Abstract
Yersinia enterocolitica is an invasive pathogen capable of causing a wide spectrum of gastrointestinal diseases in man. While there is a considerable body of data on the invasiveness ofY. enterocolitica in vitro, little is known about the events in vivo leading to the translocation of the bacteria from the intestinal lumen into the ileal tissue. There is no detailed ultrastructural information describing the course of infection of pathogenicY. enterocolitica in comparison with an avirulent strain. We compared a virulent plasmid-bearing strain and an isogenic avirulent plasmid-free derivative strain ofY. enterocolitica serotype O∶8 at the ultrastructural level, in the established model of murine yersiniosis. At 12 h postinoculation we found no indications of an active invasion of the intestinal epithelium, although microcolonies of the pathogenic strain were detectable closely under the follicle-associated epithelium of the Peyer's patches. The plasmid-bearing strain ofY. enterocolitica affected the gut-associated lymphoid tissue which was destroyed 36 h post-infection. Unlike the pathogenic strain ofY. enterocolitica, the nonpathogenic plasmid-free strain caused no detectable morphological alterations in the ileal tissue by this time. Morphological evidence is provided thatYersinia does not invade the ileal epithelium in an active manner, as has been observed in vitro, but appears to be transported across the epithelial barrier by M-cells.
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Attwood, SEA, Cafferkey MT, Keane FBV (1989) Yersinia infections in surgical practice. Br J Surg 76:499–504
Ben-Gurion, Shafferman A (1981) Essential virulence determinants of differentYersinia species are carried on a common plasmid. Plasmid 5:183–187
Carter PB (1975) Pathogenicity ofYersinia enterocolitica for mice. Infect Immun 11:164–170
Carter PB, Collins FM (1974) ExperimentalYersinia enterocolitica infection in mice: kinetics of growth. Infect Immun 9:851–857
Cornelis G, Laroche Y, Balligand G, Sory M-P, Wauters G (1987)Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev Infect Dis 9:64–86
Devenish J, Schiemann DA (1981) HeLa cell infection byYersinia enterocolitica: evidence for lack of intracellular multiplication and development of a new procedure for quantitative expression of infectivity. Infect Immun 32:48–55
Falcao DP, Shimizu MT, Trabulsi LR (1984) Kinetics of infection induced byYersinia. Curr Microbiol 11:303–308
Grützkau A. Hanski C, Hahn H, Riecken EO (1990) Involvement of M cells in the bacterial invasion of Peyer's patches: a common mechanism shared byYersinia enterocolitica and other enteroinvasive bacteria. Gut 31:1011–1015
Hanski C, Kutschka U, Schmoranzer HP, Naumann M, Stallmach A, Hahn H, Menge H, Riecken EO (1989a) Immunohistochemical and electron microscopic study of interaction ofYersinia enterocolitica serotype O8 with intestinal mucosa during experimental enteritis. Infect Immun 57:673–678
Hanski C, Naumann M, Hahn H, Riecken EO (1989b) Determinants of invasion and survival ofYersinia enterocolitica in intestinal tissue. Med Microbiol Immunol (Berl) 178:289–296
Hanski C, Naumann M, Grützkau A, Pluschke G, Friedrich B, Hahn H, Riecken EO (1991) Humoral and cellular defense against intestinal murine infection withYersinia enterocolitica. Infect Immun 59:1106–1111
Hartiala K, Granberg I, Toivanen A, Viljanen M (1989) Inhibition of polymorphonuclear leucocyte functions in vivo byYersinia enterocolitica lipopolysaccharide. Ann Rheum Dis 48:42–47
Heesemann J, Laufs R (1985) Double immunofluorescence microscopic technique for accurate differentiation of extracellularly and intracellularly located bacteria in cell culture. J Clin Microbiol 22:168–175
Heesemann J, Keller C, Morawa R, Schmidt N, Siemens HJ, Laufs R (1983) Plasmids of human strains ofYersinia enterocolitica: molecular relatedness and possible importance for pathogenesis. J Infect Dis 147:570–574
