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. 1995 Dec;63(12):4837–4848. doi: 10.1128/iai.63.12.4837-4848.1995

Pathogenesis of defined invasion mutants of Yersinia enterocolitica in a BALB/c mouse model of infection.

J C Pepe 1, M R Wachtel 1, E Wagar 1, V L Miller 1
PMCID: PMC173693  PMID: 7591144

Abstract

It has been hypothesized for many years that the ability of Yersinia spp. to invade tissue culture cells is reflective of their ability to penetrate the intestinal epithelium and that this capacity is an important aspect of the disease process. Three different genes from Yersinia spp. that are involved in the tissue culture invasion phenotype have been identified: inv, ail, and yadA. It was previously shown that inv is necessary for efficient penetration of the intestinal epithelium by Yersinia enterocolitica. The present study was initiated to determine whether other known Yersinia invasion factors could promote uptake of the bacteria by mice in the absence of invasion. In addition, the roles of these three invasion factors in the survival of the bacteria, lethality for mice, and development of pathology were compared. We found that YadA is necessary for persistence of Y. enterocolitica in Peyer's patches, and consistent with this observation, the yadA mutant was avirulent for mice infected either orally or intraperitoneally. In addition, the inv yadA double mutant was avirulent. Histological and immunohistological examination of the Peyer's patches of infected mice indicated that despite the presence of large numbers of CFU at 24 h the yadA and ail yadA mutants cause only minimal pathology and recruitment of macrophages. At 42 h postinfection, Peyer's patches from mice infected with the inv mutant showed no pathology, despite the prediction that some of the mice by this time would be colonized. However, at 72 h, inflammation and necrosis were evident in some Peyer's patches. Together, these observations suggest that for visible pathology to develop, a threshold number of bacteria (> 10(5)) is needed and the bacteria need to persist for more than 24 h. Lastly, YadA but not Ail may play a role in the less efficient, delayed invasion of the intestinal epithelium observed for the inv mutant.

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Selected References

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  1. Autenrieth I. B., Beer M., Bohn E., Kaufmann S. H., Heesemann J. Immune responses to Yersinia enterocolitica in susceptible BALB/c and resistant C57BL/6 mice: an essential role for gamma interferon. Infect Immun. 1994 Jun;62(6):2590–2599. doi: 10.1128/iai.62.6.2590-2599.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Autenrieth I. B., Beer M., Hantschmann P., Preger S., Vogel U., Heymer B., Heesemann J. The cellular immune response against Yersinia enterocolitica in different inbred strains of mice: evidence for an important role of T lymphocytes. Zentralbl Bakteriol. 1993 Apr;278(2-3):383–395. doi: 10.1016/s0934-8840(11)80855-8. [DOI] [PubMed] [Google Scholar]
  3. Autenrieth I. B., Hantschmann P., Heymer B., Heesemann J. Immunohistological characterization of the cellular immune response against Yersinia enterocolitica in mice: evidence for the involvement of T lymphocytes. Immunobiology. 1993 Jan;187(1-2):1–16. doi: 10.1016/S0171-2985(11)80241-X. [DOI] [PubMed] [Google Scholar]
  4. Autenrieth I. B., Heesemann J. In vivo neutralization of tumor necrosis factor-alpha and interferon-gamma abrogates resistance to Yersinia enterocolitica infection in mice. Med Microbiol Immunol. 1992;181(6):333–338. doi: 10.1007/BF00191545. [DOI] [PubMed] [Google Scholar]
