Monophasic expression of FliC by 4,[5],12:i:- DT193 does not alter its pathogenicity during infection of porcine intestinal epithelial cells Free

Abstract

Non-typhoidal serotypes of remain important food-borne pathogens worldwide and the frequent emergence of epidemic strains in food-producing animals is a risk to public health. In recent years, 4,[5],12:i:- isolates, expressing only phase 1 (FliC) of the two flagellar antigens, have emerged and increased in prevalence worldwide. In Europe, the majority of 4,[5],12:i:- isolates belong to phage types DT193 and DT120 of Typhimurium and pigs have been identified as the reservoir species. In this study we investigated the ability of pig-derived monophasic (4,[5],12:i:-) and biphasic DT193 isolates to invade a porcine intestinal epithelial cell line (IPEC-1) and activate TLR-5, IL-8 and caspases. We found that the 4,[5],12:i:- isolates exhibited comparable adhesion and invasion to that of the virulent . Typhimurium isolate 4/74, suggesting that these strains could be capable of colonizing the small intestine of pigs . Infection with 4,[5],12:i:- and biphasic DT193 isolates resulted in approximately the same level of TLR-5 (a flagellin receptor) and IL-8 (a proinflammatory chemokine) mRNA upregulation. The monophasic variants also elicited similar levels of caspase activation and cytotoxicity to the phase-variable DT193 isolates. These findings suggest that failure of 4,[5],12:i:- DT193 isolates to express a second phase of flagellar antigen (FljB) is unlikely to hamper their pathogenicity during colonization of the porcine intestinal tract.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.081349-0
2014-11-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/11/2507.html?itemId=/content/journal/micro/10.1099/mic.0.081349-0&mimeType=html&fmt=ahah

References

  1. Aldridge P. D., Wu C., Gnerer J., Karlinsey J. E., Hughes K. T., Sachs M. S. ( 2006). Regulatory protein that inhibits both synthesis and use of the target protein controls flagellar phase variation in Salmonella enterica . Proc Natl Acad Sci U S A 103:11340–11345 [View Article][PubMed]
    [Google Scholar]
  2. Anderson E. S., Ward L. R., Saxe M. J., de Sa J. D. H. ( 1977). Bacteriophage-typing designations of Salmonella typhimurium . J Hyg (Lond) 78:297–300 [View Article][PubMed]
    [Google Scholar]
  3. Anon.. ( 2013). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. EFSA Journal 11:3129
    [Google Scholar]
  4. Anon.. ( 2014). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA Journal 12:3547
    [Google Scholar]
  5. Arques J. L., Hautefort I., Ivory K., Bertelli E., Regoli M., Clare S., Hinton J. C. D., Nicoletti C. ( 2009). Salmonella induces flagellin- and MyD88-dependent migration of bacteria-capturing dendritic cells into the gut lumen. Gastroenterology 137:579–587, e1–e2 [View Article][PubMed]
    [Google Scholar]
  6. Bearson B. L., Bearson S. M. D. ( 2011). Host specific differences alter the requirement for certain Salmonella genes during swine colonization. Vet Microbiol 150:215–219 [View Article][PubMed]
    [Google Scholar]
  7. Bonifield H. R., Hughes K. T. ( 2003). Flagellar phase variation in Salmonella enterica is mediated by a posttranscriptional control mechanism. J Bacteriol 185:3567–3574 [View Article][PubMed]
    [Google Scholar]
  8. Carnell S. C., Bowen A., Morgan E., Maskell D. J., Wallis T. S., Stevens M. P. ( 2007). Role in virulence and protective efficacy in pigs of Salmonella enterica serovar Typhimurium secreted components identified by signature-tagged mutagenesis. Microbiology 153:1940–1952 [View Article][PubMed]
    [Google Scholar]
