1887

Abstract

Despite being classically defined as non-pathogenic, there is growing evidence that biotype 1A isolates may be aetiological agents of disease in humans. In previous studies, a potential link between motility and the ability of biotype 1A strains to invade cultured epithelial cells was observed. In an attempt to further investigate this finding, a flagella mutant was constructed in a human faecal biotype 1A isolate. The flagella mutation abolished the ability of the strain to invade cultured human epithelial cells, although adherence was not affected. The aflagellate mutant was also attenuated in its ability to survive within cultured macrophages, being cleared after 3 h, whilst the wild-type persisted for 24 h after infection. Examination of cytokine secretion by infected macrophages also suggested that the flagella of biotype 1A strains act as anti-inflammatory agents, decreasing production of tumour necrosis factor (TNF)- whilst increasing secretion of interleukin (IL)-10. Preliminary studies using porcine organ culture (IVOC) tissue suggested that the flagella mutant was also attenuated in its ability to colonize intestinal tissue.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/000919-0
2007-05-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/5/1339.html?itemId=/content/journal/micro/10.1099/mic.0.2006/000919-0&mimeType=html&fmt=ahah

References

  1. Aleksic S., Bockemuhl J. 1984; Proposed revision of the Wauters et al. antigenic scheme for serotyping of Yersinia enterocolitica. J Clin Microbiol 20:99–102
    [Google Scholar]
  2. Andor A., Trulzsch K., Essler M., Roggenkamp A., Wiedemann A., Heesemann J., Aepfelbacher M. 2001; YopE of Yersinia , a GAP for Rho GTPases, selectively modulates Rac-dependent actin structures in endothelial cells. Cell Microbiol 3:301–310 [CrossRef]
    [Google Scholar]
  3. Bengoechea J. A., Brandenburg K., Arraiza M. D., Seydel U., Skurnik M., Moriyon I. 2003; Pathogenic Yersinia enterocolitica strains increase the outer membrane permeability in response to environmental stimuli by modulating lipopolysaccharide fluidity and lipid A structure. Infect Immun 71:2014–2021 [CrossRef]
    [Google Scholar]
  4. Bengoechea J. A., Najdenski H., Skurnik M. 2004; Lipopolysaccharide O antigen status of Yersinia enterocolitica O : 8 is essential for virulence and absence of O antigen affects the expression of other Yersinia virulence factors. Mol Microbiol 52:451–469 [CrossRef]
    [Google Scholar]
  5. Bleves S., Marenne M. N., Detry G., Cornelis G. R. 2002; Up-regulation of the Yersinia enterocolitica yop regulon by deletion of the flagellum master operon flhDC. J Bacteriol 184:3214–3223 [CrossRef]
    [Google Scholar]
  6. Boland A., Cornelis G. R. 1998; Role of YopP in suppression of tumor necrosis factor alpha release by macrophages during Yersinia infection. Infect Immun 66:1878–1884
    [Google Scholar]
  7. Bottone E. J. 1999; Yersinia enterocolitica : overview and epidemiologic correlates. Microbes Infect 1:323–333 [CrossRef]
    [Google Scholar]
  8. Carlos I. Z., Monnazzi L. G. S., Falcao D. P., Machado de Medeiros B. M. 2004; TNF- α , H2O2 and NO response of peritoneal macrophages to Yersinia enterocolitica O : 3 derivatives. Microbes Infect 6:207–212 [CrossRef]
    [Google Scholar]
  9. Chang A. C., Cohen S. N. 1978; Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134:1141–1156
    [Google Scholar]
  10. Cornelis G. R., Wolf-Watz H. 1997; The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol 23:861–867 [CrossRef]
    [Google Scholar]
  11. Denecker G., Totemeyer S., Mota L. J., Troisfontaines P., Lambermont I., Youta C., Stainier I., Ackermann M., Cornelis G. R. 2002; Effect of low- and high-virulence Yersinia enterocolitica strains on the inflammatory response of human umbilical vein endothelial cells. Infect Immun 70:3510–3520 [CrossRef]
    [Google Scholar]
  12. Donnelly M. A., Steiner T. S. 2002; Two nonadjacent regions in enteroaggregative Escherichia coli flagellin are required for activation of toll-like receptor 5. J Biol Chem 277:40456–40461 [CrossRef]
    [Google Scholar]
  13. El Tahir Y., Kuusela P., Skurnik M. 2000; Functional mapping of the Yersinia enterocolitica adhesin YadA. Identification of eight NSVAIG-S motifs in the amino-terminal half of the protein involved in collagen binding. Mol Microbiol 37:192–206 [CrossRef]
    [Google Scholar]
  14. Erfurth S. E., Grobner S., Kramer U., Gunst D. S., Soldanova I., Schaller M., Autenrieth I. B., Borgmann S. 2004; Yersinia enterocolitica induces apoptosis and inhibits surface molecule expression and cytokine production in murine dendritic cells. Infect Immun 72:7045–7054 [CrossRef]
    [Google Scholar]
  15. Fearnley C., On S. L., Kokotovich B., Manning G., Cheasty T., Newell D. G. 2005; Application of fluorescent amplified fragment length polymorphism to the comparison of human and animal Yersinia enterocolitica. Appl Environ Microbiol 71:4951–4959 [CrossRef]
    [Google Scholar]
  16. Finlay B. B., Falkow S. 1988; Comparison of the invasion strategies used by Salmonella cholerae Suis, Shigella flexneri and Yersinia enterocolitica to enter cultured animal cells: endosome acidification is not required for bacterial invasion or intracellular replication. Biochimie 70:1089–1099 [CrossRef]
    [Google Scholar]
  17. Giron J. A., Torres A. G., Freer E., Kaper J. B. 2002; The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44:361–379 [CrossRef]
    [Google Scholar]
  18. Grant T., Bennett-Wood V., Robins-Browne R. M. 1998; Identification of virulence-associated characteristics in clinical isolates of Yersinia enterocolitica lacking classical virulence markers. Infect Immun 66:1113–1120
    [Google Scholar]
  19. Grant T., Bennett-Wood V., Robins-Browne R. M. 1999; Characterization of the interaction between Yersinia enterocolitica biotype 1A and phagocytes and epithelial cells in vitro. Infect Immun 67:4367–4375
    [Google Scholar]
  20. Grosdent N., Maridonneau-Parini I., Sory M. P., Cornelis G. R. 2002; Role of Yops and adhesins in resistance of Yersinia enterocolitica to phagocytosis. Infect Immun 70:4165–4176 [CrossRef]
    [Google Scholar]
  21. Howard S. L., Gaunt M. W., Hinds J., Witney A. A., Stabler R., Wren B. W. 2006; Application of comparative phylogenomics to study the evolution of Yersinia enterocolitica and to identify genetic differences relating to pathogenicity. J Bacteriol 188:3645–3653 [CrossRef]
    [Google Scholar]
  22. Iriarte M., Stainier I., Mikulskis A. V., Cornelis G. R. 1995; The flia gene encoding Sigma(28) in Yersinia enterocolitica. J Bacteriol 177:2299–2304
    [Google Scholar]
  23. Kampik D., Schulte R., Autenrieth I. B. 2000; Yersinia enterocolitica invasin protein triggers differential production of interleukin-1, monocyte chemoattractant protein 1, granulocyte-macrophage colony-stimulating factor, and tumour necrosis factor alpha in epithelial cells: implications for understanding the early cytokine network in Yersinia infections. Infect Immun 68:2484–2492 [CrossRef]
    [Google Scholar]
  24. Kaniga K., Delor I., Cornelis G. R. 1991; A wide-host-range suicide vector for improving reverse genetics in Gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109:137–141 [CrossRef]
    [Google Scholar]
  25. Kapatral V., Minnich S. A. 1995; Co-ordinate, temperature-sensitive regulation of the three Yersinia enterocolitica flagellin genes. Mol Microbiol 17:49–56 [CrossRef]
    [Google Scholar]
  26. La Ragione R. M., Cooley W. A., Velge P., Jepson M. A., Woodward M. J. 2003; Membrane ruffling and invasion of human and avian cell lines is reduced for aflagellate mutants of Salmonella enterica serotype Enteriditis. Int J Med Microbiol 293:261–272 [CrossRef]
    [Google Scholar]
  27. McNally A., Cheasty T., Fearnley C., Dalziel R. W., Paiba G., Manning G., Newell D. G. 2004; Comparison of the biotypes of Yersinia enterocolitica isolated from pigs, cattle and sheep at slaughter and from humans with yersiniosis in Great Britain during 1999–2000. Lett Appl Microbiol 39:103–108 [CrossRef]
    [Google Scholar]
  28. McNally A., Dalton T., La Ragione R. M., Stapleton K., Manning G., Newell D. G. 2006; Yersinia enterocolitica isolates of differing biotypes from humans and animals are adherent, invasive and persist in macrophages, but differ in cytokine secretion profiles in vitro. J Med Microbiol 55:1725–1734 [CrossRef]
    [Google Scholar]
  29. Miller V. L., Falkow S. 1988; Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect Immun 56:1242–1248
    [Google Scholar]
  30. Morris J. G., Prado V., Ferreccio C., Robins-Browne R. M., Bordun A., Cayazzo M., Kay B. A., Levine M. M. 1991; Yersinia enterocolitica isolated from two cohorts of young children in Santiago, Chile: incidence of and lack of correlation between illness and propsed virulence factors. J Clin Microbiol 29:2784–2788
    [Google Scholar]
  31. Parke D. 1990; Construction of mobilizable vectors derived from plasmids RP4, pUC18 and pUC19. Gene 93:135–137 [CrossRef]
    [Google Scholar]
  32. Pepe J. C., Miller V. L. 1993; Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc Natl Acad Sci U S A 90:6473–6477 [CrossRef]
    [Google Scholar]
  33. Portnoy D. A., Moseley S. L., Falkow S. 1981; Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Infect Immun 31:775–782
    [Google Scholar]
  34. Rebeil R., Ernst R. K., Gowen B. B., Miller S. I., Hinnebusch B. J. 2004; Variation in lipid A structure in the pathogenic yersiniae. Mol Microbiol 52:1363–1373 [CrossRef]
    [Google Scholar]
  35. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  36. Schmid Y., Grassl G. A., Buhler O. T., Skurnik M., Autenrieth I. B., Bohn E. 2004; Yersinia enterocolitica adhesin A induces production of interleukin-8 in epithelial cells. Infect Immun 72:6780–6789 [CrossRef]
    [Google Scholar]
  37. Schmitt C. K., Darnell S. C., Tesh V. L., Stocker B. A., O'Brien A. D. 1994; Mutation of flgM attenuates virulence of Salmonella Typhimurium, and mutation of fliA represses the attenuated phenotype. J Bacteriol 176:368–377
    [Google Scholar]
  38. Schmitt C. K., Ikeda J. S., Darnell S. C., Watson P. R., Bispham J., Wallis T. S., Weinstein D. L., Metcalf E. S., O'Brien A. D. 2001; Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect Immun 69:5619–5625 [CrossRef]
    [Google Scholar]
  39. Scholz O., Thiel A., Hillen W., Niederweis M. 2000; Quantitative analysis of gene expression with an improved green fluorescent protein. Eur J Biochem 267:1565–1570 [CrossRef]
    [Google Scholar]
  40. Tennant S. M., Grant T. H., Robins-Browne R. M. 2003; Pathogenicity of Yersinia enterocolitica biotype 1A. FEMS Immunol Med Microbiol 38:127–137 [CrossRef]
    [Google Scholar]
  41. Woodcock D. M., Crowther P. J., Doherty J., Jefferson S., DeCruz E., Noyer-Weidner M., Smith S. S., Michael M. Z., Graham M. W. 1989; Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res 17:3469–3478 [CrossRef]
    [Google Scholar]
  42. Wyant T. L., Tanner M. K., Sztein M. B. 1999; Salmonella typhi flagella are potent inducers of proinflammatory cytokine secretion by human monocytes. Infect Immun 67:3619–3624
    [Google Scholar]
  43. Young G. M., Schmiel D. H., Miller V. L. 1999a; A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc Natl Acad Sci U S A 96:6456–6461 [CrossRef]
    [Google Scholar]
  44. Young G. M., Smith M. J., Minnich S. A., Miller V. L. 1999b; The Yersinia enterocolitica motility master regulatory operon, flhDC , is required for flagellin production, swimming motility, and swarming motility. J Bacteriol 181:2823–2833
    [Google Scholar]
  45. Young G. M., Badger J. L., Miller V. L. 2000; Motility is required to initiate host cell invasion by Yersinia enterocolitica. Infect Immun 68:4323–4326 [CrossRef]
    [Google Scholar]
  46. Zhou X., Giron J. A., Torres A. G., Crawford J. A., Negrete E., Vogel S. N., Kaper J. B. 2003; Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 cells. Infect Immun 71:2120–2129 [CrossRef]
    [Google Scholar]
  47. Zumbihl R., Aepfelbacher M., Andor A., Jacobi C. A., Ruckdeschel H., Rouot B., Heesemann J. 1999; The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small GTP-binding protein RhoA. J Biol Chem 274:29289–29293 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/000919-0
Loading
/content/journal/micro/10.1099/mic.0.2006/000919-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error