New Virulence Factors of Enterohemorrhagic Escherichia coli (EHEC) O157:H7 in Dairy Food Processing

  • Moon, Yong-Il (Dept. of Animal Source Foods, Woosuk University) ;
  • Oh, Sangnam (BK21 Plus Graduate Program, Department of Animal Science and Institute of Agricultural Science & Technology, Chonbuk National University) ;
  • Park, Mi Ri (BK21 Plus Graduate Program, Department of Animal Science and Institute of Agricultural Science & Technology, Chonbuk National University) ;
  • Son, Seok Jun (BK21 Plus Graduate Program, Department of Animal Science and Institute of Agricultural Science & Technology, Chonbuk National University) ;
  • Go, Gwang-woong (Dept. of Food and Nutrition, Kookmin University) ;
  • Song, Minho (Dept. of Animal Science and Biotechnology, Chungnam National University) ;
  • Oh, Sejong (Division of Animal Science, Chonnam National University) ;
  • Kim, Sae Hun (Division of Food Bioscience and Technology, College of Life Sciences and Biotechnology, Korea University) ;
  • Kim, Younghoon (BK21 Plus Graduate Program, Department of Animal Science and Institute of Agricultural Science & Technology, Chonbuk National University)
  • Received : 2015.03.01
  • Accepted : 2015.03.26
  • Published : 2015.03.31

Abstract

Enterohemorrhagic Escherichia coli (EHEC) O157:H7 is well-characterized as an important food-borne pathogen worldwide and causes human diseases such as diarrhea, hemorrhagic colitis, and hemolytic uremic syndrome (HUS) by producing shiga-like toxin (Stx). It has been reported that a number of dairy foods, including cheese, can act as the source of EHEC O157:H7 infections. In addition to the toxicity of Stx, recently it has been indicated that EHEC O157:H7 possesses virulence factors related to attachment, quorum sensing, and biofilms. Moreover, these novel virulence factors might become critical points to be considered in the future production of food derived from animals. Here, we review the evidences that support these insights on new virulence factors and discuss the potential mechanisms mediating the pathogenesis of EHEC O157:H7 in the dairy food industry.

Keywords

References

  1. Adler, S. and Bollu, R. 1998. Glomerular endothelial cell injury mediated by Shiga-like toxin-1. Kidney Blood Pressure Res. 21:13-21. https://doi.org/10.1159/000025838
  2. Bean, N. H., Goulding, J. S., Lao, C. and Angulo, F. J. 1996. Surveillance for food borne-disease outbreaks-United States, 1988-1992. MMWR. 45(SS-5):1-65.
  3. Bidet, P., Mariani-Kurkdjian, P., Grimont, F., Brahimi, N., Courroux, C., Grimont, P. and Bingen, E. 2005. Characterization of Escherichia coli O157:H7 isolates causing haemolytic uraemic syndrome in France. J. Med. Microbiol. 54:71-75. https://doi.org/10.1099/jmm.0.45841-0
  4. Branda, S. S., Vik, S., Friedman, L. and Kolter, R. 2005. Biofilms: The matrix revisited. Trends Microbiol. 13:20-26. https://doi.org/10.1016/j.tim.2004.11.006
  5. Camara, M., Williams, P. and Hardman, A. 2002. Controlling infection by tuning in and turning down the volume of bacterial small-talk. Lancet Infect Dis. 2:667-676. https://doi.org/10.1016/S1473-3099(02)00447-4
  6. Carmen, J. C., Nelson, J. L., Beckstead, B. L., Runyan, C. M., Robison, R. A., Schaalje, G. B. and Pitt, W. P. 2004. Ultrasonic-enhanced gentamicin transport through colony biofilms of Pseudomonas aeruginosa and Escherichia coli. J. Infect. Chemother. 10:193-199. https://doi.org/10.1007/s10156-004-0319-1
  7. D'Amico, D. J., Druart, M. J. and Donnelly, C. W. 2010. Behavior of Escherichia coli O157:H7 during the manufacture and aging of Gouda and Stirred-curd Cheddar cheeses manufactured from raw milk. J. Food Prot. 73:2217-2224. https://doi.org/10.4315/0362-028X-73.12.2217
  8. De Kievit, T. R., Gillis, R., Marx, S., Brown, C. and Iglewski, B. H. 2001. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: Their role and expression patterns. Appl. Environ. Microbiol. 67:1865-1873. https://doi.org/10.1128/AEM.67.4.1865-1873.2001
  9. Donlan, R. M. and Costerton, J. W. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol Rev. 15:167-193. https://doi.org/10.1128/CMR.15.2.167-193.2002
  10. Elliot, S., Wainwright, L. A., McDaniel, T. K., MacNamara, B., Donnenberg, M. and Kaper, J. B. 1998. The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol. Microbiol. 28:1-4.
