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Abstract:

Shiga toxin-producing Escherichia coli (STEC) are important food-borne pathogens, with the main virulence factor of this bacterium being its capacity to secrete Shiga toxins (Stxs). Therefore, the use of certain antibiotics for the treatment of this infection, which induces the liberation of Stxs, is controversial. Reactive oxygen and nitrogen species are also involved in the pathogenesis of different diseases. The purpose of this study was to analyze the effects of antibiotics on biofilms of STEC and the relationships between cellular stress and the release of Stx. To this end, biofilms of reference and clinical strains were treated with antibiotics (ciprofloxacin, fosfomycin and rifaximin) and the production of oxidants, the antioxidant defense system and toxin release were evaluated. Ciprofloxacin altered the prooxidant-antioxidant balance, with a decrease of oxidant metabolites and an increase of superoxide dismutase and catalase activity, being associated with high-levels of Stx production. Furthermore, inhibition of oxidative stress by exogenous antioxidants was correlated with a reduction in the liberation of Stx, indicating the participation of this phenomenon in the release of this toxin. In contrast, fosfomycin and rifaximin produced less alteration with a minimal production of Stx. Our data show that treatment of biofilm-STEC with these antibiotics induces oxidative stress-mediated release of Stx. © 2015 Elsevier Ltd.

Registro:

Documento: Artículo
Título:Effect of antibiotics on cellular stress generated in Shiga toxin-producing Escherichia coli O157: H7 and non-O157 biofilms
Autor:Angel Villegas, N.; Baronetti, J.; Albesa, I.; Etcheverría, A.; Becerra, M.C.; Padola, N.L.; Paraje, M.G.
Filiación:IMBIV-CONICET y Departamento de Farmacia, Facultad de Ciencias Químicas, Universidad Nacional de Córdoba, Argentina
IMBIV-CONICET y Cátedra de Microbiología, Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de Córdoba, Argentina
Laboratorio de Inmunoquímica y Biotecnología, Dpto. SAMP, Facultad de Ciencias Veterinarias, Universidad Nacional del Centro de la Provincia de Buenos Aires, Tandil, Argentina
Palabras clave:Antibiotic; Biofilms; Ciprofloxacin; Escherichia coli O157:H7; Fosfomycin; Hemolytic uremic syndrome (HUS); Rifaximin; Shiga toxin (Stx); antibiotic agent; antioxidant; ascorbic acid; catalase; ciprofloxacin; fosfomycin; glutathione; nitrite; oxidizing agent; reactive oxygen metabolite; rifaximin; Shiga toxin; superoxide dismutase; tiron; antiinfective agent; antioxidant; ascorbic acid; catalase; ciprofloxacin; fosfomycin; glutathione; nitric oxide; reactive oxygen metabolite; rifamycin; rifaximin; superoxide dismutase; verotoxin 1; verotoxin 2; virulence factor; antibiotic resistance; antibiotic sensitivity; antioxidant activity; antioxidant responsive element; Article; bacterial strain; bacterial virulence; biofilm; cell stress; controlled study; cytotoxicity; drug effect; enzyme activity; Escherichia coli O157; metabolite; minimum inhibitory concentration; nonhuman; oxidative stress; Vero cell line; animal; biofilm; cell survival; Chlorocebus aethiops; drug effects; genetics; metabolism; microbial sensitivity test; physiology; Shiga toxin producing Escherichia coli; Bacteria (microorganisms); Escherichia coli; Animals; Anti-Bacterial Agents; Antioxidants; Ascorbic Acid; Biofilms; Catalase; Cell Survival; Cercopithecus aethiops; Ciprofloxacin; Fosfomycin; Glutathione; Microbial Sensitivity Tests; Nitric Oxide; Oxidative Stress; Reactive Oxygen Species; Rifamycins; Shiga Toxin 1; Shiga Toxin 2; Shiga-Toxigenic Escherichia coli; Superoxide Dismutase; Vero Cells; Virulence Factors