  9. Eaves-Pyles T. D., Wong H. R., Odoms K., Pyles R. B. ( 2001). Salmonella flagellin-dependent proinflammatory responses are localized to the conserved amino and carboxyl regions of the protein. J Immunol 167:7009–7016 [View Article][PubMed]
    [Google Scholar]
  10. Elewaut D., DiDonato J. A., Kim J. M., Truong F., Eckmann L., Kagnoff M. F. ( 1999). NF-κB is a central regulator of the intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. J Immunol 163:1457–1466[PubMed]
    [Google Scholar]
  11. Fink S. L., Cookson B. T. ( 2007). Pyroptosis and host cell death responses during Salmonella infection. Cell Microbiol 9:2562–2570 [View Article][PubMed]
    [Google Scholar]
  12. Gewirtz A. T., Navas T. A., Lyons S., Godowski P. J., Madara J. L. ( 2001a). Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167:1882–1885 [View Article][PubMed]
    [Google Scholar]
  13. Gewirtz A. T., Simon P. O. Jr, Schmitt C. K., Taylor L. J., Hagedorn C. H., O’Brien A. D., Neish A. S., Madara J. L. ( 2001b). Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest 107:99–109 [View Article][PubMed]
    [Google Scholar]
  14. Gonzalez-Vallina R., Wang H., Zhan R., Berschneider H. M., Lee R. M., Davidson N. O., Black D. D. ( 1996). Lipoprotein and apolipoprotein secretion by a newborn piglet intestinal cell line (IPEC-1). Am J Physiol 271:G249–G259[PubMed]
    [Google Scholar]
  15. Hapfelmeier S., Stecher B., Barthel M., Kremer M., Müller A. J., Heikenwalder M., Stallmach T., Hensel M., Pfeffer K. & other authors ( 2005). The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J Immunol 174:1675–1685 [View Article][PubMed]
    [Google Scholar]
  16. Hauser E., Tietze E., Helmuth R., Junker E., Blank K., Prager R., Rabsch W., Appel B., Fruth A., Malorny B. ( 2010). Pork contaminated with Salmonella enterica serovar 4,[5],12:i:-, an emerging health risk for humans. Appl Environ Microbiol 76:4601–4610 [View Article][PubMed]
    [Google Scholar]
  17. Hayashi F., Smith K. D., Ozinsky A., Hawn T. R., Yi E. C., Goodlett D. R., Eng J. K., Akira S., Underhill D. M., Aderem A. ( 2001). The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099–1103 [View Article][PubMed]
    [Google Scholar]
  18. Hopkins K. L., Kirchner M., Guerra B., Granier S. A., Lucarelli C., Porrero M. C., Jakubczak A., Threlfall E. J., Mevius D. J. ( 2010). Multiresistant Salmonella enterica serovar 4,[5],12:i:- in Europe: a new pandemic strain. Euro Surveill 15:19580[PubMed]
    [Google Scholar]
  19. Hopkins K. L., de Pinna E., Wain J. ( 2012). Prevalence of Salmonella enterica serovar 4,[5],12:i:- in England and Wales, 2010. Euro Surveill 17:20275[PubMed]
    [Google Scholar]
  20. Ikeda J. S., Schmitt C. K., Darnell S. C., Watson P. R., Bispham J., Wallis T. S., Weinstein D. L., Metcalf E. S., Adams P. & other authors ( 2001). Flagellar phase variation of Salmonella enterica serovar Typhimurium contributes to virulence in the murine typhoid infection model but does not influence Salmonella-induced enteropathogenesis. Infect Immun 69:3021–3030 [View Article][PubMed]
    [Google Scholar]
  21. Imre A., Olasz F., Nagy B. ( 2005). Development of a PCR system for the characterisation of Salmonella flagellin genes. Acta Vet Hung 53:163–172 [View Article][PubMed]
    [Google Scholar]
  22. Knodler L. A., Vallance B. A., Celli J., Winfree S., Hansen B., Montero M., Steele-Mortimer O. ( 2010). Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc Natl Acad Sci U S A 107:17733–17738 [View Article][PubMed]
    [Google Scholar]
  23. Martelli F., Gosling R., Kennedy E., Rabie A., Reeves H., Clifton-Hadley F., Davies R., La Ragione R. ( 2014). Characterization of the invasiveness of monophasic and aphasic Salmonella Typhimurium strains in 1-day-old and point-of-lay chickens. Avian Pathol 43:269–275 [View Article][PubMed]
