Anti-genotoxic or anti-mutagenic activity has been described for a number of Gram-positive probiotic bacterial species. Here we present evidence that Gram-negative Escherichia coli Nissle 1917 (EcN) also displays anti-genotoxic/anti-mutagenic activity, as assessed in vitro by the Comet Assay and the Ames Test, respectively. This activity was demonstrated by use of the mutagens 4-nitroquinoline-1-oxide (NQO), hydrogen peroxide (H2O2) and benzo(a) pyrene (B[a]P). For both assays and all three test agents the anti-genotoxic/anti-mutagenic activity of EcN was shown to be concentration dependent. By the use of extracts of bacteria that were inactivated by various procedures (heat treatment, ultrasound sonication or ultraviolet light irradiation), mechanistic explanations could be put forward. The proposed mechanisms were enforced by treating the bacterial material with proteinase K prior to testing. The mutagen H2O2 is most likely inactivated by enzymic activity, with catalase a likely candidate, while several explanations can be put forward for inactivation of B[a]P. NQO is most likely inactivated by metabolising enzymes, since the formation of the metabolite 4-aminoquinoline could be demonstrated. In conclusion, the in vitro results presented here make a strong case for antimutagenic properties of EcN.
Ames, B.N., Mccann, J. and Yamasaki, E., 1975. Methods for detecting carcinogens and mutagens with the Salmonella/mammalian-microsome mutagenicity test. Mutation Research 31: 347-364.
'Methods for detecting carcinogens and mutagens with the Salmonella/mammalian-microsome mutagenicity test ' () 31 Mutation Research : 347 -364.
Anderson, D., Yu, T.W., Phillips, B.J. and Schmezer, P., 1994. The effect of various antioxidants and other modifying agents on oxygen-radical-generated DNA damage in human lymphocytes in the COMET assay. Mutation Research 307: 261-271.
'The effect of various antioxidants and other modifying agents on oxygen-radical-generated DNA damage in human lymphocytes in the COMET assay ' () 307 Mutation Research : 261 -271.
Bang, S.Y., Kim, J.H., Lee, P.Y., Bae, K.H., Lee, J.S., Kim, P.S., Lee, D.H., Myung, P.K., Park, B.C. and Park, S.G., 2012. Confirmation of Frm2 as a novel nitroreductase in Saccharomyces cerevisiae. Biochemical and Biophysical Research Communications 423: 638-641.
'Confirmation of Frm2 as a novel nitroreductase in Saccharomyces cerevisiae ' () 423 Biochemical and Biophysical Research Communications : 638 -641.
Benson, A.M., 1993. Conversion of 4-nitroquinoline 1-oxide (4NQO) to 4-hydroxyaminoquinoline 1-oxide by a dicumarol-resistant hepatic 4NQO nitroreductase in rats and mice. Biochemical Pharmacology 46: 1217-1221.
'Conversion of 4-nitroquinoline 1-oxide (4NQO) to 4-hydroxyaminoquinoline 1-oxide by a dicumarol-resistant hepatic 4NQO nitroreductase in rats and mice ' () 46 Biochemical Pharmacology : 1217 -1221.
Bernardes, N., Chakrabarty, A.M. and Fialho, A.M., 2013. Engineering of bacterial strains and their products for cancer therapy. Applied Microbiology and Biotechnology 97: 5189-5199.
'Engineering of bacterial strains and their products for cancer therapy ' () 97 Applied Microbiology and Biotechnology : 5189 -5199.
Boonchan, S., Britz, M.L. and Stanley, G.A., 1998. Surfactant-enhanced biodegradation of high molecular weight polycyclic aromatic hydrocarbons by Stenotrophomonas maltophilia. Biotechnology and Bioengineering 59: 482-494.
'Surfactant-enhanced biodegradation of high molecular weight polycyclic aromatic hydrocarbons by Stenotrophomonas maltophilia ' () 59 Biotechnology and Bioengineering : 482 -494.