Año:2015
Volumen:29
Número:7
Página de inicio:1692
Página de fin:1700
DOI: http://dx.doi.org/10.1016/j.tiv.2015.06.025
Título revista:Toxicology in Vitro
Título revista abreviado:Toxicol. Vitro
ISSN:08872333
CODEN:TIVIE
CAS:ascorbic acid, 134-03-2, 15421-15-5, 50-81-7; catalase, 9001-05-2; ciprofloxacin, 85721-33-1; fosfomycin, 23155-02-4; glutathione, 70-18-8; nitrite, 14797-65-0; rifaximin, 80621-81-4, 88747-56-2; Shiga toxin, 75757-64-1; superoxide dismutase, 37294-21-6, 9016-01-7, 9054-89-1; tiron, 149-45-1, 149-46-2; nitric oxide, 10102-43-9; rifamycin, 6998-60-3, 14897-39-3, 15105-92-7; Anti-Bacterial Agents; Antioxidants; Ascorbic Acid; Catalase; Ciprofloxacin; Fosfomycin; Glutathione; Nitric Oxide; Reactive Oxygen Species; Rifamycins; rifaximin; Shiga Toxin 1; Shiga Toxin 2; Superoxide Dismutase; Virulence Factors
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_08872333_v29_n7_p1692_AngelVillegas

Referencias:

  • Abu-Ali, G.S., Ouellette, L.M., Henderson, S.T., Lacher, D.W., Riordan, J.T., Increased adherence and expression of virulence genes in a lineage of Escherichia coli O157:H7 commonly associated with human infections (2010) PLoS ONE, 5, p. 10167
  • Aiassa, V., Barnes, A.I., Smania, A.M., Albesa, I., Sublethal ciprofloxacin treatment leads to resistance via antioxidant systems in Proteus mirabilis (2012) FEMS Microbiol. Lett., 327, pp. 25-32
  • Al Safadi, R., Abu-Ali, G.S., Sloup, R.E., Rudrik, J.T., Waters, C.M., Eaton, K.A., Manning, S.D., Correlation between in vivo biofilm formation and virulence gene expression in Escherichia coli O104:H4 (2012) PLoS One, 7, p. 41628
  • Albesa, I., Becerra, M.C., Battán, P.C., Páez, P.L., Oxidative stress involved in the antibacterial action of different antibiotics (2004) Biochem. Biophys. Res. Commun., 317, pp. 605-609
  • Angel Villegas, N., Baronetti, J., Albesa, I., Polifroni, R., Parma, A., Etcheverría, A., Becerra, M., Paraje, M., Relevance of biofilms in the pathogenesis of Shiga-Toxin-producing Escherichia coli, infection (2013) Sci. World J., 12, p. 607258
  • Arce Miranda, J.E., Sotomayor, C.E., Albesa, I., Paraje, M.G., Oxidative and nitrosative stress in Staphylococcus aureus biofilm (2011) FEMS Microbiol. Lett., 1, pp. 23-29
  • Baronetti, J.L., Angel Villegas, N., Paraje, M.G., Albesa, I., Nitric oxide-mediated apoptosis in rat macrophages subjected to Shiga toxin 2 from Escherichia coli (2011) Microbiol. Immunol., 55, pp. 231-238
  • Baronetti, J.L., Angel Villegas, N., Aiassa, V., Paraje, M.G., Albesa, I., Hemolysin from Escherichia coli induces oxidative stress in blood (2013) Toxicon, 70, pp. 15-20
  • Barraud, N., Hassett, D.J., Hwang, S.H., Rice, S.A., Kjelleberg, S., Webb, J.S., Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa (2006) J. Bacteriol., 188, pp. 7344-7353
  • Bergan, J., Dyve Lingelem, A.B., Simm, R., Skotland, T., Sandvig, K., Shiga toxins (2012) Toxicon, 60, pp. 1085-1107
  • Bielaszewska, M., Mellmann, A., Zhang, W., Köck, R., Fruth, A., Bauwens, A., Peters, G., Karch, H., Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study (2011) Lancet Infect Dis, 1, pp. 671-676
  • Bielaszewska, M., Idelevich, E.A., Zhang, W., Bauwens, A., Schaumburg, F., Mellmann, A., Peters, G., Karch, H., Effects of antibiotics on Shiga toxin 2 production and bacteriophage induction by epidemic Escherichia coli O104:H4 strain (2012) Antimicrob. Agents Chemother., 56, pp. 3277-3282
  • Boehm, A., Steiner, S., Zaehringer, F., Casanova, A., Hamburger, F., Ritz, D., Keck, W., Jenal, U., Second messenger signalling governs Escherichia coli biofilm induction upon ribosomal stress (2009) Mol. Microbiol., 72, pp. 1500-1516
  • Boles, B.R., Singh, P.K., Endogenous oxidative stress produces diversity and adaptability in biofilm communities (2008) Proc. Natl. Acad. Sci. USA, 105, pp. 12503-12508
  • Burmolle, M., Thomsen, T.R., Fazli, M., Dige, I., Christensen, L., Biofilms in chronic infections - a matter of opportunity - monospecies biofilms in multispecies infections (2010) FEMS Immunol. Med. Microbiol., 59, pp. 324-336
  • (2010) Performance Standards for Antimicrobial Susceptibility Testing, , 20th Informational Supplement,; M100-S20 and M100 S20 Supplement. Wayne, PA, EE.UU
  • Croxen, M.A., Law, R.J., Scholz, R., Keeney, K.M., Wlodarska, M., Finlay, B.B., Recent advances in understanding enteric pathogenic Escherichia coli (2013) Clin. Microbiol. Rev., 26, pp. 822-880
  • Dwyer, D.J., Kohanski, M.A., Hayete, B., Collins, J.J., Gyrase inhibitors induce an oxidative damage cellular death pathway in Escherichia coli (2007) Mol. Syst. Biol., 3, p. 91
  • Dwyer, D.J., Kohanski, M.A., Collins, J.J., Role of reactive oxygen species in antibiotic action and resistance (2009) Curr. Opin. Microbiol., 12, pp. 482-489
  • Fernández, D., Krüger, A., Polifroni, R., Bustamante, V.A., Sanso, M., Etcheverría, A.I., Lucchesi, P.M.A., Padola, N.L., Characterization of Shiga toxin producing Escherichia coli O130:H11 and O178:H19 isolated from dairy cows (2013) Front. Cell. Infect. Microbiol., 8, pp. 3-9
  • Goswami, M., Mangoli, S.H., Jawali, N., Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli (2006) Antimicrob. Agents Chemother., 50, pp. 949-954
  • Hoffman, L.R., D'Argenio, D.A., MacCoss, M.J., Zhang, Z., Jones, R.A., Miller, S.I., Aminoglycoside antibiotics induce bacterial biofilm formation (2005) Nature, 436, pp. 1171-1175
  • Kim, Y.H., Lee, Y., Kim, S., Yeom, J., Seok Kim, B., Oh, S., Park, S., Park, W., The role of periplasmic antioxidant enzymes of the Shiga toxin-producing E. coli O157:H7 in the formation of biofilms (2006) Proteomics, 23, pp. 6181-6193
  • Kimmitt, P.T., Harwood, C.R., Barer, M.R., Toxin gene expression by Shiga toxin producing Escherichia coli: the role of antibiotics and the bacterial SOS response (2000) Emerg. Infect. Dis., 6, pp. 458-465
  • Kohanski, M.A., Dwyer, D.J., Hayete, B., Lawrence, C.A., Collins, J.J., A common mechanism of cellular death induced by bactericidal antibiotics (2007) Cell, 130, pp. 797-810
  • Kohanski, M.A., Dwyer, D.J., Wierzbowski, J., Cottarel, G., Collins, J.J., Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death (2008) Cell, 135, pp. 679-690
  • Kolodkin-Gal, I., Engelberg-Kulka, H., The extracellular death factor: physiological and genetic factors influencing its production and response in Escherichia coli (2008) J. Bacteriol., 190, pp. 3169-3175
  • Kolodkin-Gal, I., Sat, B., Keshet, A., Kulka, H.E., The communication factor EDF and the toxin-antitoxin module mazEF determine the mode of action of antibiotics (2008) PLoS Biol., 6, pp. 2775-2785
  • Kothary, V., Scherl, E.J., Bosworth, B., Jiang, Z.D., Dupont, H.L., Harel, J., Simpson, K.W., Dogan, B., Rifaximin resistance in Escherichia coli associated with inflammatory bowel disease correlates with prior rifaximin use, mutations in rpoB, and activity of Phe-Arg-β naphthylamide-inhibitable efflux pumps (2013) Antimicrob. Agents Chemother., 57, pp. 811-817
  • Krüger, A., Lucchesi, P.M.A., Parma Verotoxins in bovine and meat verotoxin-producing Escherichia coli isolates: type, number of variants, and relationship to cytotoxicity (2011) Appl. Environ. Microbiol., 77, pp. 73-79
