Phenethyl isothiocyanate inhibits Shiga toxin production in enterohemorrhagic Escherichia coli by stringent response induction

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 4, 2014, Pages 2304-2315

  Nowicki, Dariusz ^a   Macia̧g Dorszyńska, Monika ^a   Kobiela, Wioletta ^a   Herman Antosiewicz, Anna ^a   Wȩgrzyn, Alicja ^b   Szalewska Pałasz, Agnieszka ^a   Wȩgrzyn, Grzegorz ^a  

^a UNIVERSITY OF GDA SK   (Poland)

^b UNIVERSITY OF SZCZECIN   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; ASPARAGINE; ASPARTIC ACID; CYSTEINE; GLUTAMIC ACID; GLUTAMINE; GLYCINE; GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; HISTIDINE; ISOLEUCINE; ISOTHIOCYANIC ACID; LEUCINE; LYSINE; METHIONINE; MITOMYCIN; PHENETHYL ISOTHIOCYANATE; PHENYLALANINE; PROLINE; SERINE; SHIGA TOXIN; THREONINE; TRYPTOPHAN; TYROSINE; VALINE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIOPHAGE; BACTERIUM CULTURE; DNA REPLICATION; ENTEROHEMORRHAGIC ESCHERICHIA COLI; GENE EXPRESSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA SYNTHESIS;

ANTI-BACTERIAL AGENTS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ISOTHIOCYANATES; SHIGA TOXIN;

EID: 84896944431     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02515-13     Document Type: Article

References (65)

1. Hunt JM. 2010. Shiga toxin-producing Escherichia coli (STEC). Clin. Lab. Med. 30:21-45. http://dx.doi.org/10.1016/j.cll.2009.11.001.
2. Gyles CL. 2007. Shiga toxin-producing Escherichia coli: an overview. J. Anim. Sci. 85:E45-E62. http://dx.doi.org/10.2527/jas.2006-508.
3. Razzaq S. 2006. Hemolytic uremic syndrome: an emerging health risk. Am. Fam. Physician 74:991-996. http://www.aafp.org/afp/2006/0915/p991.html.
4. Mellmann A, Harmsen D, Cummings CA, Zentz EB, Leopold SR, Rico A, Prior K, Szczepanowski R, Ji Y, Zhang W, McLaughlin SF, Henkhaus JK, Leopold B, Bielaszewska M, Prager R, Brzoska PM, Moore RL, Guenther S, Rothberg JM, Karch H. 2011. Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PLoS One 6:e22751. http://dx.doi.org/10.1371/journal.pone.0022751.
5. Beutin L, Martin A. 2012. Outbreak of Shiga toxin-producing Escherichia coli (STEC) O104:H4 infection in Germany causes a paradigm shift with regard to human pathogenicity of STEC strains. J. Food Prot. 75:408-418. http://dx.doi.org/10.4315/0362-028X.JFP-11-452.
6. Bloch SA, Felczykowska A, Nejman-Faleńczyk B. 2012. Escherichia coli O104:H4 outbreak - have we learnt a lesson from it? Acta Biochim. Pol. 59:483-488.
7. Karch H, Denamur E, Dobrindt U, Finlay BB, Hengge R, Johannes L, Ron EZ, Tønjum T, Sansonetti PJ, Vicente M. 2012. The enemy within us: lessons from the 2011 European Escherichia coli O104:H4 outbreak. EMBO Mol. Med. 4:841-848. http://dx.doi.org/10.1002/emmm.201201662.
8. Werber D, Krause G, Frank C, Fruth A, Flieger A, Mielke M, Schaade L, Stark K. 2012. Outbreaks of virulent diarrheagenic Escherichia coli - are we in control? BMC Med. 10:11. http://dx.doi.org/10.1186/1741-7015-10-11.