    [Google Scholar]
  24. McCormick B. A., Hofman P. M., Kim J., Carnes D. K., Miller S. I., Madara J. L. ( 1995). Surface attachment of Salmonella typhimurium to intestinal epithelia imprints the subepithelial matrix with gradients chemotactic for neutrophils. J Cell Biol 131:1599–1608 [View Article][PubMed]
    [Google Scholar]
  25. Misselwitz B., Strittmatter G., Periaswamy B., Schlumberger M. C., Rout S., Horvath P., Kozak K., Hardt W. D. ( 2010). Enhanced CellClassifier: a multi-class classification tool for microscopy images. BMC Bioinformatics 11:30 [View Article][PubMed]
    [Google Scholar]
  26. Misselwitz B., Dilling S., Vonaesch P., Sacher R., Snijder B., Schlumberger M., Rout S., Stark M., von Mering C. & other authors ( 2011). RNAi screen of Salmonella invasion shows role of COPI in membrane targeting of cholesterol and Cdc42. Mol Syst Biol 7:474 [View Article][PubMed]
    [Google Scholar]
  27. Misselwitz B., Barrett N., Kreibich S., Vonaesch P., Andritschke D., Rout S., Weidner K., Sormaz M., Songhet P. & other authors ( 2012). Near surface swimming of Salmonella Typhimurium explains target-site selection and cooperative invasion. PLoS Pathog 8:e1002810 [View Article][PubMed]
    [Google Scholar]
  28. Morgan E., Campbell J. D., Rowe S. C., Bispham J., Stevens M. P., Bowen A. J., Barrow P. A., Maskell D. J., Wallis T. S. ( 2004). Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol Microbiol 54:994–1010 [View Article][PubMed]
    [Google Scholar]
  29. Paesold G., Guiney D. G., Eckmann L., Kagnoff M. F. ( 2002). Genes in the Salmonella pathogenicity island 2 and the Salmonella virulence plasmid are essential for Salmonella-induced apoptosis in intestinal epithelial cells. Cell Microbiol 4:771–781 [View Article][PubMed]
    [Google Scholar]
  30. Parsons B. N., Crayford G., Humphrey T. J., Wigley P. ( 2013). Infection of chickens with antimicrobial-resistant Salmonella enterica Typhimurium DT193 and monophasic Salmonella Typhimurium-like variants: an emerging risk to the poultry industry. Avian Pathol 42:443–446 [View Article][PubMed]
    [Google Scholar]
  31. Perrett C. A., Jepson M. A. ( 2007). Applications of cell imaging in Salmonella research. Methods Mol Biol 394:235–273 [View Article][PubMed]
    [Google Scholar]
  32. Rabsch W., Tschäpe H., Bäumler A. J. ( 2001). Non-typhoidal salmonellosis: emerging problems. Microbes Infect 3:237–247 [View Article][PubMed]
    [Google Scholar]
  33. Rajtak U., Boland F., Leonard N., Bolton D., Fanning S. ( 2012). Roles of diet and the acid tolerance response in survival of common Salmonella serotypes in feces of finishing pigs. Appl Environ Microbiol 78:110–119 [View Article][PubMed]
    [Google Scholar]
  34. Reed W. M., Olander H. J., Thacker H. L. ( 1986). Studies on the pathogenesis of Salmonella typhimurium and Salmonella choleraesuis var kunzendorf infection in weanling pigs. Am J Vet Res 47:75–83[PubMed]
    [Google Scholar]
  35. Reis B. P., Zhang S., Tsolis R. M., Bäumler A. J., Adams L. G., Santos R. L. ( 2003). The attenuated sopB mutant of Salmonella enterica serovar Typhimurium has the same tissue distribution and host chemokine response as the wild type in bovine Peyer’s patches. Vet Microbiol 97:269–277 [View Article][PubMed]
    [Google Scholar]
  36. Schwerk C., Schulze-Osthoff K. ( 2003). Non-apoptotic functions of caspases in cellular proliferation and differentiation. Biochem Pharmacol 66:1453–1458 [View Article][PubMed]
    [Google Scholar]
  37. Simon R., Samuel C. E. ( 2007). Activation of NF-κB-dependent gene expression by Salmonella flagellins FliC and FljB. Biochem Biophys Res Commun 355:280–285 [View Article][PubMed]