  • Kuczynska-Wisnik, D., Matuszewska, E., Laskowska, E., Escherichia coli heat-shock proteins IbpA and IbpB affect biofilm formation by influencing the level of extracellular indole (2010) Microbiology, 156, pp. 148-157
  • Landoni, V.I., de Campos-Nebel, M., Schierloh, P., Calatayud, C., Fernandez, G.C., Ramos, M.V., Rearte, B., Isturiz, M.A., Shiga toxin 1-induced inflammatory response in lipopolysaccharide-sensitized astrocytes is mediated by endogenous tumor necrosis factor alpha (2010) Infect. Immun., 78, pp. 1193-1201
  • Ledesma, M.A., Ochoa, S.A., Cruz, A., Rocha-Ramírez, L.M., Mas-Oliva, J., Eslava, C.A., Xicohtencatl-Cortes, J., The hemorrhagic coli pilus (HCP) of Escherichia coli O157:H7 is an inducer of proinflammatory cytokine secretion in intestinal epithelial cells (2010) PLoS ONE, 5, p. e12127
  • Lee, J.H., Stein, B.D., Antimicrobials effective for inhibition of enterohaemorrhagic Escherichia coli strains O26, O111, and O157 and their effects on Shiga toxin releases (2009) J. Microbiol. Biotechnol., 19, pp. 1238-1243
  • Loś, J.M., Loś, M., Wegrzyn, A., Wegrzyn, G., Hydrogen peroxide-mediated induction of the Shiga toxin-converting lambdoid prophage ST2-8624 in Escherichia coli O157:H7 (2010) FEMS Immunol. Med. Microbiol., 58, pp. 322-329
  • McGannon, C.M., Fuller, C.A., Weiss, A.A., Different classes of antibiotics differentially influence Shiga toxin production (2010) Antimicrob. Agents Chemother., 54, pp. 3790-3798
  • Nataro, J.P., Enteroaggregative Escherichia coli pathogenesis (2005) Curr. Opin. Gastroenterol., 21, pp. 4-8
  • Nguyen, Y., Sperandio, V., Enterohemorrhagic E. coli (EHEC) pathogenesis (2012) Front. Cell. Infect. Microbiol., 12, pp. 2-90
  • Nguyen, D., Joshi-Datar, A., Lepine, F., Bauerle, E., Olakanmi, O., Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria (2011) Science, 334, pp. 982-986
  • O'Toole, G.A., Kolter, R., Initiation of biofilm formation in Pseudomonas fluorescensWCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis (1998) Mol. Microbiol., 28, pp. 449-461
  • Ochoa, T.J., Chen, J., Walker, C.M., Gonzales, E., Cleary, T.G., Rifaximin does not induce toxin production or phage-mediated lysis of Shiga toxin-producing Escherichia coli (2007) Antimicrob. Agents Chemother., 51, pp. 2837-2841
  • Padayatty, S.J., Katz, A., Wang, Y., Eck, P., Kwon, O., Lee, J.H., Chen, S., Levine, M., Vitamin C as an antioxidant: evaluation of its role in disease prevention (2003) J. Am. Coll. Nutr., 22, pp. 18-35
  • Páez, P.L., Becerra, M.C., Albesa, I., Antioxidative mechanisms protect resistant strains of Staphylococcus aureus against ciprofloxacin oxidative damage (2010) Fundam. Clin. Pharmacol., 24, pp. 771-776
  • Páez, P.L., Becerra, M.C., Albesa, I., Effect of the association of reduced glutathione and ciprofloxacin on the antimicrobial activity in Staphylococcus aureus (2010) FEMS Microbiol. Lett., 303, pp. 101-105
  • Páez, P.L., Becerra, M.C., Albesa, I., Comparison of macromolecular oxidation by reactive oxygen species in three bacterial genera exposed to different antibiotics (2011) Cell Biochem. Biophys., 61, pp. 467-472
  • Páez, P.L., Becerra, M.C., Albesa, I., Impact of ciprofloxacin and chloramphenicol on the lipid bilayer of Staphylococcus aureus: changes in membrane potential (2013) Biomed. Res. Int., 2013, p. 276524
  • Paraje, M.G., Antimicrobial resistance in biofilms (2011) Science Against Microbial Pathogens: Communicating Current Research and Technological Advances, , Formatex Research Center, Badajoz, pp. 736-744, A. Méndez-Vilas (Ed.)
  • Paton, A.W., Paton, J.C., Direct detection and characterization of Shiga toxigenic Escherichia coli by multiplex PCR for stx1, stx2, eae, ehxA, and saa (2002) J. Clin. Microbiol., 40, pp. 271-274
  • Rivas, L., Dykes, G.A., Fegan, N., A comparative study of biofilm formation by Shiga toxigenic Escherichia coli using epifluorescence microscopy on stainless steel and a microtitre plate method (2007) J. Microbiol. Methods, 69, pp. 44-51
  • Ryu, J.H., Beuchat, L.R., Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine (2005) Appl. Environ. Microbiol., 71, pp. 247-255
  • Ryu, J.H., Kim, H., Beuchat, L.R., Attachment and biofilm formation by Escherichia coli O157:H7 on stainless steel as influenced by exopolysaccharide production, nutrient availability, and temperature (2004) J. Food Prot., 10, pp. 2123-2131
  • Schlag, S., Nerz, C., Birkenstock, T.A., Altenberend, F., Götz, F., Inhibition of staphylococcal biofilm formation by nitrite (2007) J. Bacteriol., 189, pp. 7911-7919
  • Smith, K.E., Wilker, P.R., Reiter, P.L., Hedican, E.B., Bender, J.B., Hedberg, C.W., Antibiotic treatment of Escherichia coli O157 infection and the risk of hemolytic uremic syndrome, Minnesota (2012) Pediatr. Infect. Dis. J., 31, pp. 37-41
  • Tarr, P.I., Gordon, C.A., Chandler, W.L., Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome (2005) Lancet, 365, pp. 1073-1086
  • Teel, L.D., Daly, J.A., Jerris, R.C., Maul, D., Svanas, G., O'Brien, A.D., Park, C.H., Rapid detection of Shiga toxin-producing Escherichia coli by optical immunoassay (2007) J. Clin. Microbiol., 45, pp. 3377-3380
  • Ullrich, S., Bremer, P., Neumann-Grutzeck, C., Otto, H., Rüther, C., von Seydewitz, C.U., Meyer, G.P., Hagenmüller, F., Symptoms and clinical course of EHEC O104 infection in hospitalized patients: a prospective single center study (2013) PLoS ONE, 8, p. 55278
  • Van Meervenne, E., De Weirdt, R., Van Coillie, E., Devlieghere, F., Herman, L., Boon, N., Biofilm models for the food industry: hot spots for plasmid transfer? (2014) Pathog. Dis., 70, pp. 332-338
  • Zhang, X., McDaniel, A.D., Wolf, L.E., Keusch, G.T., Waldor, M.K., Acheson, D.W., Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice (2000) J. Infect. Dis., 181, pp. 664-670
  • Zhang, Q., Donohue-Rolfe, A., Krautz-Peterson, G., Sevo, M., Parry, N., Abeijon, C., Tzipori, S., Gnotobiotic piglet infection model for evaluating the safe use of antibiotics against Escherichia coli O157:H7 infection (2009) J. Infect. Dis., 199, pp. 486-493

Citas:

---------- APA ----------
Angel Villegas, N., Baronetti, J., Albesa, I., Etcheverría, A., Becerra, M.C., Padola, N.L. & Paraje, M.G. (2015) . Effect of antibiotics on cellular stress generated in Shiga toxin-producing Escherichia coli O157: H7 and non-O157 biofilms. Toxicology in Vitro, 29(7), 1692-1700.
http://dx.doi.org/10.1016/j.tiv.2015.06.025
---------- CHICAGO ----------
Angel Villegas, N., Baronetti, J., Albesa, I., Etcheverría, A., Becerra, M.C., Padola, N.L., et al. "Effect of antibiotics on cellular stress generated in Shiga toxin-producing Escherichia coli O157: H7 and non-O157 biofilms" . Toxicology in Vitro 29, no. 7 (2015) : 1692-1700.
http://dx.doi.org/10.1016/j.tiv.2015.06.025
---------- MLA ----------
Angel Villegas, N., Baronetti, J., Albesa, I., Etcheverría, A., Becerra, M.C., Padola, N.L., et al. "Effect of antibiotics on cellular stress generated in Shiga toxin-producing Escherichia coli O157: H7 and non-O157 biofilms" . Toxicology in Vitro, vol. 29, no. 7, 2015, pp. 1692-1700.
http://dx.doi.org/10.1016/j.tiv.2015.06.025
---------- VANCOUVER ----------
Angel Villegas, N., Baronetti, J., Albesa, I., Etcheverría, A., Becerra, M.C., Padola, N.L., et al. Effect of antibiotics on cellular stress generated in Shiga toxin-producing Escherichia coli O157: H7 and non-O157 biofilms. Toxicol. Vitro. 2015;29(7):1692-1700.
http://dx.doi.org/10.1016/j.tiv.2015.06.025