  11. Food Safety and Inspection Service (FSIS). 2004. "Microbiological results of raw ground beef products analyzed for Escherichia coli O157:H7. [Internet WWW]." ADDRESS: http://www.fsis.usda.gov/OPHS/ecoltest/tables1.htm. Accessed 12 Jan 2005.
  12. Fraser, M. E., Fujinaga, M., Cherney, M. M., Melton-Celsa, A. R., Twiddy, E. M., O'Brien, A. D. and James, M. N. G. 2004. Structure of Shiga toxin type 2 (Stx2) from Escherichia coli O157:H7. J. Biol. Chem. 279:27511-27517. https://doi.org/10.1074/jbc.M401939200
  13. Griffin, P. M. and Taxue, R. V. 1991. The epidemiology of infections caused by E. coli O157:H7, other enterohemorrhagic E. coli, and the associated hemolytic uremic syndrome. Epidemiol. Rev. 13:60-98. https://doi.org/10.1093/oxfordjournals.epirev.a036079
  14. Hausner, M. and Wuertz, S. 1999. High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl. Environ. Microbiol. 65:3710-3713. https://doi.org/10.1128/AEM.65.8.3710-3713.1999
  15. Hoey, D. E., Currie, C., Else, R. W., Nutikka, A., Lingwood, C. A., Gally, D. L. and Smith, D. G. E. 2002. Expression of receptors for verotoxin 1 from Escherichia coli O157 on bovine intestinal epithelium. J. Med. Microbiol. 51:143-149. https://doi.org/10.1099/0022-1317-51-2-143
  16. Hudson, L. M., Chen, J., Hill, A. R. and Griffiths, M. W. 1997. Bioluminescence: A rapid indicator of E. coli O157:H7 in selected yogurt and cheese varieties. J. Food Prot. 60:891-897. https://doi.org/10.4315/0362-028X-60.8.891
  17. Hughes, K. A., Sutherland, I. W. and Jones, M. V. 1998. Biofilm susceptibility to bacteriophage attack: The role of phage-borne polysaccharide depolymerase. Microbiology 144:3039-3047. https://doi.org/10.1099/00221287-144-11-3039
  18. Jarvis, K. G., Giron, J. A., Jerse, A. E., McDaniel, T. K., Donnenberg, M. S. and Kaper, J. B. 1995. Enteropathogenic Escherichia coli contains a specialized secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc. Natl. Acad. Sci. USA. 92:7996-8000. https://doi.org/10.1073/pnas.92.17.7996
  19. Jerse, A. E. and Kaper, J. B. 1991. The eae gene of enteropathogenic Escherichia coli encodes a 94-kilodalton membrane protein, the expression of which is influenced by the EAF plasmid. Infect. Immun. 59:4302-4309.
  20. Kaper, J. B. and Sperandio, V. 2005. Bacterial cell-to-cell signaling in the gastrointestinal tract. Infect. Immun. 73:3197-209. https://doi.org/10.1128/IAI.73.6.3197-3209.2005
  21. Kenny, B., DeVinney, R., Stein, M., Reinscheid, D. J., Frey, E. A. and Finlay, B. B. 1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:511-520. https://doi.org/10.1016/S0092-8674(00)80437-7
  22. Kim, Y., Lee, Y., Kim, S. H., Yeom, J., Kim, B. S., Oh, S., Park, S., Jeon, C. O. and Park, W. 2006. Role of periplasmic antioxidant enzymes (superoxide dismutase and thiol peroxidase) of the Shiga toxin-producing Escherichia coli O157:H7 in the formation of biofilms. Proteomics 6:6181-6193. https://doi.org/10.1002/pmic.200600320
  23. Kim, Y., Oh, S. and Kim, S. H. 2009. Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157:H7. Biochemical and Biophysical Research Communications 379:324-329. https://doi.org/10.1016/j.bbrc.2008.12.053
  24. Knutton, S., Adu-Bobie, J., Bain, C., Phillips, A. D., Dougan, G. and Frankel, G. 1997. Down regulation of intimin expression during attaching and effacing enteropathogenic Escherichia coli adhesion. Infect Immun. 65: 1644-1652.
  25. Lingwood, C. A. 1996. Role of verotoxin receptors in pathogenesis. Trends Microbiol. 4:147-153. https://doi.org/10.1016/0966-842X(96)10017-2
  26. Mah, T. F. and O'Toole, G. A. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9:34-39. https://doi.org/10.1016/S0966-842X(00)01913-2
  27. Mayville, P., Ji, G., Beavis, R., Yang, H., Goger, M., Novick, R. P. and Muir, T. W. 1999. Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc. Natl. Acad. Sci. USA. 96:1218-1223. https://doi.org/10.1073/pnas.96.4.1218
  28. Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., Griffin, P. M. and Tauxe, R. V. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625. https://doi.org/10.3201/eid0505.990502
  29. Mellies, J. L., Elliot, S. J., Sperandio, V., Donnenberg, M. S. and Kaper, J. B. 1999. The Per regulon of enteropathogenic Escherichia coli: Identification of regulatory cascade and a novel transcriptional activator, the locus of enterocyte effacement (LEE)-encoded regulator (Ler). Mol. Microbiol. 33:1176-1189.
  30. Miller, S. T., Xavier, K. B., Campagna, S. R., Taga, M. E., Semmelhack, M. F., Bassler, B. L. and Hughson, F. M. 2004. Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2. Mol. Cell 15:677-687. https://doi.org/10.1016/j.molcel.2004.07.020
  31. Morbidity and Mortality Weekly Report (MMWR). 2003. "Preliminary FoodNet Data on the incidence of foodborne illnesses - Selected sites, United States, 2002." [Internet WWW]. ADDRESS: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5215a4.htm. Accessed 25 March 2005.
  32. Nataro, J. P. and Kaper, J. B. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201. https://doi.org/10.1128/CMR.11.1.142
  33. Niemela, S. M., Ikaheimo, I., Koskela, M., Veiranto, M., Suokas, E., Tormala, P., Waris, T., Ashammakhi, N. and Syrjala, H. 2006. Ciprofloxacin-releasing bioabsorbable polymer is superior to titanium in preventing Staphylococcus epidermidis attachment and biofilm formation in vitro. J. Biomed. Mater Res. B. Appl. Biomater. 76:8-14.
  34. Norris, P., Noble, M., Francolini, I., Vinogradov, A. M., Stewart, P. S., Ratner, B. D., Costerton, C. W. and Stoodley, P. 2005. Ultrasonically controlled release of ciprofloxacin from self-assembled coatings on poly (2-hydroxyethyl methacrylate) hydrogels for Pseudomonas aeruginosa biofilm prevention. Antimicrob. Agents Chemother. 49:4272-4279. https://doi.org/10.1128/AAC.49.10.4272-4279.2005
  35. Prigent-Combaret, C., Vidal, O., Dorel, C. and Lejeune, P. 1999. Abiotic surface sensing and biofilm dependent regulation of gene expression in Escherichia coli. J. Bacteriol. 181:5993-6002.
  36. Probert, H. M. and Gibson, G. R. 2002. Bacterial biofilms in the human gastrointestinal tract. Curr. Issues Intest. Microbiol. 3:23-27.
  37. Pruimboom-Brees, I. M., Morgan, T. W., Ackermann, M. R., Nystrom, E. D., Samuel, J. E., Cornick, N. A. and Moon, H. W. 2000. Cattle lack vascular receptors for Escherichia coli O157:H7 Shiga toxins. Proc. Natl. Acad. Sci. USA 97:10325-10329. https://doi.org/10.1073/pnas.190329997
  38. Ramey, B. E., Koutsoudis, M., von Bodman, S. B. and Fuqua, C. 2004. Biofilm formation in plant-microbe associations. Curr. Opin. Microbiol. 7:602-609. https://doi.org/10.1016/j.mib.2004.10.014
  39. Raulio, M., Pore, V., Areva, S., Ritala, M., Leskela, M., Linden, M., Rosenholm, J. B., Lounatmaa, K. and Salkinoja-Salonen, M. 2005. Destruction of Deinococcus geothermalis biofilm by photocatalytic ALD and sol-gel $TiO(_2)$ surfaces. J. Ind. Microbiol. Biotechnol. 1-8.