  5. Autenrieth I. B., Tingle A., Reske-Kunz A., Heesemann J. T lymphocytes mediate protection against Yersinia enterocolitica in mice: characterization of murine T-cell clones specific for Y. enterocolitica. Infect Immun. 1992 Mar;60(3):1140–1149. doi: 10.1128/iai.60.3.1140-1149.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Autenrieth I. B., Vogel U., Preger S., Heymer B., Heesemann J. Experimental Yersinia enterocolitica infection in euthymic and T-cell-deficient athymic nude C57BL/6 mice: comparison of time course, histomorphology, and immune response. Infect Immun. 1993 Jun;61(6):2585–2595. doi: 10.1128/iai.61.6.2585-2595.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bakour R., Balligand G., Laroche Y., Cornelis G., Wauters G. A simple adult-mouse test for tissue invasiveness in Yersinia enterocolitica strains of low experimental virulence. J Med Microbiol. 1985 Apr;19(2):237–246. doi: 10.1099/00222615-19-2-237. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Beer K. B., Miller V. L. Amino acid substitutions in naturally occurring variants of ail result in altered invasion activity. J Bacteriol. 1992 Feb;174(4):1360–1369. doi: 10.1128/jb.174.4.1360-1369.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Berche P. A., Carter P. B. Calcium requirement and virulence of Yersinia enterocolitica. J Med Microbiol. 1982 Aug;15(3):277–284. doi: 10.1099/00222615-15-3-277. [DOI] [PubMed] [Google Scholar]
  11. Bliska J. B., Copass M. C., Falkow S. The Yersinia pseudotuberculosis adhesin YadA mediates intimate bacterial attachment to and entry into HEp-2 cells. Infect Immun. 1993 Sep;61(9):3914–3921. doi: 10.1128/iai.61.9.3914-3921.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Bohn E., Heesemann J., Ehlers S., Autenrieth I. B. Early gamma interferon mRNA expression is associated with resistance of mice against Yersinia enterocolitica. Infect Immun. 1994 Jul;62(7):3027–3032. doi: 10.1128/iai.62.7.3027-3032.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Bottone E. J. Yersinia enterocolitica: a panoramic view of a charismatic microorganism. CRC Crit Rev Microbiol. 1977;5(2):211–241. doi: 10.3109/10408417709102312. [DOI] [PubMed] [Google Scholar]
  15. Bradford W. D., Noce P. S., Gutman L. T. Pathologic features of enteric infection with Yersinia enterocolitica. Arch Pathol. 1974 Jul;98(1):17–22. [PubMed] [Google Scholar]
  16. Bölin I., Wolf-Watz H. Molecular cloning of the temperature-inducible outer membrane protein 1 of Yersinia pseudotuberculosis. Infect Immun. 1984 Jan;43(1):72–78. doi: 10.1128/iai.43.1.72-78.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Carter P. B. Pathogenecity of Yersinia enterocolitica for mice. Infect Immun. 1975 Jan;11(1):164–170. doi: 10.1128/iai.11.1.164-170.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. China B., N'Guyen B. T., de Bruyere M., Cornelis G. R. Role of YadA in resistance of Yersinia enterocolitica to phagocytosis by human polymorphonuclear leukocytes. Infect Immun. 1994 Apr;62(4):1275–1281. doi: 10.1128/iai.62.4.1275-1281.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Cornelis G., Laroche Y., Balligand G., Sory M. P., Wauters G. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev Infect Dis. 1987 Jan-Feb;9(1):64–87. doi: 10.1093/clinids/9.1.64. [DOI] [PubMed] [Google Scholar]
  21. Cover T. L., Aber R. C. Yersinia enterocolitica. N Engl J Med. 1989 Jul 6;321(1):16–24. doi: 10.1056/NEJM198907063210104. [DOI] [PubMed] [Google Scholar]
  22. Dower W. J., Miller J. F., Ragsdale C. W. High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 1988 Jul 11;16(13):6127–6145. doi: 10.1093/nar/16.13.6127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Figurski D. H., Helinski D. R. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1648–1652. doi: 10.1073/pnas.76.4.1648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gripenberg-Lerche C., Skurnik M., Zhang L., Söderström K. O., Toivanen P. Role of YadA in arthritogenicity of Yersinia enterocolitica serotype O:8: experimental studies with rats. Infect Immun. 1994 Dec;62(12):5568–5575. doi: 10.1128/iai.62.12.5568-5575.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Grützkau A., Hanski C., Hahn H., Riecken E. O. Involvement of M cells in the bacterial invasion of Peyer's patches: a common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria. Gut. 1990 Sep;31(9):1011–1015. doi: 10.1136/gut.31.9.1011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hancock G. E., Schaedler R. W., MacDonald T. T. Yersinia enterocolitica infection in resistant and susceptible strains of mice. Infect Immun. 1986 Jul;53(1):26–31. doi: 10.1128/iai.53.1.26-31.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hanski C., Kutschka U., Schmoranzer H. P., Naumann M., Stallmach A., Hahn H., Menge H., Riecken E. O. Immunohistochemical and electron microscopic study of interaction of Yersinia enterocolitica serotype O8 with intestinal mucosa during experimental enteritis. Infect Immun. 1989 Mar;57(3):673–678. doi: 10.1128/iai.57.3.673-678.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hanski C., Naumann M., Grützkau A., Pluschke G., Friedrich B., Hahn H., Riecken E. O. Humoral and cellular defense against intestinal murine infection with Yersinia enterocolitica. Infect Immun. 1991 Mar;59(3):1106–1111. doi: 10.1128/iai.59.3.1106-1111.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hanski C., Naumann M., Hahn H., Riecken E. O. Determinants of invasion and survival of Yersinia enterocolitica in intestinal tissue. An in vivo study. Med Microbiol Immunol. 1989;178(5):289–296. doi: 10.1007/BF00191063. [DOI] [PubMed] [Google Scholar]
  30. Isberg R. R. Determinants for thermoinducible cell binding and plasmid-encoded cellular penetration detected in the absence of the Yersinia pseudotuberculosis invasin protein. Infect Immun. 1989 Jul;57(7):1998–2005. doi: 10.1128/iai.57.7.1998-2005.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Isberg R. R., Falkow S. A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature. 1985 Sep 19;317(6034):262–264. doi: 10.1038/317262a0. [DOI] [PubMed] [Google Scholar]
  32. Isberg R. R., Leong J. M. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell. 1990 Mar 9;60(5):861–871. doi: 10.1016/0092-8674(90)90099-z. [DOI] [PubMed] [Google Scholar]
  33. Isberg R. R., Voorhis D. L., Falkow S. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell. 1987 Aug 28;50(5):769–778. doi: 10.1016/0092-8674(87)90335-7. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Kinder S. A., Badger J. L., Bryant G. O., Pepe J. C., Miller V. L. Cloning of the YenI restriction endonuclease and methyltransferase from Yersinia enterocolitica serotype O8 and construction of a transformable R-M+ mutant. Gene. 1993 Dec 22;136(1-2):271–275. doi: 10.1016/0378-1119(93)90478-l. [DOI] [PubMed] [Google Scholar]
  36. Kolter R., Inuzuka M., Helinski D. R. Trans-complementation-dependent replication of a low molecular weight origin fragment from plasmid R6K. Cell. 1978 Dec;15(4):1199–1208. doi: 10.1016/0092-8674(78)90046-6. [DOI] [PubMed] [Google Scholar]
  37. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Lee W. H., McGrath P. P., Carter P. H., Eide E. L. The ability of some Yersinia enterocolitica strains to invade HeLa cells. Can J Microbiol. 1977 Dec;23(12):1714–1722. doi: 10.1139/m77-247. [DOI] [PubMed] [Google Scholar]
  40. Lian C. J., Hwang W. S., Kelly J. K., Pai C. H. Invasiveness of Yersinia enterocolitica lacking the virulence plasmid: an in-vivo study. J Med Microbiol. 1987 Nov;24(3):219–226. doi: 10.1099/00222615-24-3-219. [DOI] [PubMed] [Google Scholar]
  41. MacDonald T. T., Carter P. B. Isolation and functional characteristics of adherent phagocytic cells from mouse Peyer's patches. Immunology. 1982 Apr;45(4):769–774. [PMC free article] [PubMed] [Google Scholar]
  42. 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]
  43. Mielke M. E., Ehlers S., Hahn H. T-cell subsets in delayed-type hypersensitivity, protection, and granuloma formation in primary and secondary Listeria infection in mice: superior role of Lyt-2+ cells in acquired immunity. Infect Immun. 1988 Aug;56(8):1920–1925. doi: 10.1128/iai.56.8.1920-1925.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Mielke M. E., Niedobitek G., Stein H., Hahn H. Acquired resistance to Listeria monocytogenes is mediated by Lyt-2+ T cells independently of the influx of monocytes into granulomatous lesions. J Exp Med. 1989 Aug 1;170(2):589–594. doi: 10.1084/jem.170.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Miller V. L., Bliska J. B., Falkow S. Nucleotide sequence of the Yersinia enterocolitica ail gene and characterization of the Ail protein product. J Bacteriol. 1990 Feb;172(2):1062–1069. doi: 10.1128/jb.172.2.1062-1069.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Miller V. L., Falkow S. Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect Immun. 1988 May;56(5):1242–1248. doi: 10.1128/iai.56.5.1242-1248.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Miller V. L., Farmer J. J., 3rd, Hill W. E., Falkow S. The ail locus is found uniquely in Yersinia enterocolitica serotypes commonly associated with disease. Infect Immun. 1989 Jan;57(1):121–131. doi: 10.1128/iai.57.1.121-131.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Miller V. L., Mekalanos J. J. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol. 1988 Jun;170(6):2575–2583. doi: 10.1128/jb.170.6.2575-2583.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Näher H., Sperling U., Hahn H. H-2K-restricted granuloma formation by Ly-2+ T cells in antibacterial protection to facultative intracellular bacteria. J Immunol. 1985 Jan;134(1):569–572. [PubMed] [Google Scholar]
  50. Näher H., Sperling U., Takacs L., Hahn H. Dynamics of T cells of L3T4 and Ly 2 phenotype within granulomas in murine listeriosis. Clin Exp Immunol. 1985 Jun;60(3):559–564. [PMC free article] [PubMed] [Google Scholar]
  51. Owen R. L., Pierce N. F., Apple R. T., Cray W. C., Jr M cell transport of Vibrio cholerae from the intestinal lumen into Peyer's patches: a mechanism for antigen sampling and for microbial transepithelial migration. J Infect Dis. 1986 Jun;153(6):1108–1118. doi: 10.1093/infdis/153.6.1108. [DOI] [PubMed] [Google Scholar]
  52. Owen R. L. Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer's patches in the normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology. 1977 Mar;72(3):440–451. [PubMed] [Google Scholar]
  53. Paerregaard A., Espersen F., Skurnik M. Role of the Yersinia outer membrane protein YadA in adhesion to rabbit intestinal tissue and rabbit intestinal brush border membrane vesicles. APMIS. 1991 Mar;99(3):226–232. doi: 10.1111/j.1699-0463.1991.tb05143.x. [DOI] [PubMed] [Google Scholar]
  54. Pai C. H., DeStephano L. Serum resistance associated with virulence in Yersinia enterocolitica. Infect Immun. 1982 Feb;35(2):605–611. doi: 10.1128/iai.35.2.605-611.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Pedersen K. B., Winblad S., Bitsch V. Studies on the interaction between different O-serotypes of Yersinia enterocolitica and HeLa cells. Acta Pathol Microbiol Scand B. 1979 Apr;87B(2):141–145. doi: 10.1111/j.1699-0463.1979.tb02417.x. [DOI] [PubMed] [Google Scholar]
  56. Pepe J. C., Badger J. L., Miller V. L. Growth phase and low pH affect the thermal regulation of the Yersinia enterocolitica inv gene. Mol Microbiol. 1994 Jan;11(1):123–135. doi: 10.1111/j.1365-2958.1994.tb00295.x. [DOI] [PubMed] [Google Scholar]
  57. Pepe J. C., Miller V. L. The Yersinia enterocolitica inv gene product is an outer membrane protein that shares epitopes with Yersinia pseudotuberculosis invasin. J Bacteriol. 1990 Jul;172(7):3780–3789. doi: 10.1128/jb.172.7.3780-3789.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Pepe J. C., Miller V. L. Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6473–6477. doi: 10.1073/pnas.90.14.6473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. 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]
  60. Portnoy D. A., Moseley S. L., Falkow S. Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Infect Immun. 1981 Feb;31(2):775–782. doi: 10.1128/iai.31.2.775-782.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Robins-Browne R. M., Prpic J. K. Effects of iron and desferrioxamine on infections with Yersinia enterocolitica. Infect Immun. 1985 Mar;47(3):774–779. doi: 10.1128/iai.47.3.774-779.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. 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]
  63. Rosqvist R., Forsberg A., Rimpiläinen M., Bergman T., Wolf-Watz H. The cytotoxic protein YopE of Yersinia obstructs the primary host defence. Mol Microbiol. 1990 Apr;4(4):657–667. doi: 10.1111/j.1365-2958.1990.tb00635.x. [DOI] [PubMed] [Google Scholar]
  64. Rosqvist R., Forsberg A., Wolf-Watz H. Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect Immun. 1991 Dec;59(12):4562–4569. doi: 10.1128/iai.59.12.4562-4569.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Rosqvist R., Skurnik M., Wolf-Watz H. Increased virulence of Yersinia pseudotuberculosis by two independent mutations. Nature. 1988 Aug 11;334(6182):522–524. doi: 10.1038/334522a0. [DOI] [PubMed] [Google Scholar]
  66. Schiemann D. A., Devenish J. A. Relationship of HeLa cell infectivity to biochemical, serological, and virulence characteristics of Yersinia enterocolitica. Infect Immun. 1982 Feb;35(2):497–506. doi: 10.1128/iai.35.2.497-506.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Skurnik M. Expression of antigens encoded by the virulence plasmid of Yersinia enterocolitica under different growth conditions. Infect Immun. 1985 Jan;47(1):183–190. doi: 10.1128/iai.47.1.183-190.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Skurnik M., Poikonen K. Experimental intestinal infection of rats by Yersinia enterocolitica 0:3. A follow-up study with specific antibodies to the virulence plasmid specified antigens. Scand J Infect Dis. 1986;18(4):355–364. doi: 10.3109/00365548609032347. [DOI] [PubMed] [Google Scholar]
  69. Tamm A., Tarkkanen A. M., Korhonen T. K., Kuusela P., Toivanen P., Skurnik M. Hydrophobic domains affect the collagen-binding specificity and surface polymerization as well as the virulence potential of the YadA protein of Yersinia enterocolitica. Mol Microbiol. 1993 Dec;10(5):995–1011. doi: 10.1111/j.1365-2958.1993.tb00971.x. [DOI] [PubMed] [Google Scholar]
  70. Une T. Studies on the pathogenicity of Yersinia enterocolitica. I. Experimental infection in rabbits. Microbiol Immunol. 1977;21(7):341–363. [PubMed] [Google Scholar]
  71. Une T. Studies on the pathogenicity of Yersinia enterocolitica. II. Interaction with cultured cells in vitro. Microbiol Immunol. 1977;21(7):365–377. doi: 10.1111/j.1348-0421.1977.tb00301.x. [DOI] [PubMed] [Google Scholar]
  72. Une T. Studies on the pathogenicity of Yersinia enterocolitica. III. Comparative studies between Y. enterocolitica and Y. pseudotuberculosis. Microbiol Immunol. 1977;21(9):505–516. doi: 10.1111/j.1348-0421.1977.tb00316.x. [DOI] [PubMed] [Google Scholar]
  73. Van Nhieu G. T., Isberg R. R. The Yersinia pseudotuberculosis invasin protein and human fibronectin bind to mutually exclusive sites on the alpha 5 beta 1 integrin receptor. J Biol Chem. 1991 Dec 25;266(36):24367–24375. [PubMed] [Google Scholar]
  74. Vantrappen G., Ponette E., Geboes K., Bertrand P. Yersinia enteritis and enterocolitis: gastroenterological aspects. Gastroenterology. 1977 Feb;72(2):220–227. [PubMed] [Google Scholar]
  75. Vesikari T., Sundqvist C., Mäki M. Adherence and toxicity of Yersinia enterocolitica 0:3 and 0:9 containing virulence-associated plasmids for various cultured cells. Acta Pathol Microbiol Immunol Scand B. 1983 Apr;91(2):121–127. doi: 10.1111/j.1699-0463.1983.tb00020.x. [DOI] [PubMed] [Google Scholar]
  76. Wachtel M. R., Miller V. L. In vitro and in vivo characterization of an ail mutant of Yersinia enterocolitica. Infect Immun. 1995 Jul;63(7):2541–2548. doi: 10.1128/iai.63.7.2541-2548.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Walker R. I., Schmauder-Chock E. A., Parker J. L., Burr D. Selective association and transport of Campylobacter jejuni through M cells of rabbit Peyer's patches. Can J Microbiol. 1988 Oct;34(10):1142–1147. doi: 10.1139/m88-201. [DOI] [PubMed] [Google Scholar]
  78. Wassef J. S., Keren D. F., Mailloux J. L. Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect Immun. 1989 Mar;57(3):858–863. doi: 10.1128/iai.57.3.858-863.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Wolf J. L., Rubin D. H., Finberg R., Kauffman R. S., Sharpe A. H., Trier J. S., Fields B. N. Intestinal M cells: a pathway for entry of reovirus into the host. Science. 1981 Apr 24;212(4493):471–472. doi: 10.1126/science.6259737. [DOI] [PubMed] [Google Scholar]
  80. Yang Y., Isberg R. R. Cellular internalization in the absence of invasin expression is promoted by the Yersinia pseudotuberculosis yadA product. Infect Immun. 1993 Sep;61(9):3907–3913. doi: 10.1128/iai.61.9.3907-3913.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Young V. B., Miller V. L., Falkow S., Schoolnik G. K. Sequence, localization and function of the invasin protein of Yersinia enterocolitica. Mol Microbiol. 1990 Jul;4(7):1119–1128. doi: 10.1111/j.1365-2958.1990.tb00686.x. [DOI] [PubMed] [Google Scholar]

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