Caldini, G., Trotta, F., Corsetti, A. and Cenci, G., 2008. Evidence for in vitro anti-genotoxicity of cheese non-starter lactobacilli. Antonie Van Leeuwenhoek 93: 51-59.
'Evidence for in vitro anti-genotoxicity of cheese non-starter lactobacilli ' () 93 Antonie Van Leeuwenhoek : 51 -59.
Caldini, G., Trotta, F., Villarini, M., Moretti, M., Pasquini, R., Scassellati-Sforzolini, G. and Cenci, G., 2005. Screening of potential lactobacilli antigenotoxicity by microbial and mammalian cell-based tests. International Journal of Food Microbiology 102: 37-47.
'Screening of potential lactobacilli antigenotoxicity by microbial and mammalian cell-based tests ' () 102 International Journal of Food Microbiology : 37 -47.
Cheng, L., Kellogg 3rd, E.W. and Packer, L., 1981. Photoinactivation of catalase. Photochemistry and Photobiology 34: 125-129.
'Photoinactivation of catalase ' () 34 Photochemistry and Photobiology : 125 -129.
Fahey, R.C., Brown, W.C., Adams, W.B. and Worsham, M.B., 1978. Occurrence of glutathione in bacteria. Journal of Bacteriology 133: 1126-1129.
'Occurrence of glutathione in bacteria ' () 133 Journal of Bacteriology : 1126 -1129.
Ferguson, G.P. and Booth, I.R., 1998. Importance of glutathione for growth and survival of Escherichia coli cells: detoxification of methylglyoxal and maintenance of intracellular K+. Journal of Bacteriology 180: 4314-4318.
'Importance of glutathione for growth and survival of Escherichia coli cells: detoxification of methylglyoxal and maintenance of intracellular K+ ' () 180 Journal of Bacteriology : 4314 -4318.
Ferrante, M., Zanghì, G., Cristaldi, A., Copat, C., Grasso, A., Fiore, M., Signorelli, S.S., Zuccarello, P. and Oliveri Conti, G., 2018. PAHs in seafood from the mediterranean sea: an exposure risk assessment. Food and Chemical Toxicology 115: 385-390.
'PAHs in seafood from the mediterranean sea: an exposure risk assessment ' () 115 Food and Chemical Toxicology : 385 -390.
Goodson 3rd, W.H., Lowe, L., Carpenter, D.O., Gilbertson, M., Manaf Ali, A., Lopez de Cerain Salsamendi, A., Lasfar, A., Carnero, A., Azqueta, A., Amedei, A., Charles, A.K., Collins, A.R., Ward, A., Salzberg, A.C., Colacci, A., Olsen, A.-K., Berg, A., Barclay, B.J., Zhou, B.P., Blanco-Aparicio, C., Baglole, C.J., Dong, C., Mondello, C., Hsu, C.-W., Naus, C.C., Yedjou, C., Curran, C.S., Laird, D.W., Koch, D.C., Carlin, D.J., Felsher, D.W., Roy, D., Brown, D.G., Ratovitski, E., Ryan, E.P., Corsini, E., Rojas, E., Moon, E.-Y., Laconi, E., Marongiu, F., Al-Mulla, F., Chiaradonna, F., Darroudi, F., Martin, F.L., Van Schooten, F.J., Goldberg, G.S., Wagemaker, G., Nangami, G.N., Calaf, G.M., Williams, G., Wolf, G.T., Koppen, G., Brunborg, G., Lyerly, H.K., Krishnan, H., Ab Hamid, H., Yasaei, H., Sone, H., Kondoh, H., Salem, H.K., Hsu, H.