Roles of the glutathione- and thioredoxin-dependent systems in the Escherichia coli responses to ciprofloxacin and ampicillin

Archives of Microbiology

Volumn 198, Issue 9, 2016, Pages 913-921

  Smirnova, Galina ^a   Muzyka, Nadezda ^a   Lepekhina, Elena ^a,b   Oktyabrsky, Oleg ^a,b  

^a INSTITUTE OF ECOLOGY AND GENETICS OF MICROORGANISMS   (Russian Federation)

^b PERM NATIONAL RESEARCH POLYTECHNIC UNIVERSITY   (Russian Federation)

Author keywords

Antibiotics; Escherichiacoli; Glutathione; Oxidative stress

Indexed keywords

AMPICILLIN; CIPROFLOXACIN; GLUTATHIONE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; THIOREDOXIN; ANTIINFECTIVE AGENT; ANTIOXIDANT; BACTERIAL PROTEIN; GLRX PROTEIN, HUMAN; GLUTAREDOXIN;

ANTIOXIDANT ACTIVITY; ARTICLE; BACTERICIDAL ACTIVITY; CELL WALL; DNA SYNTHESIS; DRUG RESPONSE; ESCHERICHIA COLI; GROWTH RATE; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

AMPICILLIN; ANTI-BACTERIAL AGENTS; ANTIOXIDANTS; BACTERIAL PROTEINS; CIPROFLOXACIN; ESCHERICHIA COLI; GLUTAREDOXINS; GLUTATHIONE; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; THIOREDOXINS;

EID: 84976291699     PISSN: 03028933     EISSN: 1432072X     Source Type: Journal    
DOI: 10.1007/s00203-016-1247-z     Document Type: Article

References (47)