    [Google Scholar]
  38. Smith K. D., Andersen-Nissen E., Hayashi F., Strobe K., Bergman M. A., Barrett S. L., Cookson B. T., Aderem A. ( 2003). Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 4:1247–1253 [View Article][PubMed]
    [Google Scholar]
  39. Tallant T., Deb A., Kar N., Lupica J., De Veer M. J., DiDonato J. A. ( 2004). Flagellin acting via TLR5 is the major activator of key signaling pathways leading to NF-κB and proinflammatory gene program activation in intestinal epithelial cells. BMC Microbiol 4:33 [View Article][PubMed]
    [Google Scholar]
  40. Tsolis R. M., Adams L. G., Ficht T. A., Bäumler A. J. ( 1999). Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect Immun 67:4879–4885[PubMed]
    [Google Scholar]
  41. van Asten A. J. A. M., Zwaagstra K. A., Baay M. F., Kusters J. G., Huis in’t Veld J. H., van der Zeijst B. A. ( 1995). Identification of the domain which determines the g,m serotype of the flagellin of Salmonella enteritidis . J Bacteriol 177:1610–1613[PubMed]
    [Google Scholar]
  42. Van Parys A., Boyen F., Leyman B., Verbrugghe E., Haesebrouck F., Pasmans F. ( 2011). Tissue-specific Salmonella Typhimurium gene expression during persistence in pigs. PLoS ONE 6:e24120 [View Article][PubMed]
    [Google Scholar]
  43. Vijay-Kumar M., Wu H., Jones R., Grant G., Babbin B., King T. P., Kelly D., Gewirtz A. T., Neish A. S. ( 2006). Flagellin suppresses epithelial apoptosis and limits disease during enteric infection. Am J Pathol 169:1686–1700 [View Article][PubMed]
    [Google Scholar]
  44. Watson P. R., Paulin S. M., Bland A. P., Jones P. W., Wallis T. S. ( 1995). Characterization of intestinal invasion by Salmonella typhimurium and Salmonella dublin and effect of a mutation in the invH gene. Infect Immun 63:2743–2754[PubMed]
    [Google Scholar]
  45. Wells T. J., Sherlock O., Rivas L., Mahajan A., Beatson S. A., Torpdahl M., Webb R. I., Allsopp L. P., Gobius K. S. & other authors ( 2008). EhaA is a novel autotransporter protein of enterohemorrhagic Escherichia coli O157 : H7 that contributes to adhesion and biofilm formation. Environ Microbiol 10:589–604 [View Article][PubMed]
    [Google Scholar]
  46. Yoon S. I., Kurnasov O., Natarajan V., Hong M., Gudkov A. V., Osterman A. L., Wilson I. A. ( 2012). Structural basis of TLR5-flagellin recognition and signaling. Science 335:859–864 [View Article][PubMed]
    [Google Scholar]
  47. Yu Y., Zeng H., Lyons S., Carlson A., Merlin D., Neish A. S., Gewirtz A. T. ( 2003). TLR5-mediated activation of p38 MAPK regulates epithelial IL-8 expression via posttranscriptional mechanism. Am J Physiol Gastrointest Liver Physiol 285:G282–G290[PubMed] [CrossRef]
    [Google Scholar]
  48. Zeng H., Carlson A. Q., Guo Y., Yu Y., Collier-Hyams L. S., Madara J. L., Gewirtz A. T., Neish A. S. ( 2003). Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella . J Immunol 171:3668–3674 [View Article][PubMed]
    [Google Scholar]
  49. Zeng H., Wu H., Sloane V., Jones R., Yu Y., Lin P., Gewirtz A. T., Neish A. S. ( 2006). Flagellin/TLR5 responses in epithelia reveal intertwined activation of inflammatory and apoptotic pathways. Am J Physiol Gastrointest Liver Physiol 290:G96–G108[PubMed] [CrossRef]
    [Google Scholar]
  50. Zhang S., Kingsley R. A., Santos R. L., Andrews-Polymenis H., Raffatellu M., Figueiredo J., Nunes J., Tsolis R. M., Adams L. G., Bäumler A. J. ( 2003). Molecular pathogenesis of Salmonella enterica serotype Typhimurium-induced diarrhea. Infect Immun 71:1–12 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.081349-0
Loading
/content/journal/micro/10.1099/mic.0.081349-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed