Tea polyphenol epigallocatechin gallate inhibits Escherichia coli by increasing endogenous oxidative stress

Food Chemistry

Volumn 217, Issue , 2017, Pages 196-204

  Xiong, Li Gui ^a   Chen, Yi Jun ^a   Tong, Jie Wen ^a   Huang, Jian An ^a   Li, Juan ^a   Gong, Yu Shun ^a   Liu, Zhong Hua ^a  

^a HUNAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Adaptive response; Antibacterial; Epigallocatechin gallate; Escherichia coli; Reactive oxygen species

Indexed keywords

OXIDATIVE STRESS;

ADAPTIVE RESPONSE; ANAEROBIC CONDITIONS; ANTIBACTERIAL; ANTIBACTERIAL EFFECTS; BACTERICIDAL EFFECTS; EPIGALLOCATECHIN GALLATE; OXIDATIVE STRESS RESPONSE; REACTIVE OXYGEN SPECIES;

ESCHERICHIA COLI;

ACETYLCYSTEINE; DPS PROTEIN; EPIGALLOCATECHIN GALLATE; HYDROGEN PEROXIDE; KATG PROTEIN; PARAQUAT; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; ANTIOXIDANT; CATALASE; CATECHIN; POLYPHENOL; TEA;

AHPC GENE; AHPF GENE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERICIDAL ACTIVITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; DRUG POTENTIATION; ESCHERICHIA COLI; GENETIC TRANSCRIPTION; GOR GENE; NONHUMAN; OXIDATIVE STRESS; OXYR GENE; OXYS GENE; REGULON; SODA GENE; SOXR GENE; SOXS GENE; TEA; UPREGULATION; ANALOGS AND DERIVATIVES; CHEMISTRY; DRUG EFFECTS; METABOLISM;

ACETYLCYSTEINE; ANTIOXIDANTS; CATALASE; CATECHIN; ESCHERICHIA COLI; HYDROGEN PEROXIDE; OXIDATIVE STRESS; POLYPHENOLS; REACTIVE OXYGEN SPECIES; TEA;

EID: 84984664345     PISSN: 03088146     EISSN: 18737072     Source Type: Journal    
DOI: 10.1016/j.foodchem.2016.08.098     Document Type: Article

References (38)