1. Aslund F, Zheng M, Beckwith J, Storz G (1999) Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc Natl Acad Sci USA 96:6161–6165
2. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2(2006):0008
3. Berney M, Weilenmann H-U, Ihssen J, Bassin C, Egli T (2006) Specific growth rate determines the sensitivity of Escherichia coli to thermal, UVA, and solar disinfection. Appl Environ Microbiol 72:2586–2593
4. Carmel-Harel O, Storz G (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stresses. Annu Rev Microbiol 54:439–461
5. Chen W, Zhao Y, Seefeldt T, Guan X (2008) Determination of thiols and disulfides via HPLC quantification of 5-thio-2-nitrobenzoic acid. J Pharm Biomed Anal 48:1375–1380
6. Christman MF, Morgan RW, Jacobson FS, Ames BN (1985) Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41:753–762
7. CLSI (2009) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: approved standard. CLSI publication M07-A8. Clinical and Laboratory Standard Institute, Wayne PA
8. Dhamdhere G, Krishnamoorthy G, Zgurskaya HI (2010) Interplay between drug efflux and antioxidants in Escherichia coli resistance to antibiotics. Antimicrob Agents Chemother 54:5366–5368
9. Dwyer DJ, Belenky PA, Yang JH, MacDonald IC, Martell JD, Takahashi N, Chan CTY, Lobritz MA, Braff D, Schwarz EG, Ye JD, Pati M, Vercruysse M, Ralifo PS, Allison KR, Khalil AS, Ting AY, Walker GC, Collins JJ (2014) Antibiotics induce redox-related physiological alterations as part of their lethality. Proc Natl Acad Sci USA 111:E2100–E2109
10. Eng RHK, Padberg FT, Smith SM, Tan EN, Cherubin CE (1991) Bactericidal effects of antibiotics on slowly growing and nongrowing bacteria. Antimicrob Agents Chemother 35:1824–1828
11. Fahey RC, Brown WC, Adams WB, Worsham MB (1978) Occurrence of glutathione in bacteria. J Bacteriol 133:1126–1129
12. Gilbert P, Collier PJ, Brown MRW (1990) Influence of growth rate on susceptibility to antimicrobial agents: biofilms, cell cycle, dormancy, and stringent response. Antimicrob Agents Chemother 34:1865–1868
13. Goswami M, Jawali N (2007) Glutathione-mediated augmentation of β-lactam antibacterial activity against Escherichia coli. J Antimicrob Chemother 60:184–185
14. Goswami M, Mangoli SH, Jawali N (2006) Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli. Antimicrob Agents Chemother 50:949–954
15. Goswami M, Mangoli SH, Jawali N (2007) Effects of glutathione and ascorbic acid on streptomycin sensitivity of Escherichia coli. Antimicrob Agents Chemother 51:1119–1122
16. s. Letters Appl Microbiol 29:323–326
17. Holmgren A (1989) Thioredoxin and glutaredoxin systems. J Biol Chem 264:13963–13966
18. Imlay JA (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77:755–776
19. Keren I, Wu Y, Inocencio J, Mulcahy LR, Lewis K (2013) Killing by bactericidal antibiotics does not depend on reactive oxygen species. Science 339:1213–1216
20. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins J (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797–810
21. Leavitt RI, Umbarger HE (1962) Isoleucine and valine metabolism in Escherichia coli. XI. Valine inhibition of the growth of Escherichia coli strain K-12. J Bacteriol 83:624–630
22. Leichert LI, Jakob U (2004) Protein thiol modifications visualized in vivo. PLoS Biol 2:e333
23. Lillig CH, Potamitou A, Schwenn J, Vlamis-Gardikas A, Holmgren A (2003) Redox regulation of 3′-phosphoadenylylsulfate reductase from Escherichia coli by glutathione and glutaredoxins. J Biol Chem 278:22325–22330
24. Liu Y, Imlay JA (2013) Cell death from antibiotics without the involvement of reactive oxygen species. Science 339:1210–1213
25. McLaggan D, Rufino H, Jaspars M, Booth IR (2000) Glutathione-dependent conversion of N-ethylmaleimide to the maleamic acid by Escherichia coli: an intracellular detoxification process. Appl Environ Microbiol 66:1393–1399
26. Meyer Y, Buchanan BB, Vignols F, Reichheld JP (2009) Thioredoxins and glutaredoxins: unifying elements in redox biology. Annu Rev Genet 43:335–367
27. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
28. Mishra S, Imlay J (2012) Why do bacteria use so many enzymes to scavenge hydrogen peroxide. Arch Biochem Biophys 525:145–160
29. Park S, Imlay JA (2003) High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J Bacteriol 185:1942–1950
30. Potamitou A, Holmgren A, Vlamis-Gardikas A (2002a) Protein levels of Escherichia coli thioredoxins and glutaredoxins and their relation to null mutants, growth phase, and function. J Biol Chem 277:18561–18567
31. s. J Biol Chem 277:17775–17780
32. Potrykus K, Murphy H, Philippe N, Cashel M (2011) ppGpp is the major source of growth rate control in E. coli. Environ Microbiol 13:563–575
33. Prinz WA, Aslund F, Holmgren A, Beckwith A (1997) The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm. J Biol Chem 272:15661–15667
34. Ritz D, Patel H, Doan B, Zhen M, Aslund F, Storz G, Beckwith J (2000) Thioredoxin 2 is involved in the oxidative stress response in Escherichia coli. J Biol Chem 275:2505–2512
35. Seaver LC, Imlay JA (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183:7173–7181
36. Smirnova G, Muzyka N, Oktyabrsky O (2012) Transmembrane glutathione cycling in growing Escherichia coli cells. Microbiol Res 167:166–172
37. Storz G, Imlay J (1999) Oxidative stress. Cur Opin Microbiol 2:188–194
38. Takemoto T, Zhang Q-M, Yoney S (1998) Different forms in defense against hydrogen peroxide in Escherichia coli. Free Radic Biol Med 24:556–562
39. Tao K (1997) oxyR-dependent induction of Escherichia coli grx gene expression by peroxide stress. J Bacteriol 179:5967–5970
40. Tao K, Makino K, Yonei S, Nacata A, Shinagawa H (1989) Molecular cloning and nucleotide sequencing of oxyR, the positive regulatory gene of a regulon for an adaptive response to oxidative stress in Escherichia coli: homologies between OxyR protein and a family of bacterial activator proteins. Mol Gen Genet 218:371–376
41. Tietze F (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27:502–522
42. Tuomanen E, Cozens R, Tosch W, Zak O, Tomasz A (1986) The rate of killing of Escherichia coli by β-lactam antibiotics is strictly proportional to the rate of bacterial growth. J Gen Microbiol 132:1297–1304
43. Visick JE, Clarke S (1997) RpoS- and OxyR-independent induction of HPI catalase of stationary phase in Escherichia coli and identification of rpoS mutations in common laboratory strains. J Bacteriol 179:4158–4163
44. Vlamis-Gardikas A (2008) The multiple functions of the thiol-based electron flow pathways of Escherichia coli: eternal concepts revised. Biochim Biophys Acta 1780:1170–1200
45. Vlamis-Gardikas A, Potamitou A, Zarivach R, Hochman A, Holmgren A (2002) Characterization of Esherichia coli null mutants for glutaredoxin 2. J Biol Chem 277:10861–10868
46. Wang X, Zhao X (2009) Contribution of oxidative damage to antimicrobial lethality. Antimicrob Agents Chemother 53:1395–1402
47. Weissbach H, Resnick L, Brot N (2005) Methionine sulfoxide reductases: history and cellular role in protecting against oxidative damage. Biochim Biophys Acta 1703:203–212