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Role of secondary oxidative stress in the bactericidal action of antibiotics

Abstract

Exposure to β-lactam, fluoroquinolone and aminoglycoside antibiotics caused an increase in the production of hydrogen peroxide and the expression of OxyR-regulon of the oxidative stress response in Escherichia coli cells. Under the conditions of microaeration, the attenuation of secondary oxidative stress due to the addition of an antioxidant thiourea affected the antibacterial effect of fluoroquinolones. Thiourea potentiated the effect of sub-lethal (which did not reduce the number of colony-forming units below 103/mL) doses of the antibiotic and increased the viability of cells exposed to lethal doses. The addition of thiourea reduced the expression of OxyR-regulon, increased by the sub-lethal antibiotic action, to an antibiotic-free culture level. When exposed to lethal doses, a decrease in the antibiotic-mediated expression of oxidative stress response genes in the presence of thiourea was also observed, however, the expression level remained higher as compared to an antibiotic-free culture. This may indicate the dual role of ROS under antibiotic treatment as the damaging agents contributing to killing and the signal molecules activating stress responses.

About the Authors

A. V. Akhova
Institute of Ecology and Genetics of Microorganisms, Perm Federal Research Center, Ural Branch of the Russian Academy of Sciences
Russian Federation
Golev st. 13, Perm, 614081


A. G. Tkachenko
Institute of Ecology and Genetics of Microorganisms, Perm Federal Research Center, Ural Branch of the Russian Academy of Sciences
Russian Federation
Golev st. 13, Perm, 614081


References

1. Albesa I., Becerra M., Battán P., Páez P. Oxidative stress involved in the antibacterial action of different antibiotics // Biochem. Biophys. Res. Commun. 2004. Vol. 317. N 2. P. 605–609.

2. Becerra M., Paez P., Larovere L., Albesa I. Lipids and DNA oxidation in Staphylococcus aureus as a consequence of oxidative stress generated by ciprofloxacin // Mol. Cell. Biochem. 2006. Vol. 285. N 1–2. P. 29–34.

3. Kohanski M., Dwyer D., Hayete B., Lawrence C., Collins J. A common mechanism of cellular death induced by bactericidal antibiotics // Cell. 2007. Vol. 130. N 5. P. 797–810.

4. Liu Y., Imlay J. Cell death from antibiotics without the involvement of reactive oxygen species // Science. 2013. Vol. 339. N 6124. P. 1210–1213.

5. Van Acker H., Coenye T. The role of reactive oxygen species in antibiotic-mediated killing of bacteria // Trends Microbiol. 2017. Vol. 25. N 6. P. 456–466.

6. Hong Y., Zeng J., Wang X., Drlica K., Zhao X. Poststress bacterial cell death mediated by reactive oxygen species // Proc. Natl. Acad. Sci. U.S.A. 2019. Vol. 116. N 20. P. 10064–10071.

7. Goswami M., Mangoli S., Jawali N. Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli // Antimicrob. Agents Chemother. 2006. Vol. 50. N 3. P. 949–954.

8. Wang X., Zhao X. Contribution of oxidative damage to antimicrobial lethality // Antimicrob. Agents Chemother. 2009. Vol. 53. N 4. P. 1395–1402.

9. Dwyer D., Belenky P., Yang J., et al. Antibiotics induce redox-related physiological alterations as part of their lethality // Proc. Natl. Acad. Sci. U.S.A. 2014. Vol. 111. N 20. P. 2100–2109.

10. Akhova A., Tkachenko A. ATP/ADP alteration as a sign of the oxidative stress development in Escherichia coli cells under antibiotic treatment // FEMS Microbiol. Lett. 2014. Vol. 353. N 1. P. 69–76.

11. Battan P., Barnes A., Albesa I. Resistance to oxidative stress caused by ceftazidime and piperacillin in a biofilm of Pseudomonas // Luminescence. 2004. Vol. 19. N 5. P. 265–70.

12. Boles B., Singh P. Endogenous oxidative stress produces diversity and adaptability in biofilm communities // Proc. Natl. Acad. Sci. U.S.A. 2008. Vol. 105. N 34. P. 12503–12508.

13. Kohanski M., DePristo M., Collins J. Sublethal antibiotic treatment leads to multidrug resistance via radicalinduced mutagenesis // Mol. Cell. 2010. Vol. 37. N. 3. P. 311–320.

14. Imlay J. Pathways of oxidative damage // Annu. Rev. Microbiol. 2003. Vol. 57. P. 395–418.

15. Koutsolioutsou A., Peña-Llopis S., Demple B. Constitutive soxR mutations contribute to multipleantibiotic resistance in clinical Escherichia coli isolates // Antimicrob. Agents Chemother. 2005. Vol. 49. N. 7. P. 2746–2752.

16. Sato Y., Unno Y., Miyazaki C., Ubagai T., Ono Y. Multidrug-resistant Acinetobacter baumannii resists reactive oxygen species and survives in macrophages // Sci. Rep. 2019. Vol. 9. N 1: 17462.

17. Ding H., Demple B. In vivo kinetics of a redoxregulated transcriptional switch // Proc. Natl. Acad. Sci. U.S.A. 1997. Vol. 94. N 16. P. 8445–8449.

18. Miller J.H. Experiments in molecular genetics. N.Y.: Cold Spring Harbor Laboratory Press, 1972. 466 pp.

19. Randall L. Reaction of thiol compounds with peroxidase and hydrogen peroxide // J. Biol. Chem. 1946. Vol. 164. N 2. P. 521–527.

20. Anbar M., Neta P. A compilation of specific bimolecular rate constants for the reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals with inorganic and organic compounds in aqueous solution // Int. J. Appl. Radiat. Isot. 1967. Vol. 18. N 7. P. 493–523.

21. Kelner M., Bagnell R., Welch K. Thioureas react with superoxide radicals to yield a sulfhydryl compound. Explanation for protective effect against paraquat // J. Biol. Chem. 1990. Vol. 265. N 3. P. 1306–1311.

22. Mols M., Pier I., Zwietering M., Abee T. The impact of oxygen availability on stress survival and radical formation of Bacillus cereus // Int. J. Food Microbiol. 2009. Vol. 135. N 3. P. 303–311.

23. Fraud S., Poole K. Oxidative stress induction of the MexXY multidrug efflux genes and promotion of aminoglycoside resistance development in Pseudomonas aeruginosa // Antimicrob. Agents Chemother. 2011. Vol. 55. N 3. P. 1068–1074.

24. Wang X., Kim Y., Hong S., Ma Q., Brown B., Pu M., Tarone A., Benedik M., Peti W., Page R., Wood T. Antitoxin MqsA helps mediate the bacterial general stress response // Nat. Chem. Biol. 2011. Vol. 7. N 6. P. 359–366.

25. Tkachenko A. Stress responses of bacterial cells as mechanism of development of antibiotic tolerance // Appl. Biochem. Microbiol. 2018. Vol. 54. N 2. P. 108–127.


Review

For citations:


Akhova A.V., Tkachenko A.G. Role of secondary oxidative stress in the bactericidal action of antibiotics. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2020;75(4):258-264. (In Russ.)

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ISSN 0137-0952 (Print)