1. Akagawa, M., Shigemitsu, T., Suyama, K., Production of hydrogen peroxide by polyphenols and polyphenol-rich beverages under quasi-physiological conditions. Bioscience, Biotechnology, and Biochemistry 67:12 (2003), 2632–2640.
2. Arakawa, H., Maeda, M., Okubo, S., Shimamura, T., Role of hydrogen peroxide in bactericidal action of catechin. Biological and Pharmaceutical Bulletin 27:3 (2004), 277–281.
3. Birringer, M., Hormetics: Dietary triggers of an adaptive stress response. Pharmaceutical Research 28:11 (2011), 2680–2694.
4. Bury, D., Jelen, P., Kalab, M., Disruption of Lactobacillus delbrueckii ssp. bulgaricus 11842 cells for lactose hydrolysis in dairy products: A comparison of sonication, high-pressure homogenization and bead milling. Innovative Food Science & Emerging Technologies 2:1 (2001), 23–29.
5. Chadwick, W., Maudsley, S., Hormesis: A revolution in biology, toxicology and medicine. 2010, Springer Science, New York.
6. Cui, Y., Oh, Y., Lim, J., Youn, M., Lee, I., Pak, H.,. Park, S., AFM study of the differential inhibitory effects of the green tea polyphenol (−)-epigallocatechin-3-gallate (EGCG) against Gram-positive and Gram-negative bacteria. Food Microbiology 29:1 (2012), 80–87.
7. Dwyer, D.J., Belenky, P.A., Yang, J.H., MacDonald, I.C., Martell, J.D., Takahashi, N.,. Schwarz, E.G., Antibiotics induce redox-related physiological alterations as part of their lethality. Proceedings of the National Academy of Sciences 111:20 (2014), E2100–E2109.
8. Elbling, L., Herbacek, I., Weiss, R.-M., Jantschitsch, C., Micksche, M., Gerner, C.,. Berger, W., Hydrogen peroxide mediates EGCG-induced antioxidant protection in human keratinocytes. Free Radical Biology and Medicine 49:9 (2010), 1444–1452.
9. Goswami, M., Jawali, N., N-Acetylcysteine-mediated modulation of bacterial antibiotic susceptibility. Antimicrobial Agents and Chemotherapy 54:8 (2010), 3529–3530.
10. Goswami, M., Mangoli, S., Jawali, N., Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli. Antimicrobial Agents and Chemotherapy 50:3 (2006), 949–954.
11. Hong, J., Lu, H., Meng, X., Ryu, J.-H., Hara, Y., Yang, C.S., Stability, cellular uptake, biotransformation, and efflux of tea polyphenol (−)-epigallocatechin-3-gallate in HT-29 human colon adenocarcinoma cells. Cancer Research 62:24 (2002), 7241–7246.
12. Imlay, J.A., The molecular mechanisms and physiological consequences of oxidative stress: Lessons from a model bacterium. Nature Reviews Microbiology 11:7 (2013), 443–454.
13. Isbrucker, R., Bausch, J., Edwards, J., Wolz, E., Safety studies on epigallocatechin gallate (EGCG) preparations. Part 1: Genotoxicity. Food and Chemical Toxicology 44:5 (2006), 626–635.
14. Kim, H.-S., Quon, M.J., Kim, J.-a., New insights into the mechanisms of polyphenols beyond antioxidant properties; Lessons from the green tea polyphenol, epigallocatechin 3-gallate. Redox Biology 2 (2014), 187–195.
15. Kohanski, M.A., Dwyer, D.J., Hayete, B., Lawrence, C.A., Collins, J.J., A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:5 (2007), 797–810.
16. Korshunov, S.S., Imlay, J.A., A potential role for periplasmic superoxide dismutase in blocking the penetration of external superoxide into the cytosol of Gram-negative bacteria. Molecular Microbiology 43:1 (2002), 95–106.
17. Lambert, J.D., Elias, R.J., The antioxidant and pro-oxidant activities of green tea polyphenols: A role in cancer prevention. Archives of Biochemistry and Biophysics 501:1 (2010), 65–72.
18. Liu, Y., Imlay, J.A., Cell death from antibiotics without the involvement of reactive oxygen species. Science 339:6124 (2013), 1210–1213.
19. Liu, X., Li, J., Wang, Y., Li, T., Zhao, J., Zhang, C., Green tea polyphenols function as prooxidants to inhibit Pseudomonas aeruginosa and induce the expression of oxidative stress-related genes. Folia Microbiologica 58:3 (2013), 211–217.
20. Lobritz, M.A., Belenky, P., Porter, C.B., Gutierrez, A., Yang, J.H., Schwarz, E.G.,. Collins, J.J., Antibiotic efficacy is linked to bacterial cellular respiration. Proceedings of the National Academy of Sciences 112:27 (2015), 8173–8180.
21. Long, L.H., Clement, M.V., Halliwell, B., Artifacts in cell culture: Rapid generation of hydrogen peroxide on addition of (−)-epigallocatechin, (−)-epigallocatechin gallate, (+)-catechin, and quercetin to commonly used cell culture media. Biochemical and Biophysical Research Communications 273:1 (2000), 50–53.
22. Long, L.H., Halliwell, B., Artefacts in cell culture: Pyruvate as a scavenger of hydrogen peroxide generated by ascorbate or epigallocatechin gallate in cell culture media. Biochemical and Biophysical Research Communications 388:4 (2009), 700–704.
23. Long, L.H., Kirkland, D., Whitwell, J., Halliwell, B., Different cytotoxic and clastogenic effects of epigallocatechin gallate in various cell-culture media due to variable rates of its oxidation in the culture medium. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 634:1 (2007), 177–183.
24. Matthijssens, F., Back, P., Braeckman, B.P., Vanfleteren, J.R., Prooxidant activity of the superoxide dismutase (SOD)-mimetic EUK-8 in proliferating and growth-arrested Escherichia coli cells. Free Radical Biology and Medicine 45:5 (2008), 708–715.
25. Mochizuki, M., Yamazaki, S.-i., Kano, K., Ikeda, T., Kinetic analysis and mechanistic aspects of autoxidation of catechins. Biochimica et Biophysica Acta (BBA) – General Subjects 1569:1 (2002), 35–44.
26. Nakayama, M., Shigemune, N., Tsugukuni, T., Tokuda, H., Miyamoto, T., Difference of EGCg adhesion on cell surface between Staphylococcus aureus and Escherichia coli visualized by electron microscopy after novel indirect staining with cerium chloride. Journal of Microbiological Methods 86:1 (2011), 97–103.
27. Navarro-Martínez, M.D., Navarro-Perán, E., Cabezas-Herrera, J., Ruiz-Gómez, J., García-Cánovas, F., Rodríguez-López, J.N., Antifolate activity of epigallocatechin gallate against Stenotrophomonas maltophilia. Antimicrobial Agents and Chemotherapy 49:7 (2005), 2914–2920.
28. Reygaert, W.C., The antimicrobial possibilities of green tea. Frontiers in Microbiology, 5, 2014.
29. Sang, S., Hou, Z., Lambert, J.D., Yang, C.S., Redox properties of tea polyphenols and related biological activities. Antioxidants & Redox Signaling 7:11–12 (2005), 1704–1714.
30. Seaver, L.C., Imlay, J.A., Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. Journal of Bacteriology 183:24 (2001), 7182–7189.
31. Si, W., Gong, J., Tsao, R., Kalab, M., Yang, R., Yin, Y., Bioassay-guided purification and identification of antimicrobial components in Chinese green tea extract. Journal of Chromatography A 1125:2 (2006), 204–210.
32. Singh, B.N., Shankar, S., Srivastava, R.K., Green tea catechin, epigallocatechin-3-gallate (EGCG): Mechanisms, perspectives and clinical applications. Biochemical Pharmacology 82:12 (2011), 1807–1821.
33. Steinmann, J., Buer, J., Pietschmann, T., Steinmann, E., Anti-infective properties of epigallocatechin-3-gallate (EGCG), a component of green tea. British Journal of Pharmacology 168:5 (2013), 1059–1073.
34. Tao, L., Forester, S.C., Lambert, J.D., The role of the mitochondrial oxidative stress in the cytotoxic effects of the green tea catechin, (−)-epigallocatechin-3-gallate, in oral cells. Molecular Nutrition & Food Research 58:4 (2014), 665–676.
35. Umezawa, N., Arakane, K., Ryu, A., Mashiko, S., Hirobe, M., Nagano, T., Participation of reactive oxygen species in phototoxicity induced by quinolone antibacterial agents. Archives of Biochemistry and Biophysics 342:2 (1997), 275–281.
36. Wang, J.-H., Singh, R., Benoit, M., Keyhan, M., Sylvester, M., Hsieh, M.,. Matin, A., Sigma S-dependent antioxidant defense protects stationary-phase Escherichia coli against the bactericidal antibiotic gentamicin. Antimicrobial Agents and Chemotherapy 58:10 (2014), 5964–5975.
37. Yang, C.S., Wang, X., Lu, G., Picinich, S.C., Cancer prevention by tea: Animal studies, molecular mechanisms and human relevance. Nature Reviews Cancer 9:6 (2009), 429–439.
38. Zhang, Y.-M., Rock, C.O., Evaluation of epigallocatechin gallate and related plant polyphenols as inhibitors of the FabG and FabI reductases of bacterial type II fatty-acid synthase. Journal of Biological Chemistry 279:30 (2004), 30994–31001.