Metabolic response of Escherichia coli upon treatment with hypochlorite at sub-lethal concentrations

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Drazic, Adrian ^a   Kutzner, Erika ^b   Winter, Jeannette ^a   Eisenreich, Wolfgang ^b  

^a Munich Center for Integrated Protein Science   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOCHLORITE; AMINO ACID; FATTY ACID; HYPOCHLOROUS ACID; SOLVENT;

AMINO ACID METABOLISM; ARTICLE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIAL VIABILITY; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL STRESS; ESCHERICHIA COLI; FATTY ACID METABOLISM; MASS FRAGMENTOGRAPHY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATIVE STRESS; PRINCIPAL COMPONENT ANALYSIS; PROTEOMICS; CELL MEMBRANE; DRUG EFFECTS; METABOLISM; METABOLOME; METABOLOMICS; PHYSIOLOGICAL STRESS; PROTON NUCLEAR MAGNETIC RESONANCE; TIME FACTOR;

ESCHERICHIA COLI;

AMINO ACIDS; CELL MEMBRANE; ESCHERICHIA COLI; FATTY ACIDS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HYPOCHLOROUS ACID; MAGNETIC RESONANCE SPECTROSCOPY; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; METABOLOMICS; PRINCIPAL COMPONENT ANALYSIS; PROTON MAGNETIC RESONANCE SPECTROSCOPY; SOLVENTS; STRESS, PHYSIOLOGICAL; TIME FACTORS;

EID: 84928800236     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125823     Document Type: Article

References (50)

1. Ha EM, Oh CT, Bae YS, Lee WJ. A direct role for dual oxidase in Drosophila gut immunity. Science 2005; 310: 847-850. doi: 10.1126/science.1117311 PubMed PMID: 16272120.
2. Roos D, Winterbourn CC. Immunology. Lethal weapons. Science 2002; 296: 669-671. doi: 10.1126/science.1071271 ;296/5568/669 [pii]. PMID: 11976433
3. Gabbita SP, Aksenov MY, Lovell MA, Markesbery WR. Decrease in peptide methionine sulfoxide reductase in Alzheimer's disease brain. J Neurochem. 1999; 73: 1660-1666. PMID: 10501213
4. Stadtman ER. Protein oxidation and aging. Science 1992; 257: 1220-1224. PubMed PMID: 1355616.
5. Dukan S, Nystrom T. Bacterial senescence: stasis results in increased and differential oxidation of cytoplasmic proteins leading to developmental induction of the heat shock regulon. Genes Dev. 1998; 12: 3431-3441. PubMed PMID: 9808629; PubMed Central PMCID: PMC317226.
6. Drazic A, Tsoutsoulopoulos A, Peschek J, Gundlach J, Krause M, Bach NC, et al. Role of cysteines in the stability and DNA-binding activity of the hypochlorite-specific transcription factor HypT. PLoS One 2013; 8: e75683. doi: 10.1371/journal.pone.0075683 PubMed PMID: 24116067; PubMed Central PMCID: PMC3792123.
7. Miller RA, Britigan BE. Role of oxidants in microbial pathophysiology. Clin Microbiol Rev. 1997; 10: 1-18. PMID: 8993856
8. Candeias LP, Stratford MR, Wardman P. Formation of hydroxyl radicals on reaction of hypochlorous acid with ferrocyanide, a model iron(II) complex. Free Radic Res. 1994; 20: 241-249. PubMed PMID: 8205226.
9. Dukan S, Touati D. Hypochlorous acid stress in Escherichia coli: resistance, DNA damage, and comparison with hydrogen peroxide stress. J Bacteriol. 1996; 178: 6145-6150. PubMed PMID: 8892812; PubMed Central PMCID: PMC178483.
10. Gray MJ, Wholey WY, Parker BW, Kim M, Jakob U. NemR is a bleach-sensing transcription factor. J Biol Chem. 2013; 288: 13789-13798. doi: M113.454421 [pii];doi: 10.1074/jbc.M113.454421 PMID: 23536188
11. Davies MJ. The oxidative environment and protein damage. Biochim Biophys Acta. 2005; 1703: 93-109. doi: S1570-9639(04)00218-3 [pii];doi: 10.1016/j.bbapap.2004.08.007 PMID: 15680218
12. Imlay JA. Pathways of oxidative damage. Annu Rev Microbiol. 2003; 57: 395-418. doi: 10.1146/annurev.micro.57.030502.090938 PubMed PMID: 14527285.
13. Drazic A, Winter J. The physiological role of reversible methionine oxidation. Biochim Biophys Acta. 2014; 1844: 1367-1382. doi: 10.1016/j.bbapap.2014.01.001 PubMed PMID: 24418392.
14. Wang S, Deng K, Zaremba S, Deng X, Lin C, Wang Q, et al. Transcriptomic response of Escherichia coli O157:H7 to oxidative stress. Appl Environ Microbiol. 2009; 75: 6110-6123. doi: 10.1128/AEM.00914-09 PubMed PMID: 19666735; PubMed Central PMCID: PMC2753066.
15. Leichert LI, Gehrke F, Gudiseva HV, Blackwell T, Ilbert M, Walker AK, et al. Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc Natl Acad Sci U S A. 2008; 105: 8197-8202. doi: 10.1073/pnas.0707723105 PubMed PMID: 18287020; PubMed Central PMCID: PMC2448814.
16. Winter J, Ilbert M, Graf PC, Ozcelik D, Jakob U. Bleach activates a redox-regulated chaperone by oxidative protein unfolding. Cell 2008; 135: 691-701. doi: S0092-8674(08)01181-1 [pii];doi: 10.1016/j.cell.2008.09.024 PMID: 19013278
17. Rosen H, Klebanoff SJ, Wang Y, Brot N, Heinecke JW, Fu X. Methionine oxidation contributes to bacterial killing by the myeloperoxidase system of neutrophils. Proc Natl Acad Sci U S A. 2009; 106: 18686-18691. doi: 0909464106 [pii];doi: 10.1073/pnas.0909464106 PMID: 19833874
18. Drazic A, Miura H, Peschek J, Le Y, Bach NC, Kriehuber T, et al. Methionine oxidation activates a transcription factor in response to oxidative stress. Proc Natl Acad Sci U S A. 2013; 110: 9493-9498. doi: 1300578110 [pii];doi: 10.1073/pnas.1300578110 PMID: 23690622
19. Drazic A, Gebendorfer KM, Mak S, Steiner A, Krause M, Bepperling A, et al. Tetramers are the activation-competent species of the HOCl-specific transcription factor HypT. J Biol Chem. 2014; 289: 977-986. doi: 10.1074/jbc.M113.521401 PubMed PMID: 24275662; PubMed Central PMCID: PMC3887220.
20. Parker BW, Schwessinger EA, Jakob U, Gray MJ. The RclR protein is a reactive chlorine-specific transcription factor in Escherichia coli. J Biol Chem. 2013; 288: 32574-32584. doi: 10.1074/jbc.M113.503516 PubMed PMID: 24078635; PubMed Central PMCID: PMC3820890.
21. Winter J, Linke K, Jatzek A, Jakob U. Severe oxidative stress causes inactivation of DnaK and activation of the redox-regulated chaperone Hsp33. Mol Cell 2005; 17: 381-392. doi: 10.1016/j.molcel.2004.12.027 PubMed PMID: 15694339.
22. Gray MJ, Wholey WY, Jakob U. Bacterial responses to reactive chlorine species. Annu Rev Microbiol. 2013; 67: 141-160. doi: 10.1146/annurev-micro-102912-142520 PMID: 23768204
23. Jozefczuk S, Klie S, Catchpole G, Szymanski J, Cuadros-Inostroza A, Steinhauser D, et al. Metabolomic and transcriptomic stress response of Escherichia coli. Mol Syst Biol. 2010; 6: 364. doi: 10.1038/msb.2010.18 PubMed PMID: 20461071; PubMed Central PMCID: PMC2890322.
24. Schauer N, Steinhauser D, Strelkov S, Schomburg D, Allison G, Moritz T, et al. GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett. 2005; 579: 1332-1337. doi: 10.1016/j.febslet.2005.01.029 PubMed PMID: 15733837.
25. Gebendorfer KM, Drazic A, Le Y, Gundlach J, Bepperling A, Kastenmuller A, et al. Identification of a hypochlorite-specific transcription factor from Escherichia coli. J Biol Chem. 2012; 287: 6892-6903. doi: M111.287219 [pii];doi: 10.1074/jbc.M111.287219 PMID: 22223481
26. Fan TWM. Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog Nucl Magn Reson Spectrosc. 1996; 28: 161-219.
27. Levine RL, Mosoni L, Berlett BS, Stadtman ER. Methionine residues as endogenous antioxidants in proteins. Proc Natl Acad Sci U S A. 1996; 93: 15036-15040. PubMed PMID: 8986759; PubMed Central PMCID: PMC26351.
28. Grosser N, Oberle S, Berndt G, Erdmann K, Hemmerle A, Schroder H. Antioxidant action of L-alanine: heme oxygenase-1 and ferritin as possible mediators. Biochem Biophys Res Commun. 2004; 314: 351-355. PubMed PMID: 14733911.
29. Willetts NS. Intracellular protein breakdown in non-growing cells of Escherichia coli. Biochemical J. 1967; 103: 453-461. PubMed PMID: 5340366; PubMed Central PMCID: PMC1270427.
30. Yuan W, Wang Y, Heinecke JW, Fu X. Hypochlorous acid converts the gamma-glutamyl group of glutathione disulfide to 5-hydroxybutyrolactam, a potential marker for neutrophil activation. J Biol Chem. 2009; 284: 26908-26917. doi: 10.1074/jbc.M109.005496 PubMed PMID: 19584048; PubMed Central PMCID: PMC2785378.
31. Chesney JA, Eaton JW, Mahoney JR Jr. Bacterial glutathione: a sacrificial defense against chlorine compounds. J Bacteriol. 1996; 178: 2131-2135. PubMed PMID: 8606194; PubMed Central PMCID: PMC177915.
32. Kumar A, Bachhawat AK. Pyroglutamic acid: throwing light on a lightly studied metabolite. Curr Sci. 2012; 102: 288-297.
33. Gray MJ, Wholey WY, Wagner NO, Cremers CM, Mueller-Schickert A, Hock NT, et al. Polyphosphate is a primordial chaperone. Mol Cell 2014; 53: 689-699. doi: 10.1016/j.molcel.2014.01.012 PubMed PMID: 24560923.
34. Tkachenko AG, Pshenichnov MR, Nesterova L. Putrescine as a oxidative stress protecting factor in Escherichia coli. Mikrobiologiia 2001; 70: 487-494. PubMed PMID: 11558274.
35. Imlay JA. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol. 2013; 11: 443-454. doi: 10.1038/nrmicro3032 PubMed PMID: 23712352; PubMed Central PMCID: PMC4018742.
36. Mermod M, Magnani D, Solioz M, Stoyanov JV. The copper-inducible ComR (YcfQ) repressor regulates expression of ComC (YcfR), which affects copper permeability of the outer membrane of Escherichia coli. Biometals 2012; 25: 33-43. doi: 10.1007/s10534-011-9510-x PubMed PMID: 22089859.
37. Dukan S, Levi Y, Touati D. Recovery of culturability of an HOCl-stressed population of Escherichia coli after incubation in phosphate buffer: resuscitation or regrowth? Appl Environ Microbiol. 1997; 63: 4204-4209. PubMed PMID: 9361405; PubMed Central PMCID: PMC168738.
38. Deng K, Wang S, Rui X, Zhang W, Tortorello ML. Functional analysis of ycfR and ycfQ in Escherichia coli O157:H7 linked to outbreaks of illness associated with fresh produce. Appl Environ Microbiol. 2011; 77: 3952-3959. doi: 10.1128/AEM.02420-10 PubMed PMID: 21498759; PubMed Central PMCID: PMC3131662.
39. Shen T, Rui B, Zhou H, Zhang X, Yi Y, Wen H, et al. Metabolic flux ratio analysis and multi-objective optimization revealed a globally conserved and coordinated metabolic response of E. coli to paraquat-induced oxidative stress. Mol Biosyst. 2013; 9: 121-132. doi: 10.1039/c2mb25285f PubMed PMID: 23128557.
40. Rui B, Shen T, Zhou H, Liu J, Chen J, Pan X, et al. A systematic investigation of Escherichia coli central carbon metabolism in response to superoxide stress. BMC Syst Biol. 2010; 4: 122. doi: 10.1186/1752-0509-4-122 PubMed PMID: 20809933; PubMed Central PMCID: PMC2944137.
41. Valdivia-Gonzalez M, Perez-Donoso JM, Vasquez CC. Effect of tellurite-mediated oxidative stress on the Escherichia coli glycolytic pathway. Biometals 2012; 25: 451-458. doi: 10.1007/s10534-012-9518-x PubMed PMID: 22234496.
42. Ralser M, Wamelink MM, Kowald A, Gerisch B, Heeren G, Struys EA, et al. Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J Biol. 2007; 6: 10. doi: 10.1186/jbiol61 PubMed PMID: 18154684; PubMed Central PMCID: PMC2373902.
43. Antelmann H, Williams RC, Miethke M, Wipat A, Albrecht D, Harwood CR, et al. The extracellular and cytoplasmic proteomes of the non-virulent Bacillus anthracis strain UM23C1-2. Proteomics 2005; 5: 3684-3695. doi: 10.1002/pmic.200401218 PubMed PMID: 16121336.
44. Hazen SL, d'Avignon A, Anderson MM, Hsu FF, Heinecke JW. Human neutrophils employ the myeloperoxidase-hydrogen peroxide-chloride system to oxidize alpha-amino acids to a family of reactive aldehydes. Mechanistic studies identifying labile intermediates along the reaction pathway. J Biol Chem. 1998; 273: 4997-5005. PubMed PMID: 9478947.
45. van den Berg J, Winterbourn C. Measurement of reaction products from hypochlorous acid and unsaturated lipids. Methods Enzymol. 1994; 233: 639-649. PubMed PMID: 8015496.
46. Vissers MC, Stern A, Kuypers F, van den Berg J, Winterbourn CC. Membrane changes associated with lysis of red blood cells by hypochlorous acid. Free Radic Biol Med. 1994; 16: 703-712. PubMed PMID: 8070673.
47. Morales EH, Calderon IL, Collao B, Gil F, Porwollik S, McClelland M, et al. Hypochlorous acid and hydrogen peroxide-induced negative regulation of Salmonella enterica serovar Typhimurium ompW by the response regulator ArcA. BMC Microbiol. 2012; 12: 63. doi: 10.1186/1471-2180-12-63 PubMed PMID: 22545862; PubMed Central PMCID: PMC3358236.
48. Kirkpatrick C, Maurer LM, Oyelakin NE, Yoncheva YN, Maurer R, Slonczewski JL. Acetate and formate stress: opposite responses in the proteome of Escherichia coli. J Bacteriol. 2001; 183: 6466-6477. doi: 10.1128/JB.183.21.6466-6477.2001 PubMed PMID: 11591692; PubMed Central PMCID: PMC100143.
49. Leonhartsberger S, Korsa I, Bock A. The molecular biology of formate metabolism in enterobacteria. J Mol Microbiol Biotechnol. 2002; 4: 269-276. PubMed PMID: 11931558.
50. Chang DE, Smalley DJ, Conway T. Gene expression profiling of Escherichia coli growth transitions: an expanded stringent response model. Mol Microbiol. 2002; 45: 289-306. PubMed PMID: 12123445.