-Y., Park, H.H., Koturbash, I., Miousse, I.R., Scovassi, A.I., Klaunig, J.E., Vondráček, J., Raju, J., Roman, J., Wise, J.P., Sr., Whitfield, J.R., Woodrick, J., Christopher, J.A., Ochieng, J., Martinez-Leal, J.F., Weisz, J., Kravchenko, J., Sun, J., Prudhomme, K.R., Narayanan, K.B., Cohen-Solal, K.A., Moorwood, K., Gonzalez, L., Soucek, L., Jian, L., D’Abronzo, L.S., Lin, L.-T., Li, L., Gulliver, L., McCawley, L.J., Memeo, L., Vermeulen, L., Leyns, L., Zhang, L., Valverde, M., Khatami, M., Romano, M.F., Chapellier, M., Williams, M.A., Wade, M., Manjili, M.H., Lleonart, M.E., Xia, M., Gonzalez, M.J., Karamouzis, M.V., Kirsch-Volders, M., Vaccari, M., Kuemmerle, N.B., Singh, N., Cruickshanks, N., Kleinstreuer, N., van Larebeke, N., Ahmed, N., Ogunkua, O., Krishnakumar, P.K., Vadgama, P., Marignani, P.A., Ghosh, P.M., Ostrosky-Wegman, P., Thompson, P.A., Dent, P., Heneberg, P., Darbre, P., Sing Leung, P., Nangia-Makker, P., Cheng, Q.S., Robey, R.B., Al-Temaimi, R., Roy, R., Andrade-Vieira, R., Sinha, R.K., Mehta, R., Vento, R., Di Fiore, R., Ponce-Cusi, R., Dornetshuber-Fleiss, R., Nahta, R., Castellino, R.C., Palorini, R., Abd Hamid, R., Langie, S.A.S., Eltom, S.E., Brooks, S.A., Ryeom, S., Wise, S.S., Bay, S.N., Harris, S.A., Papagerakis, S., Romano, S., Pavanello, S., Eriksson, S., Forte, S., Casey, S.C., Luanpitpong, S., Lee, T.-J., Otsuki, T., Chen, T., Massfelder, T., Sanderson, T., Guarnieri, T., Hultman, T., Dormoy, V., Odero-Marah, V., Sabbisetti, V., Maguer-Satta, V., Rathmell, W.K., Engström, W., Decker, W.K., Bisson, W.H., Rojanasakul, Y., Luqmani, Y., Chen, Z. and Hu, Z., 2015. Assessing the carcinogenic potential of low-dose exposures to chemical mixtures in the environment: the challenge ahead. Carcinogenesis 36, Suppl. 1: S254-S296. Erratum in: Carcinogenesis 2016. 37: 344.
'Assessing the carcinogenic potential of low-dose exposures to chemical mixtures in the environment: the challenge ahead ' () 36 Carcinogenesis : S254 -S296.
Hartmann, A., Agurell, E., Beevers, C., Brendler-Schwaab, S., Burlinson, B., Clay P., Collins A., Smith, A., Speit, G., Thybaud, V. and Tice, R.R., 2003. 4th International Comet Assay Workshop. Recommendations for conducting the in vivo alkaline Comet assay. Mutagenesis 18: 45-51.
'4th International Comet Assay Workshop ' () 18 Mutagenesis : 45 -51.
Jakobsen, L.S., Georgiadis, S., Nielsen, B.F., Bokkers, B.G.H., Boriani, E., Duedahl-Olesen, L., Hald, T., Nauta, M.J., Stockmarr, A. and Pires, S.M., 2018. Probabilistic approach for assessing cancer risk due to benzo(a)pyrene in barbecued meat: informing advice for population groups. PLoS ONE 13: e0207032.
'Probabilistic approach for assessing cancer risk due to benzo(a)pyrene in barbecued meat: informing advice for population groups ' () 13 PLoS ONE : e0207032.
Jouanneau, Y., Meyer, C. and Duraffourg, N., 2015. Dihydroxylation of four- and five-ring aromatic hydrocarbons by the naphthalene dioxygenase from Sphingomonas CHY-1. Applied Microbiology and Biotechnology 100: 1253-1263.
