2001
32. Lewis, K. (2008). Multidrug tolerance of biofilms and persister cells. Curr. Top. Microbiol. Immunol. 322, 107-131. doi: 10.1007/978-3-540-75418-3_6
33. Lewis, K. (2010). Persister cells. Annu. Rev. Microbiol. 64, 357-372. doi: 10.1146/annurev.micro.112408.134306
34. Maisonneuve, E., Castro-Camargo, M., and Gerdes, K. (2013). (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154, 1140-1150. doi: 10.1016/j.cell.2013.07.048
35. Marques, C. N. H., Morozov, A., Planzos, P., and Zelaya, H. M. (2014). The fatty acid signalling molecule cis-2-decenoic acid increases metabolic activity and reverts persisters cells to an antimicrobial-susceptible state. Appl. Environ. Microbiol. 80, 6976-6991. doi: 10.1128/AEM.01576-14
36. Mohamed, M. F., Abdelkhalek, A., and Seleem, M. N. (2016). Evaluation of short synthetic antimicrobial peptides for treatment of drug-resistant and intracellular Staphylococcus aureus. Sci. Rep. 6:29707. doi: 10.1038/srep29707
37. Moker, N., Dean, C. R., and Tao, J. (2010). Pseudomonas aeruginosa increases formation of multidrug-tolerant persister cells in response to quorum-sensing signalling molecules. J. Bacteriol. 192, 1946-1955. doi: 10.1128/JB.01231-09
38. Orman, M. A., and Brynildsen, M. P. (2013). Dormancy is not necessary or sufficient for bacterial persistence. Antimicrob. Agents Chemother. 57, 3230-3239. doi: 10.1128/AAC.00243-13
39. Orman, M. A., Henry, T. C., DeCoste, C. J., and Brynildsen, M. P. (2016). Analyzing persister physiology with fluorescence activated cell sorting. Methods Mol. Biol. 1333, 83-100. doi: 10.1007/978-1-4939-2854-5_8
40. Pan, J., Bahar, A. A., Syed, H., and Ren, D. (2012). Reverting antibiotic tolerance of Pseudomonas aeruginosa PAO1 persister cells by (Z)-4-bromo-5-(bromomethylene)-3-methylfuran-2(5H)-one. PLOS ONE 7:e45778. doi: 10.1371/journal.pone.0045778
41. Shan, Y., Brown Gandt, A., Rowe, S. E., Deisinger, J. P., Conlon, B. P., and Lewis, K. (2017). ATP-dependent persister formation in Escherichia coli. mBio 8:e02267-16. doi: 10.1128/mBio.02267-16
42. Slattery, A., Victorsen, A. H., Brown, A., Hillman, K., and Phillips, G. J. (2013). Isolation of highly persistent mutants of Salmonella enterica Serovar Typhimurium reveals a new toxin-antitoxin module. J. Bacteriol. 195, 647-657. doi: 10.1128/JB.01397-12
43. Strahl, H., and Hamoen, L. W. (2010). Membrane potential is important for bacterial cell division. Proc. Natl. Acad. Sci. U.S.A. 107, 12281-12286. doi: 10.1073/pnas.1005485107
44. Wang, T., El Meouche, I., and Dunlop, M. J. (2017). Bacterial persistence induced by salicylate via reactive oxygen species. Sci. Rep. 7:43839. doi: 10.1038/srep43839
45. Zhang, Y. (2014). Persisters, persistent infections and the Ying-Yang model. Emerg. Microbes Infect. 3:e3. doi: 10.1038/emi.2014.3