9. Allison HE. 2007. Stx-phages: drivers and mediators of the evolution of STEC and STEC-like pathogens. Future Microbiol. 2:165-174. http://dx.doi.org/10. 2217/17460913.2.2.165. (Pubitemid 46766990)
10. Łoś JM, Łoś M, Wȩgrzyn G. 2011. Bacteriophages carrying Shiga toxin genes: genomic variations, detection and potential treatment of pathogenic bacteria. Future Microbiol. 6:909-924. http://dx.doi.org/10.2217/fmb.11.70.
11. Wagner PL, Livny J, Neely MN, Acheson DW, Friedman DI, Waldor MK. 2002. Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli. Mol. Microbiol. 44:957-970. http://dx.doi.org/10.1046/j.1365-2958.2002. 02950.x. (Pubitemid 34535532)
12. Wagner PL, Neely MN, Zhang X, Acheson DW, Waldor MK, Friedman DI. 2001. Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J. Bacteriol. 183:2081-2085. http://dx.doi.org/10.1128/ JB.183.6.2081-2085.2001. (Pubitemid 32226005)
13. Ptashne M. 2004. A genetic switch: phage lambda revisited, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
14. Wȩgrzyn G, Wȩgrzyn A. 2005. Genetic switches during bacteriophage lambda development. Prog. Nucleic Acid Res. Mol. Biol. 79:1-48. http://dx.doi.org/10.1016/S0079-6603(04)79001-7. (Pubitemid 43591148)
15. Herold S, Karch H, Schmidt H. 2004. Shiga toxin-encoding bacteriophages - genomes in motion. Int. J. Med. Microbiol. 294:115-121. http://dx.doi.org/10. 1016/j.ijmm.2004.06.023. (Pubitemid 39281041)
16. Waldor MK, Friedman DI. 2005. Phage regulatory circuits and virulence gene expression. Curr. Opin. Microbiol. 8:459-465. http://dx.doi.org/10.1016/j. mib.2005.06.001. (Pubitemid 41021908)
17. Szych J, Wołkowicz T, Ragione RL, Madajczak G. 14 October 2013. Impact of antibiotics on the intestinal microbiota and of Shiga-toxinproducing Escherichia coli and Salmonella infections treatment. Curr. Pharm. Des. http://dx.doi.org/10.2174/13816128113196660730.
18. Walterspiel JN, Ashkenazi S, Morrow AL, Cleary TG. 1992. Effect of subinhibitory concentrations of antibiotics on extracellular Shiga-like toxin I. Infection 20:25-29. http://dx.doi.org/10.1007/BF01704889.
19. Grif K, Dierich MP, Karch H, Allerberger F. 1998. Strain-specific differences in the amount of Shiga toxin released from enterohemorrhagic Escherichia coli O157 following exposure to subinhibitory concentrations of antimicrobial agents. Eur. J. Clin. Microbiol. Infect. Dis. 17:761-766. http://dx.doi.org/10.1007/s100960050181. (Pubitemid 29219127)
20. Pacheco AR, Sperandio V. 2012. Shiga toxin in enterohemorrhagic E. coli: regulation and novel anti-virulence strategies. Front. Cell. Infect. Microbiol. 2:81. http://dx.doi.org/10.3389/fcimb.2012.00081.
21. Serna A, Boedeker EC. 2008. Pathogenesis and treatment of Shiga toxin-producing Escherichia coli infections. Curr. Opin. Gastroenterol. 24:38-47. http://dx.doi.org/10.1097/MOG.0b013e3282f2dfb8. (Pubitemid 350190896)
22. Rogers TJ, Paton JC. 2009. Therapeutic strategies for Shiga toxin-producing Escherichia coli infections. Expert Rev. Anti Infect. Ther. 7:683-686. http://dx.doi.org/10.1586/eri.09.51.
23. Davis TK, McKee R, Schnadower D, Tarr PI. 2013. Treatment of Shiga toxin-producing Escherichia coli infections. Infect. Dis. Clin. North Am. 27:577-597. http://dx.doi.org/10.1016/j.idc.2013.05.010.
24. Nejman-Faleńczyk B, Golec P, Macia̧g M, Wȩgrzyn A, Wȩgrzyn G. 2012. Inhibition of development of Shiga toxin-converting bacteriophages by either treatment with citrate or amino acid starvation. Foodborne Pathog. Dis. 9:13-19. http://dx.doi.org/10.1089/fpd.2011.0980.
25. Nowicki D, Kobiela W, Wȩgrzyn A, Wȩgrzyn G, Szalewska-Pałasz A. 2013. ppGpp-dependent negative control of DNA replication of Shiga toxin-converting bacteriophages in Escherichia coli. J. Bacteriol. 195:5007-5015. http://dx.doi.org/10.1128/JB.00592-13.
26. Potrykus K, Cashel M. 2008. (p)ppGpp: still magical? Annu. Rev. Microbiol. 62:35-51. http://dx.doi.org/10.1146/annurev.micro.62.081307.162903.
27. Kanjee U, Ogata K, Houry WA. 2012. Direct binding targets of the stringent response alarmone(p) ppGpp. Mol. Microbiol. 85:1029-1043. http://dx.doi.org/10.1111/j.1365-2958.2012.08177.x.
28. Singh SV, Singh K. 2012. Cancer chemoprevention with dietary isothiocyanates mature for clinical translational research. Carcinogenesis 33:1833-1842. http://dx.doi.org/10.1093/carcin/bgs216.
29. Kurepina N, Kreiswirth BN, Mustaev A. 2013. Growth-inhibitory activity of natural and synthetic isothiocyanates against representative human microbial pathogens. J. Appl. Microbiol. 115:943-954. http://dx.doi.org/10.1111/jam.12288.
30. Kim HW, Lee CH, Kim MG, Lee HS. 2009. Antibacterial activities of phenethyl isothiocyanate and its derivatives against human oral pathogens. J. Korean Soc. Appl. Biol. Chem. 52:555-559. http://dx.doi.org/10.3839/jksabc.2009. 093.
31. Aires A, Mota VR, Saavedra MJ, Rosa EAS, Bennett RN. 2009. The antimicrobial effects of glucosinolates and their respective enzymatic hydrolysis products on bacteria isolated from the human intestinal tract. J. Appl. Microbiol. 106:2086-2095. http://dx.doi.org/10.1111/j.1365-2672.2009. 04180.x.
32. Abreu AC, Borges A, Simões LC, Saavedra MJ, Simões M. 2013. Antibacterial activity of phenyl isothiocyanate on Escherichia coli and Staphylococcus aureus. Med. Chem. 9:756-761. http://dx.doi.org/10.2174/ 1573406411309050016.
33. Mechold U, Potrykus K, Murphy H, Murakami KS, Cashel M. 2013. Differential regulation by ppGpp versus pppGpp in Escherichia coli. Nucleic Acids Res. 41:6175-6189. http://dx.doi.org/10.1093/nar/gkt302.
34. Łoś JM, Golec P, Wȩgrzyn G, Wȩgrzyn A, Łoś M. 2008. Simple method for plating Escherichia coli bacteriophages forming very small plaques or no plaques under standard conditions. Appl. Environ. Microbiol. 74:5113-5120. http://dx.doi.org/10.1128/ AEM.00306-08.
35. Wȩgrzyn G, Kwasnik E, Taylor K. 1991. Replication of lambda plasmid in amino acid-starved strains of Escherichia coli. Acta Biochim. Pol. 38:181-186.
36. Andrews JM. 2001. Determination of minimum inhibitory concentration. J. Antimicrob. Chemother. 48:5-16. http://dx.doi.org/10.1093/jac/48.suppl-1.5.
37. Mechold U, Malke H. 1997. Characterization of the stringent and relaxed responses of Streptococcus equisimilis. J. Bacteriol. 179:2658-2667. (Pubitemid 27164566)
38. Rasooly M, Do PM. 2010. Shiga toxin Stx2 is heat-stable and not inactivated by pasteurization. Int. J. Food Microbiol. 136:290-294. http://dx.doi.org/10.1016/j.ijfoodmicro.2009.10.005.
39. Macia̧g-Dorszyńska M, Szalewska-Pałasz A, Wȩgrzyn G. 2013. Different effects of ppGpp on Escherichia coli DNA replication in vivo and in vitro. FEBS Open Bio 3:161-164. http://dx.doi.org/10. 1016/j.fob.2013.03.001.
40. Cejpek K, Valusek J, Velisek J. 2000. Reactions of allyl isothiocyanate with alanine, glycine, and several peptides in model systems. J. Agric. Food Chem. 48:3560-3565. http://dx.doi.org/10.1021/jf991019s.
41. Bouzari S, Oloomi M, Azadmanesh K. 2009. Study on induction of apoptosis on HeLa and Vero cells by recombinant shiga toxin and its subunits. Cytotechnology 60:105-113. http://dx.doi.org/10.1007/s10616-009-9220-1.
42. Herold S, Siebert J, Huber A, Schmidt H. 2005. Global expression of prophage genes in Escherichia coli O157:H7 strain EDL933 in response to norfloxacin. Antimicrob. Agents Chemother. 49:931-944. http://dx.doi.org/10. 1128/AAC.49.3.931-944.2005. (Pubitemid 40327707)
43. Ochoa TJ, Chen J, Walker CM, Gonzales E, Cleary TG. 2007. Rifaximin does not induce toxin production or phage-mediated lysis of Shiga toxin-producing Escherichia coli. Antimicrob. Agents Chemother. 51:2837-2841. http://dx.doi.org/10.1128/AAC.01397-06. (Pubitemid 47206219)
44. Mohsin M, Haque A, Ali A, Sarwar Y, Bashir S, Tariq A, Afzal A, Iftikhar T, Saeed MA. 2010. Effects of ampicillin, gentamicin, and cefotaxime on the release of Shiga toxins from Shiga toxin-producing Escherichia coli isolated during a diarrhea episode in Faisalabad, Pakistan. Food-borne Pathog. Dis. 7:85-90. http://dx.doi.org/10.1089/fpd.2009.0311.
45. Bielaszewska M, Idelevich EA, Zhang W, Bauwens A, Schaumburg F, Mellmann A, Peters G, Karch H. 2012. Effects of antibiotics on Shiga toxin 2 production and bacteriophage induction by epidemic Escherichia coli O104:H4 strain. Antimicrob. Agents Chemother. 56:3277-3282. http://dx.doi.org/10.1128/AAC.06315- 11.
46. Chen ML, Hao Z, Tian Y, Zhang QY, Gao PJ, Jin JL. 2013. Different effects of six antibiotics and ten traditional Chinese medicines on Shiga toxin expression by Escherichia coli O157:H7. Evid. Based Complement. Alternat. Med. 2013:121407. http://dx.doi.org/10.1155/2013/121407.
47. Corogeanu D, Willmes R, Wolke M, Plum G, Utermöhlen O, Krönke M. 2012. Therapeutic concentrations of antibiotics inhibit Shiga toxin release from enterohemorrhagic E. coli O104:H4 from the 2011 German outbreak. BMC Microbiol. 12:160. http://dx.doi.org/10.1186/1471-2180-12-160.
48. McGannon CM, Fuller CA, Weiss AA. 2010. Different classes of antibiotics differentially influence Shiga toxin production. Antimicrob. Agents Chemother. 54:3790-3798. http://dx.doi.org/10.1128/AAC.01783-09.
49. Nelson JM, Griffin PM, Jones TF, Smith KE, Scallan E. 2011. Antimicrobial and antimotility agent use in persons with shiga toxin-producing Escherichia coli O157 infection in FoodNet sites. Clin. Infect. Dis. 52: 1130-1132. http://dx.doi.org/10.1093/cid/cir087.
50. Ichinohe N, Ohara-Nemoto Y, Nemoto TK, Kimura S, Ichinohe S. 2009. Effects of fosfomycin on Shiga toxin-producing Escherichia coli: quantification of copy numbers of Shiga toxin-encoding genes and their expression levels using real-time PCR. J. Med. Microbiol. 58:971-973. http://dx.doi.org/10.1099/jmm.0. 008573-0.
51. Ikeda K, Ida O, Kimoto K, Takatorige T, Nakanishi N, Tatara K. 1999. Effect of early fosfomycin treatment on prevention of hemolytic uremic syndrome accompanying Escherichia coli O157:H7 infection. Clin. Nephrol. 52:357-362.
52. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ. 2007. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797-810. http://dx.doi.org/10.1016/j.cell.2007.06.049. (Pubitemid 47332566)
53. Foti JJ, Devadoss B, Winkler JA, Collins JJ, Walker GC. 2012. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science 336:315-319. http://dx.doi.org/10.1126/science.1219192.
54. Łoś JM, Łoś M, Wȩgrzyn G, Wȩgrzyn A. 2009. Differential efficiency of induction of various lambdoid prophages responsible for production of Shiga toxins in response to different induction agents. Microb. Pathog. 47:289-298. http://dx.doi.org/10.1016/j. micpath.2009.09.006.
55. Łoś JM, Łoś M, Wȩgrzyn A, Wȩgrzyn G. 2010. Hydrogen peroxide-mediated induction of the Shiga toxin-converting lambdoid prophages ST2-8624 in Escherichia coli O157:H7. FEMS Immunol. Med. Microbiol. 58:322-329.
56. Liu Y, Imlay JA. 2013. Cell death from antibiotics without the involvement of reactive oxygen species. Science 339:1210-1213. http://dx.doi.org/10.1126/science.1232751.
57. 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. http://dx.doi.org/10.1126/science.1232688.
58. Łoś JM, Łoś M, Wȩgrzyn A, Wȩgrzyn G. 2013. Altruism of Shiga toxin-producing Escherichia coli: recent hypothesis versus experimental results. Front. Cell. Infect. Microbiol. 2:166.
59. Nystom T. 1994. Role of guanosine tetraphosphate in gene expression and the survival of glucose or seryl-tRNA starved cells of Escherichia coli K12. Mol. Gen. Genet. 245:355-362. http://dx.doi.org/10.1007/BF00290116.
60. Dalebroux ZD, Svensson S, Gaynor EC, Swanson MS. 2010. ppGpp conjures bacterial virulence. Microbiol. Mol. Biol. Rev. 74:171-199. http://dx.doi.org/ 10.1128/MMBR.00046-09.
61. Nakanishi N, Abe H, Ogura Y, Hayashi T, Tashiro K, Kuhara S, Sugimoto N, Tobe T. 2006. ppGpp with DksA controls gene expression in the locus of enterocyte effacement (LEE) pathogenicity island of enterohaemorrhagic Escherichia coli through activation of two virulence regulatory genes. Mol. Microbiol. 61:194-205. http://dx.doi.org/10.1111/j.1365-2958.2006.05217.x.
62. Jensen KF. 1993. The Escherichia coli K-12 "wild types" W3110 and MG1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyrE expression levels. J. Bacteriol. 175:3401-3407. (Pubitemid 23163383)
63. Xiao H, Kalman M, Ikehara K, Zemel S, Glaser G, Cashel M. 1991. Residual guanosine 3′,5′-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations. J. Biol. Chem. 266:5980-5990. (Pubitemid 21909592)
64. Gamage SD, Patton AK, Hanson JF, Weiss AA. 2004. Diversity and host range of Shiga toxin-encoding phage. Infect. Immun. 72:7131-7139. http://dx.doi.org/10.1128/IAI.72.12.7131-7139.2004. (Pubitemid 39552383)
65. Griffin PM, Ostroff SM, Tauxe RV, Greene KD, Wells JG, Lewis JH, Blake PA. 1988. Illnesses associated with Escherichia coli O157:H7 infections. A broad clinical spectrum. Ann. Intern. Med. 109:705-712. (Pubitemid 18267545)