'Dihydroxylation of four- and five-ring aromatic hydrocarbons by the naphthalene dioxygenase from Sphingomonas CHY-1 ' () 100 Applied Microbiology and Biotechnology : 1253 -1263.
Kaplan, J.G. and Paik, W.K., 1956. The action of ultraviolet radiation on yeast catalase. Journal of General Physiology 40: 147-169.
'The action of ultraviolet radiation on yeast catalase ' () 40 Journal of General Physiology : 147 -169.
Karpiński, T.M. and Adamczak, A., 2018. Anticancer activity of bacterial proteins and peptides. Pharmaceutics 10: E54.
'Anticancer activity of bacterial proteins and peptides ' () 10 Pharmaceutics : E54.
Kinouchi, T. and Ohnishi, Y., 1983. Purification and characterization of 1-nitropyrene nitroreductases from Bacteroides fragilis. Applied and Environmental Microbiology 46: 596-604.
'Purification and characterization of 1-nitropyrene nitroreductases from Bacteroides fragilis ' () 46 Applied and Environmental Microbiology : 596 -604.
Maron, D.M. and Ames, B.N., 1983. Revised methods for the Salmonella mutagenicity test. Mutation Research 113: 173-215.
'Revised methods for the Salmonella mutagenicity test ' () 113 Mutation Research : 173 -215.
O’Neill, P.M., Bray, P.G., Hawley, S.R., Ward, S.A. and Park, B.K., 1998. 4-Aminoquinolines – past, present, and future: a chemical perspective. Pharmacology and Therapeutics 77: 29-58.
'4-Aminoquinolines – past, present, and future: a chemical perspective ' () 77 Pharmacology and Therapeutics : 29 -58.
Owens, R.A. and Hartman, P.E., 1986. Export of glutathione by some widely used Salmonella typhimurium and Escherichia coli strains. Journal of Bacteriology 168: 109-114.
'Export of glutathione by some widely used Salmonella typhimurium and Escherichia coli strains ' () 168 Journal of Bacteriology : 109 -114.
Peklak-Scott, C., Townsend, A.J. and Morrow, C.S., 2005. Dynamics of glutathione conjugation and conjugate efflux in detoxification of the carcinogen, 4-nitroquinoline 1-oxide: contributions of glutathione, glutathione S-transferase, and MRP1. Biochemistry 44: 4426-4433.
'Dynamics of glutathione conjugation and conjugate efflux in detoxification of the carcinogen, 4-nitroquinoline 1-oxide: contributions of glutathione, glutathione S-transferase, and MRP1 ' () 44 Biochemistry : 4426 -4433.
PubChem, undated. 4-Aminoquinoline. National Institute of Health, Bethesda, MD, USA. Available at: https://tinyurl.com/y62tuz57.
Raman, M., Ambalam, P., Kondepudi, K.K., Pithva, S., Kothari, C., Patel, A.T., Purama, R.K., Dave, J.M. and Vyas, B.R., 2013. Potential of probiotics, prebiotics and synbiotics for management of colorectal cancer. Gut Microbes 4: 181-192.
'Potential of probiotics, prebiotics and synbiotics for management of colorectal cancer ' () 4 Gut Microbes : 181 -192.
Reister, M., Hoffmeier, K., Krezdorn, N., Rotter, B., Liang, C., Rund, S., Dandekar, T., Sonnenborn, U. and Oelschlaeger, T.A., 2014. Complete genome sequence of the gram-negative probiotic Escherichia coli strain Nissle 1917. Journal of Biotechnology 187: 106-107.
'Complete genome sequence of the gram-negative probiotic Escherichia coli strain Nissle 1917 ' () 187 Journal of Biotechnology : 106 -107.
Rentz, J.A., Alvarez, P.J. and Schnoor, J.L., 2008. Benzo(a)pyrene degradation by Sphingomonas yanoikuyae JAR02. Environmental Pollution 151: 669-677.
'Benzo(a)pyrene degradation by Sphingomonas yanoikuyae JAR02 ' () 151 Environmental Pollution : 669 -677.
Sah, B.N., Vasiljevic, T., McKechnie, S. and Donkor, O.N., 2014. Effect of probiotics on antioxidant and antimutagenic activities of crude peptide extract from yogurt. Food Chemistry 156: 264-270.
'Effect of probiotics on antioxidant and antimutagenic activities of crude peptide extract from yogurt ' () 156 Food Chemistry : 264 -270.
Seo, J.S., Keum, Y.S. and Li, Q.X., 2009. Bacterial degradation of aromatic compounds. International Journal of Environmental Research and Public Health 6: 278-309.
'Bacterial degradation of aromatic compounds ' () 6 International Journal of Environmental Research and Public Health : 278 -309.
Smirnova, G., Muzyka, N. and Oktyabrsky, O., 2012. Transmembrane glutathione cycling in growing Escherichia coli cells. Microbiology Research 167: 166-172.
'Transmembrane glutathione cycling in growing Escherichia coli cells ' () 167 Microbiology Research : 166 -172.
Song, S., Vuai, M.S. and Zhong, M., 2018. The role of bacteria in cancer therapy – enemies in the past, but allies at present. Infectious Agents and Cancer 13: 9.
'The role of bacteria in cancer therapy – enemies in the past, but allies at present ' () 13 Infectious Agents and Cancer : 9.
Sonnenborn, U. and Schulze, J., 2009. The non-pathogenic Escherichia coli strain Nissle 1917 – features of a versatile probiotic. Microbial Ecology in Health and Disease 21: 122-158.
'The non-pathogenic Escherichia coli strain Nissle 1917 – features of a versatile probiotic ' () 21 Microbial Ecology in Health and Disease : 122 -158.
Sooch, B.S., Kauldhar, B.S. and Puri, M., 2014. Recent insights into microbial catalases: isolation, production and purification. Biotechnology Advances 32: 1429-1447.
'Recent insights into microbial catalases: isolation, production and purification ' () 32 Biotechnology Advances : 1429 -1447.
Speit, G. and Hartmann, A., 2005. The comet assay: a sensitive genotoxicity test for the detection of DNA damage. Methods in Molecular Biology 291: 85-95.
'The comet assay: a sensitive genotoxicity test for the detection of DNA damage ' () 291 Methods in Molecular Biology : 85 -95.
Stritzker, J., Weibel, S., Seubert, C., Götz, A., Tresch, A., Van Rooijen, N., Oelschlaeger, T.A., Hill, P.J., Gentschev, I. and Szalay, A.A., 2010. Enterobacterial tumor colonization in mice depends on bacterial metabolism and macrophages but is independent of chemotaxis and motility. International Journal of Medical Microbiology 300: 449-456.
'Enterobacterial tumor colonization in mice depends on bacterial metabolism and macrophages but is independent of chemotaxis and motility ' () 300 International Journal of Medical Microbiology : 449 -456.
Switala, J. and Loewen, P.C., 2002. Diversity of properties among catalases. Archives of Biochemistry and Biophysics 401: 145-154.
'Diversity of properties among catalases ' () 401 Archives of Biochemistry and Biophysics : 145 -154.
Wassenaar, T.M., 2016. Insights from 100 years of studying probiotic E. coli. European Journal of Microbiology and Immunology 6: 147-161.
'Insights from 100 years of studying probiotic E. coli ' () 6 European Journal of Microbiology and Immunology : 147 -161.
Waters, M.D., Brady, A.L., Stack, H.F. and Brockman, H.E., 1990. Antimutagenicity profiles for some model compounds. Mutation Research 238: 57-85.
'Antimutagenicity profiles for some model compounds ' () 238 Mutation Research : 57 -85.
Welinder, K.G., 1991. Bacterial catalase-peroxidases are gene duplicated members of the plant peroxidase superfamily. Biochimica et Biophysica Acta 1080: 215-220.
'Bacterial catalase-peroxidases are gene duplicated members of the plant peroxidase superfamily ' () 1080 Biochimica et Biophysica Acta : 215 -220.
Zeng, J., Lin, X., Zhang, J., Li, X. and Wong, M.H., 2011. Oxidation of polycyclic aromatic hydrocarbons by the bacterial laccase CueO from E. coli. Applied Microbiology and Biotechnology 89: 1841-1849.
'Oxidation of polycyclic aromatic hydrocarbons by the bacterial laccase CueO from E. coli ' () 89 Applied Microbiology and Biotechnology : 1841 -1849.
Zeng, J., Zhu, Q., Wu, Y., Chen, H. and Lin, X., 2017. Characterization of a polycyclic aromatic ring-hydroxylation dioxygenase from Mycobacterium sp. NJS-P. Chemosphere 185: 67-74.
'Characterization of a polycyclic aromatic ring-hydroxylation dioxygenase from Mycobacterium sp ' () 185 Chemosphere : 67 -74.
Zhang, M., Wang, F., Jiang, L., Liu, R., Zhang, L., Lei, X., Li, J., Jiang, J., Guo, H., Fang, B., Zhao, L. and Ren, F., 2013. Lactobacillus salivarius REN inhibits rat oral cancer induced by 4-nitroquioline 1-oxide. Cancer Prevention Research 6: 686-694.
'Lactobacillus salivarius REN inhibits rat oral cancer induced by 4-nitroquioline 1-oxide ' () 6 Cancer Prevention Research : 686 -694.
Zhang, Y., Zhang, Y., Xia, L., Zhang, X., Ding, X., Yan, F. and Wu, F., 2012. Escherichia coli Nissle 1917 targets and restrains mouse B16 melanoma and 4T1 breast tumors through expression of azurin protein. Applied and Environmental Microbiology 78: 7603-7610.
'Escherichia coli Nissle 1917 targets and restrains mouse B16 melanoma and 4T1 breast tumors through expression of azurin protein ' () 78 Applied and Environmental Microbiology : 7603 -7610.
Zolotukhin, P.V., Prazdnova, E.V. and Chistyakov, V.A., 2018. Methods to assess the antioxidative properties of probiotics. Probiotics and Antimicrobial Proteins 10: 589-599.
'Methods to assess the antioxidative properties of probiotics ' () 10 Probiotics and Antimicrobial Proteins : 589 -599.
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Anti-genotoxic or anti-mutagenic activity has been described for a number of Gram-positive probiotic bacterial species. Here we present evidence that Gram-negative Escherichia coli Nissle 1917 (EcN) also displays anti-genotoxic/anti-mutagenic activity, as assessed in vitro by the Comet Assay and the Ames Test, respectively. This activity was demonstrated by use of the mutagens 4-nitroquinoline-1-oxide (NQO), hydrogen peroxide (H2O2) and benzo(a) pyrene (B[a]P). For both assays and all three test agents the anti-genotoxic/anti-mutagenic activity of EcN was shown to be concentration dependent. By the use of extracts of bacteria that were inactivated by various procedures (heat treatment, ultrasound sonication or ultraviolet light irradiation), mechanistic explanations could be put forward. The proposed mechanisms were enforced by treating the bacterial material with proteinase K prior to testing. The mutagen H2O2 is most likely inactivated by enzymic activity, with catalase a likely candidate, while several explanations can be put forward for inactivation of B[a]P. NQO is most likely inactivated by metabolising enzymes, since the formation of the metabolite 4-aminoquinoline could be demonstrated. In conclusion, the in vitro results presented here make a strong case for antimutagenic properties of EcN.
| All Time | Past 365 days | Past 30 Days | |
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