  40. Ren, D., Zuo, R., Gonzalez Barrios, A. F., Bedzyk, L. A., Eldridge, G. R., Pasmore, M. E. and Wood, T. K. 2005. Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid. Appl. Environ. Microbiol. 71:4022-4034. https://doi.org/10.1128/AEM.71.7.4022-4034.2005
  41. Resch, A., Rosenstein, R., Nerz, C. and Gotz, F. 2005. Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl. Environ. Microbiol. 71:2663-2676. https://doi.org/10.1128/AEM.71.5.2663-2676.2005
  42. Ruggenenti, P. and Remuzzi, G. 1998. Pathophysiology and management of thrombotic microangiopathies. J. Nephrol. 11:300-310.
  43. Schembri, M. A., Kjaergaard, K. and Klemm, P. 2003. Global gene expression in Escherichia coli biofilms. Mol. Microbiol. 48:253-267. https://doi.org/10.1046/j.1365-2958.2003.03432.x
  44. Smith, D. G. E., Naylor, S. W. and Gally, D. L. 2002. Consequences of EHEC colonisation in humans and cattle. Int. J. Med. Microbiol. 292:169-183. https://doi.org/10.1078/1438-4221-00202
  45. Sperandio, V., Li, C. C. and Kaper, J. B. 2002. Quorum sensing Escherichia coli regulator A: A regulator of the lysR family involved in the regulation of the locus of enterocyte effacement pathogenecity island in enterohemorrhagic E. coli. Infect. Immun. 70:3085-3093. https://doi.org/10.1128/IAI.70.6.3085-3093.2002
  46. Spika, J. S., Parsons, J. E., Nordenberg, D., Wells, J. G., Gunn, R. A. and Blake, P. A. 1986. Hemolytic uremic syndrome and diarrhea associated with E. coli O157:H7 in a day care center. J. Pediatr. 109:287-291. https://doi.org/10.1016/S0022-3476(86)80386-9
  47. Stoodley, P., Sauer, K., Davies, D. G. and Costerton, J. W. 2002. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56:187-209. https://doi.org/10.1146/annurev.micro.56.012302.160705
  48. te Loo, D. M. W. M., Heuvelink, A. E., de Boer, E., Nauta, J., van der Walle, J., Schroder, C., van Hinsbergh, V. W. M., Chart, H., van der Kar, N. C. A. J. and van der Heuvel, L. P. W. J. 2001. Verocytotoxin binding to polymorphonuclear leukocytes among households with children with hemolytic uremic syndrome. J. Infect. Dis. 184:446-450. https://doi.org/10.1086/322782
  49. Tuttlebee, C. M., O'Donnell, M. J., Keane, C. T., Russell, R. J., Sullivan, D. J., Falkiner, F. and Coleman, D. C. 2002. Effective control of dental chair unit waterline biofilm and marked reduction of bacterial contamination of output water using two peroxide-based disinfectants. J. Hosp. Infect. 52:192-205. https://doi.org/10.1053/jhin.2002.1282
  50. Vernozy-Rozand, C., Mazuy-Cruchaudet, C., Bavai, C., Montet, M. P., Bonin, V., Dernburg, A. and Richard, Y. 2005. Growth and survival of Escherichia coli O157:H7 during the manufacture and ripening of raw goat milk lactic cheeses. Int. J. Food Microbiol. 105:83-88. https://doi.org/10.1016/j.ijfoodmicro.2005.05.005
  51. Videla, H. A. and Herrera, L. K. 2005. Microbiologically influenced corrosion: Looking to the future. Int. Microbiol. 8:169-180.
  52. Watnick, P. and Kolter, R. 2000. Biofilm, city of microbes. J. Bacteriol. 182:2675-2679. https://doi.org/10.1128/JB.182.10.2675-2679.2000
  53. Xavier, K. B. and Bassler, B. L. 2005. Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J. Bacteriol. 187:238-248. https://doi.org/10.1128/JB.187.1.238-248.2005
  54. Xavier, K. B. and Bassler, B. L. 2003. LuxS quorum sensing: More than just a numbers game. Curr. Opin. Microbiol. 6:191-197. https://doi.org/10.1016/S1369-5274(03)00028-6