Isberg RR, Voorhis DL, Falkow S (1987) Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 50:769–778
Kraehenbuhl J-P, Neutra MR (1992) Molecular and cellular basis of immune protection of mucosal surfaces. Physiol Rev 72:853–879
Lee WH, McGrath PP, Carter PH, Eide EL (1977) The ability of someYersinia enterocolitica strains to invade HeLa cells. Can J Microbiol 23:1714–1722
Lian C-J, Pai CH (1985) Inhibition of human neutrophil chemiluminescence by plasmid-mediated outer membrane proteins ofYersinia enterocolitica. Infect Immun 49:145–151
Lian C-J, Hwang WS, Pai CH (1987) Invasiveness ofYersinia enterocolitica lacking the virulence plasmid: an in-vivo study. J Med Microbiol 24:219–226
Miller VL, Falkow S (1988) Evidence for two genetic loci inYersinia enterocolitica that can promote invasion of epithelial cells. Infect Immun 56:1242–1248
Miller VL, Finlay BB, Falkow S (1988) Factors essential for the penetration of mammalian cells byYersinia. Cur Top Microbiol Immunol 138:15–39
Miller VL, Farmer JJ III, Hill WE, Falkow S (1989) Theail locus is found uniquely inYersinia enterocolitica serotypes commonly associated with disease. Infect Immun 57:121–131
Nation JL (1983) A new method using hexamethyldisilazane (HMDS) for preparation of soft insect tissues for scanning electron microscopy. Stain Technol 58:39–48
Owen RL, Pierce NF, Apple RT, Cray WC (1986) M cell transport ofVibrio cholerae from the intestinal lumen into Peyer's patches: a mechanism for antigen sampling and for microbial transepithelial migration. J Infect Dis 153:1108–1118
Pai CH, Mors V, Seemayer Ta (1980) ExperimentalYersinia enterocolitica enteritis in rabbits. Infect Immun 28:238–244
Pappo J, Steger HJ, Owen RL (1988) Differential adherence of epithelium overlying gut-associated lymphoid tissue. Lab Invest 58:692–697
Portnoy DA, Martinez RJ (1985) Role of a plasmid in the pathogenicity ofYersinia species. Curr Top Microbiol Immunol 118:29–51
Robins-Browne RM, Tzipori S, Gonis G, Hayes J, Withers M, Prpic JK (1985) The pathogenesis ofYersinia enterocolitica infection in gnotobiotic piglets. J Med Microbiol 19:297–308
Rosqvist R, Bölin I, Wolf-Watz H (1988) Inhibition of phagocytosis inYersinia pseudotuberculosis: a virulence plasmid-encoded ability involving the Yop2b protein. Infect Immun 56:2139–2143
Simonet M, Falkow S (1992) Invasin expression inYersinia pseudotuberculosis. Infect Immun 60:4414–4417
Sneller MC, Strober W (1986) M cell and host defense. J Infect Dis 154:737–741
Une T (1977a) Studies on the pathogenicity ofYersinia enterocolitica. I. Experimental infection in rabbits. Microbiol Immunol 21:349–363
Une T (1977b) Studies on the pathogenicity ofYersinia enterocolitica: interaction with cultured cells in vitro. Microbiol Immunol 21:365–377
Vantrappen G, Agg HO, Ponette E, Geboes K, Bertrand P (1977)Yersinia enteritis and enterocolitis: gastroenterological aspects. Gastroenterology 72:220–227
Vesikari T, Bromirska J, Mäki M (1982) Enhancement of invasiveness ofYersinia enterocolitica andEscherichia coli in HEp-2 cells by centrifugation. Infect Immun 36:834–836
Walker RI, Schmauder-Chock EA, Parker JL (1988) Selective association and transport ofCampylobacter jejuni through M cells of rabbit Peyer's patches. Can J Microbiol 34:1142–1147
Wassef JS, Keren DF, Mailloux JL (1989) Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of Shigellosis. Infect Immun 57:858–863
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Grützkau, A., Hanski, C. & Naumann, M. Comparative study of histopathological alterations during intestinal infection of mice with pathogenic and non-pathogenic strains ofYersinia enterocolitica serotype O:8. Vichows Archiv A Pathol Anat 423, 97–103 (1993). https://doi.org/10.1007/BF01606583
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DOI: https://doi.org/10.1007/BF01606583