Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1994 Apr;62(4):1275–1281. doi: 10.1128/iai.62.4.1275-1281.1994

Role of YadA in resistance of Yersinia enterocolitica to phagocytosis by human polymorphonuclear leukocytes.

B China 1, B T N'Guyen 1, M de Bruyere 1, G R Cornelis 1
PMCID: PMC186269  PMID: 8132334

Abstract

Pathogenic Yersinia enterocolitica cells do not induce the chemiluminescence response of human polymorphonuclear leukocytes (PMNs). We tested the chemiluminescence response to Y. enterocolitica mutants affected in the known pYV-encoded factors. We did not detect any influence of the Yops in this phenomenon. By contrast, the presence of YadA correlated with a lack of chemiluminescence. The expression of YadA at the bacterial surface also reduced the phagocytosis by PMNs. Finally, we measured the survival of Y. enterocolitica cells confronted with PMNs by the classical plating method and by a new luminometry assay. We observed that YadA+ bacteria were not killed, while YadA- bacteria were killed. We conclude that the presence of YadA at the surface of Y. enterocolitica cells prevents phagocytosis and killing by PMNs. This conclusion is in good agreement with our recent observation that YadA protects Y. enterocolitica from opsonization by C3b.

Full text

PDF
1275

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allen R. C., Loose L. D. Phagocytic activation of a luminol-dependent chemiluminescence in rabbit alveolar and peritoneal macrophages. Biochem Biophys Res Commun. 1976 Mar 8;69(1):245–252. doi: 10.1016/s0006-291x(76)80299-9. [DOI] [PubMed] [Google Scholar]
  2. Balligand G., Laroche Y., Cornelis G. Genetic analysis of virulence plasmid from a serogroup 9 Yersinia enterocolitica strain: role of outer membrane protein P1 in resistance to human serum and autoagglutination. Infect Immun. 1985 Jun;48(3):782–786. doi: 10.1128/iai.48.3.782-786.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bliska J. B., Clemens J. C., Dixon J. E., Falkow S. The Yersinia tyrosine phosphatase: specificity of a bacterial virulence determinant for phosphoproteins in the J774A.1 macrophage. J Exp Med. 1992 Dec 1;176(6):1625–1630. doi: 10.1084/jem.176.6.1625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bliska J. B., Falkow S. Bacterial resistance to complement killing mediated by the Ail protein of Yersinia enterocolitica. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3561–3565. doi: 10.1073/pnas.89.8.3561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brubaker R. R. Factors promoting acute and chronic diseases caused by yersiniae. Clin Microbiol Rev. 1991 Jul;4(3):309–324. doi: 10.1128/cmr.4.3.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bukholm G., Kapperud G., Skurnik M. Genetic evidence that the yopA gene-encoded Yersinia outer membrane protein Yop1 mediates inhibition of the anti-invasive effect of interferon. Infect Immun. 1990 Jul;58(7):2245–2251. doi: 10.1128/iai.58.7.2245-2251.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cantinieaux B., Hariga C., Courtoy P., Hupin J., Fondu P. Staphylococcus aureus phagocytosis. A new cytofluorometric method using FITC and paraformaldehyde. J Immunol Methods. 1989 Jul 26;121(2):203–208. doi: 10.1016/0022-1759(89)90161-0. [DOI] [PubMed] [Google Scholar]
  8. China B., Michiels T., Cornelis G. R. The pYV plasmid of Yersinia encodes a lipoprotein, YlpA, related to TraT. Mol Microbiol. 1990 Sep;4(9):1585–1593. doi: 10.1111/j.1365-2958.1990.tb02070.x. [DOI] [PubMed] [Google Scholar]
  9. China B., Sory M. P., N'Guyen B. T., De Bruyere M., Cornelis G. R. Role of the YadA protein in prevention of opsonization of Yersinia enterocolitica by C3b molecules. Infect Immun. 1993 Aug;61(8):3129–3136. doi: 10.1128/iai.61.8.3129-3136.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Château M. T., Rabesandratana H., Caravano R. Suspended mouse peritoneal macrophages. Preparation and properties. J Immunol Methods. 1991 Sep 20;143(1):103–109. doi: 10.1016/0022-1759(91)90278-n. [DOI] [PubMed] [Google Scholar]
  11. Cornelis G., Colson C. Restriction of DNA in Yersinia enterocolitica detected by recipient ability for a derepressed R factor from Escherichia coli. J Gen Microbiol. 1975 Apr;87(2):285–291. doi: 10.1099/00221287-87-2-285. [DOI] [PubMed] [Google Scholar]
  12. Cornelis G., Sluiters C., de Rouvroit C. L., Michiels T. Homology between virF, the transcriptional activator of the Yersinia virulence regulon, and AraC, the Escherichia coli arabinose operon regulator. J Bacteriol. 1989 Jan;171(1):254–262. doi: 10.1128/jb.171.1.254-262.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cornelis G., Sory M. P., Laroche Y., Derclaye I. Genetic analysis of the plasmid region controlling virulence in Yersinia enterocolitica 0:9 by Mini-Mu insertions and lac gene fusions. Microb Pathog. 1986 Aug;1(4):349–359. doi: 10.1016/0882-4010(86)90067-7. [DOI] [PubMed] [Google Scholar]
  14. Cornelis G., Vanootegem J. C., Sluiters C. Transcription of the yop regulon from Y. enterocolitica requires trans acting pYV and chromosomal genes. Microb Pathog. 1987 May;2(5):367–379. doi: 10.1016/0882-4010(87)90078-7. [DOI] [PubMed] [Google Scholar]
  15. Emödy L., Heesemann J., Wolf-Watz H., Skurnik M., Kapperud G., O'Toole P., Wadström T. Binding to collagen by Yersinia enterocolitica and Yersinia pseudotuberculosis: evidence for yopA-mediated and chromosomally encoded mechanisms. J Bacteriol. 1989 Dec;171(12):6674–6679. doi: 10.1128/jb.171.12.6674-6679.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Guan K. L., Dixon J. E. Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science. 1990 Aug 3;249(4968):553–556. doi: 10.1126/science.2166336. [DOI] [PubMed] [Google Scholar]
  17. Hart P. D., Young M. R. Interference with normal phagosome-lysosome fusion in macrophages, using ingested yeast cells and suramin. Nature. 1975 Jul 3;256(5512):47–49. doi: 10.1038/256047a0. [DOI] [PubMed] [Google Scholar]
  18. Horstmann R. D., Sievertsen H. J., Knobloch J., Fischetti V. A. Antiphagocytic activity of streptococcal M protein: selective binding of complement control protein factor H. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1657–1661. doi: 10.1073/pnas.85.5.1657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kaniga K., Delor I., Cornelis G. R. A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene. 1991 Dec 20;109(1):137–141. doi: 10.1016/0378-1119(91)90599-7. [DOI] [PubMed] [Google Scholar]
  20. Kaniga K., Sory M. P., Delor I., Saegerman C., Limet J. N., Cornelis G. R. Monitoring of Yersinia enterocolitica in murine and bovine feces on the basis of the chromosomally integrated luxAB marker gene. Appl Environ Microbiol. 1992 Mar;58(3):1024–1026. doi: 10.1128/aem.58.3.1024-1026.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kapperud G., Namork E., Skurnik M., Nesbakken T. Plasmid-mediated surface fibrillae of Yersinia pseudotuberculosis and Yersinia enterocolitica: relationship to the outer membrane protein YOP1 and possible importance for pathogenesis. Infect Immun. 1987 Sep;55(9):2247–2254. doi: 10.1128/iai.55.9.2247-2254.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lachica R. V., Zink D. L., Ferris W. R. Association of fibril structure formation with cell surface properties of Yersinia enterocolitica. Infect Immun. 1984 Oct;46(1):272–275. doi: 10.1128/iai.46.1.272-275.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lambert de Rouvroit C., Sluiters C., Cornelis G. R. Role of the transcriptional activator, VirF, and temperature in the expression of the pYV plasmid genes of Yersinia enterocolitica. Mol Microbiol. 1992 Feb;6(3):395–409. [PubMed] [Google Scholar]
  24. Legocki R. P., Legocki M., Baldwin T. O., Szalay A. A. Bioluminescence in soybean root nodules: Demonstration of a general approach to assay gene expression in vivo by using bacterial luciferase. Proc Natl Acad Sci U S A. 1986 Dec;83(23):9080–9084. doi: 10.1073/pnas.83.23.9080. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lian C. J., Hwang W. S., Pai C. H. Plasmid-mediated resistance to phagocytosis in Yersinia enterocolitica. Infect Immun. 1987 May;55(5):1176–1183. doi: 10.1128/iai.55.5.1176-1183.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lian C. J., Pai C. H. Inhibition of human neutrophil chemiluminescence by plasmid-mediated outer membrane proteins of Yersinia enterocolitica. Infect Immun. 1985 Jul;49(1):145–151. doi: 10.1128/iai.49.1.145-151.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Martinez R. J. Thermoregulation-dependent expression of Yersinia enterocolitica protein 1 imparts serum resistance to Escherichia coli K-12. J Bacteriol. 1989 Jul;171(7):3732–3739. doi: 10.1128/jb.171.7.3732-3739.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Michiels T., Cornelis G. R. Secretion of hybrid proteins by the Yersinia Yop export system. J Bacteriol. 1991 Mar;173(5):1677–1685. doi: 10.1128/jb.173.5.1677-1685.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Michiels T., Vanooteghem J. C., Lambert de Rouvroit C., China B., Gustin A., Boudry P., Cornelis G. R. Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica. J Bacteriol. 1991 Aug;173(16):4994–5009. doi: 10.1128/jb.173.16.4994-5009.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Michiels T., Wattiau P., Brasseur R., Ruysschaert J. M., Cornelis G. Secretion of Yop proteins by Yersiniae. Infect Immun. 1990 Sep;58(9):2840–2849. doi: 10.1128/iai.58.9.2840-2849.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Mulder B., Michiels T., Simonet M., Sory M. P., Cornelis G. Identification of additional virulence determinants on the pYV plasmid of Yersinia enterocolitica W227. Infect Immun. 1989 Aug;57(8):2534–2541. doi: 10.1128/iai.57.8.2534-2541.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Mundi H., Björkstén B., Svanborg C., Ohman L., Dahlgren C. Extracellular release of reactive oxygen species from human neutrophils upon interaction with Escherichia coli strains causing renal scarring. Infect Immun. 1991 Nov;59(11):4168–4172. doi: 10.1128/iai.59.11.4168-4172.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Paerregaard A., Espersen F., Jensen O. M., Skurnik M. Interactions between Yersinia enterocolitica and rabbit ileal mucus: growth, adhesion, penetration, and subsequent changes in surface hydrophobicity and ability to adhere to ileal brush border membrane vesicles. Infect Immun. 1991 Jan;59(1):253–260. doi: 10.1128/iai.59.1.253-260.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pierson D. E., Falkow S. The ail gene of Yersinia enterocolitica has a role in the ability of the organism to survive serum killing. Infect Immun. 1993 May;61(5):1846–1852. doi: 10.1128/iai.61.5.1846-1852.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Pilz D., Vocke T., Heesemann J., Brade V. Mechanism of YadA-mediated serum resistance of Yersinia enterocolitica serotype O3. Infect Immun. 1992 Jan;60(1):189–195. doi: 10.1128/iai.60.1.189-195.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Plano G. V., Barve S. S., Straley S. C. LcrD, a membrane-bound regulator of the Yersinia pestis low-calcium response. J Bacteriol. 1991 Nov;173(22):7293–7303. doi: 10.1128/jb.173.22.7293-7303.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rosqvist R., Bölin I., Wolf-Watz H. Inhibition of phagocytosis in Yersinia pseudotuberculosis: a virulence plasmid-encoded ability involving the Yop2b protein. Infect Immun. 1988 Aug;56(8):2139–2143. doi: 10.1128/iai.56.8.2139-2143.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schulze-Koops H., Burkhardt H., Heesemann J., von der Mark K., Emmrich F. Plasmid-encoded outer membrane protein YadA mediates specific binding of enteropathogenic yersiniae to various types of collagen. Infect Immun. 1992 Jun;60(6):2153–2159. doi: 10.1128/iai.60.6.2153-2159.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Skurnik M., Bölin I., Heikkinen H., Piha S., Wolf-Watz H. Virulence plasmid-associated autoagglutination in Yersinia spp. J Bacteriol. 1984 Jun;158(3):1033–1036. doi: 10.1128/jb.158.3.1033-1036.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Skurnik M., Toivanen P. Yersinia enterocolitica lipopolysaccharide: genetics and virulence. Trends Microbiol. 1993 Jul;1(4):148–152. doi: 10.1016/0966-842x(93)90130-j. [DOI] [PubMed] [Google Scholar]
  41. Skurnik M., Wolf-Watz H. Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp. Mol Microbiol. 1989 Apr;3(4):517–529. doi: 10.1111/j.1365-2958.1989.tb00198.x. [DOI] [PubMed] [Google Scholar]
  42. Smith D. L., Rommel F. A rapid micro method for the simultaneous determination of phagocytic-microbiocidal activity of human peripheral blood leukocytes in vitro. J Immunol Methods. 1977;17(3-4):241–247. doi: 10.1016/0022-1759(77)90106-5. [DOI] [PubMed] [Google Scholar]
  43. Straley S. C., Skrzypek E., Plano G. V., Bliska J. B. Yops of Yersinia spp. pathogenic for humans. Infect Immun. 1993 Aug;61(8):3105–3110. doi: 10.1128/iai.61.8.3105-3110.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Tertti R., Eerola E., Lehtonen O. P., Ståhlberg T. H., Viander M., Toivanen A. Virulence-plasmid is associated with the inhibition of opsonization in Yersinia enterocolitica and Yersinia pseudotuberculosis. Clin Exp Immunol. 1987 May;68(2):266–274. [PMC free article] [PubMed] [Google Scholar]
  45. Tertti R., Skurnik M., Vartio T., Kuusela P. Adhesion protein YadA of Yersinia species mediates binding of bacteria to fibronectin. Infect Immun. 1992 Jul;60(7):3021–3024. doi: 10.1128/iai.60.7.3021-3024.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Zaleska M., Lounatmaa K., Nurminen M., Wahlström E., Mäkelä P. H. A novel virulence-associated cell surface structure composed of 47-kd protein subunits in Yersinia enterocolitica. EMBO J. 1985 Apr;4(4):1013–1018. doi: 10.1002/j.1460-2075.1985.tb03732.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES