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. 1997 Feb;65(2):531–536. doi: 10.1128/iai.65.2.531-536.1997

Escherichia coli K5 capsule expression enhances colonization of the large intestine in the gnotobiotic rat.

M V Hérias 1, T Midtvedt 1, L A Hanson 1, A E Wold 1
PMCID: PMC176092  PMID: 9009309

Abstract

The role of capsule expression in the capacity of Escherichia coli to colonize in the large intestinal environment was studied in a gnotobiotic rat model. The rats were given perorally a mixture of two mutant strains differing in K5 expression. After 2 weeks, the rats were sacrificed, and subsequently intestinal contents, intestinal mucosae, and mesenteric lymph nodes were homogenized and bacterial numbers were quantified. Two E. coli mutant pairs were used, the first pair (972-998) lacking the O-specific side chain and the second pair (973-997) carrying the O75 lipopolysaccharide. The K5+ mutants established themselves at a higher level than the K5- mutants (10(9) versus 10(6) CFU/g [P < 0.001] for the first pair and 10(9) versus 10(8) CFU/g [P < 0.01] for the second pair, respectively). The results were confirmed by serology showing a K5+ phenotype for practically all isolates. The bacterial population associated with the mucosa was similar to that in the luminal contents with respect to the proportions of the respective mutants, and translocation occurred in numbers proportional to the intestinal population densities of the respective mutants. All mutants were able to express type 1 as well as P fimbriae. After colonization, the expression of P fimbriae remained high whereas only a minority of the isolates expressed type 1 fimbriae. The results suggest that capsule expression and P fimbriae enhance intestinal colonization by E. coli and that these virulence factors, by increasing bacterial densities in the intestine, secondarily increase translocation.

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Selected References

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  1. Adlerberth I., Hanson L. A., Svanborg C., Svennerholm A. M., Nordgren S., Wold A. E. Adhesins of Escherichia coli associated with extra-intestinal pathogenicity confer binding to colonic epithelial cells. Microb Pathog. 1995 Jun;18(6):373–385. doi: 10.1006/mpat.1995.0034. [DOI] [PubMed] [Google Scholar]
  2. Berg R. D., Garlington A. W. Translocation of certain indigenous bacteria from the gastrointestinal tract to the mesenteric lymph nodes and other organs in a gnotobiotic mouse model. Infect Immun. 1979 Feb;23(2):403–411. doi: 10.1128/iai.23.2.403-411.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boulnois G. J., Roberts I. S. Genetics of capsular polysaccharide production in bacteria. Curr Top Microbiol Immunol. 1990;150:1–18. doi: 10.1007/978-3-642-74694-9_1. [DOI] [PubMed] [Google Scholar]
  4. Cohen P. S., Rossoll R., Cabelli V. J., Yang S. L., Laux D. C. Relationship between the mouse colonizing ability of a human fecal Escherichia coli strain and its ability to bind a specific mouse colonic mucous gel protein. Infect Immun. 1983 Apr;40(1):62–69. doi: 10.1128/iai.40.1.62-69.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cottagnoud P., Tomasz A. Triggering of pneumococcal autolysis by lysozyme. J Infect Dis. 1993 Mar;167(3):684–690. doi: 10.1093/infdis/167.3.684. [DOI] [PubMed] [Google Scholar]
  6. Cross A. S. The biologic significance of bacterial encapsulation. Curr Top Microbiol Immunol. 1990;150:87–95. doi: 10.1007/978-3-642-74694-9_5. [DOI] [PubMed] [Google Scholar]
  7. Dahlgren U., Ahlstedt S., Andersson T., Hedman L., Hanson L. A. IgA antibodies in rat bile are not solely derived from thoracic duct lymph. Scand J Immunol. 1983 Jun;17(6):569–574. doi: 10.1111/j.1365-3083.1983.tb00825.x. [DOI] [PubMed] [Google Scholar]
  8. De Man P., Jodal U., Van Kooten C., Svanborg C. Bacterial adherence as a virulence factor in urinary tract infection. APMIS. 1990 Dec;98(12):1053–1060. doi: 10.1111/j.1699-0463.1990.tb05034.x. [DOI] [PubMed] [Google Scholar]
  9. Friman V., Adlerberth I., Connell H., Svanborg C., Hanson L. A., Wold A. E. Decreased expression of mannose-specific adhesins by Escherichia coli in the colonic microflora of immunoglobulin A-deficient individuals. Infect Immun. 1996 Jul;64(7):2794–2798. doi: 10.1128/iai.64.7.2794-2798.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fubara E. S., Freter R. Source and protective function of coproantibodies in intestinal disease. Am J Clin Nutr. 1972 Dec;25(12):1357–1363. doi: 10.1093/ajcn/25.12.1357. [DOI] [PubMed] [Google Scholar]
  11. GUSTAFSSON B. E. Lightweight stainless steel systems for rearing germfree animals. Ann N Y Acad Sci. 1959 May 8;78:17–28. doi: 10.1111/j.1749-6632.1959.tb53092.x. [DOI] [PubMed] [Google Scholar]
  12. Herías M. V., Midtvedt T., Hanson L. A., Wold A. E. Role of Escherichia coli P fimbriae in intestinal colonization in gnotobiotic rats. Infect Immun. 1995 Dec;63(12):4781–4789. doi: 10.1128/iai.63.12.4781-4789.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Holmgren J., Eggertsen G., Hanson L. A., Lincoln K. Immunodiffusion studies on Escherichia coli. 1. Identification of O, K and H antigens in an O6 strain. Acta Pathol Microbiol Scand. 1969;76(2):304–318. [PubMed] [Google Scholar]
  14. Kaijser B., Jodal U. Escherichia coli K5 antigen in relation to various infections and in healthy individuals. J Clin Microbiol. 1984 Feb;19(2):264–266. doi: 10.1128/jcm.19.2.264-266.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Krogfelt K. A., McCormick B. A., Burghoff R. L., Laux D. C., Cohen P. S. Expression of Escherichia coli F-18 type 1 fimbriae in the streptomycin-treated mouse large intestine. Infect Immun. 1991 Apr;59(4):1567–1568. doi: 10.1128/iai.59.4.1567-1568.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kunin C. M., Polyak F., Postel E. Periurethral bacterial flora in women. Prolonged intermittent colonization with Escherichia coli. JAMA. 1980 Jan 11;243(2):134–139. [PubMed] [Google Scholar]
  17. Lambert-Zechovsky N., Bingen E., Denamur E., Brahimi N., Brun P., Mathieu H., Elion J. Molecular analysis provides evidence for the endogenous origin of bacteremia and meningitis due to Enterobacter cloacae in an infant. Clin Infect Dis. 1992 Jul;15(1):30–32. doi: 10.1093/clinids/15.1.30. [DOI] [PubMed] [Google Scholar]
  18. Laux D. C., McSweegan E. F., Williams T. J., Wadolkowski E. A., Cohen P. S. Identification and characterization of mouse small intestine mucosal receptors for Escherichia coli K-12(K88ab). Infect Immun. 1986 Apr;52(1):18–25. doi: 10.1128/iai.52.1.18-25.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Levin B. R., Svanborg Edén C. Selection and evolution of virulence in bacteria: an ecumenical excursion and modest suggestion. Parasitology. 1990;100 (Suppl):S103–S115. doi: 10.1017/s0031182000073054. [DOI] [PubMed] [Google Scholar]
  20. Lidin-Janson G., Falsen E., Jodal U., Kaijser B., Lincoln K. Characteristics of antibiotic-resistant Escherichia coli in the rectum of healthy school-children. J Med Microbiol. 1977 Aug;10(3):299–308. doi: 10.1099/00222615-10-3-299. [DOI] [PubMed] [Google Scholar]
  21. Lincoln K., Lidin-Janson G., Winberg J. Resistant urinary infections resulting from changes in resistance pattern of faecal flora induced by sulphonamide and hospital environment. Br Med J. 1970 Aug 8;3(5718):305–309. doi: 10.1136/bmj.3.5718.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Morris K. M., Colten H. R., Bing D. H. The first component of complement. A quantitative comparison of its biosynthesis in culture by human epithelial and mesenchymal cells. J Exp Med. 1978 Oct 1;148(4):1007–1019. doi: 10.1084/jem.148.4.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Moxon E. R., Kroll J. S. The role of bacterial polysaccharide capsules as virulence factors. Curr Top Microbiol Immunol. 1990;150:65–85. doi: 10.1007/978-3-642-74694-9_4. [DOI] [PubMed] [Google Scholar]
  24. Orskov I., Orskov F. Escherichia coli in extra-intestinal infections. J Hyg (Lond) 1985 Dec;95(3):551–575. doi: 10.1017/s0022172400060678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Perlmutter D. H., Daniels J. D., Auerbach H. S., De Schryver-Kecskemeti K., Winter H. S., Alpers D. H. The alpha 1-antitrypsin gene is expressed in a human intestinal epithelial cell line. J Biol Chem. 1989 Jun 5;264(16):9485–9490. [PubMed] [Google Scholar]
  26. Plos K., Connell H., Jodal U., Marklund B. I., Mårild S., Wettergren B., Svanborg C. Intestinal carriage of P fimbriated Escherichia coli and the susceptibility to urinary tract infection in young children. J Infect Dis. 1995 Mar;171(3):625–631. doi: 10.1093/infdis/171.3.625. [DOI] [PubMed] [Google Scholar]
  27. Poulsen L. K., Licht T. R., Rang C., Krogfelt K. A., Molin S. Physiological state of Escherichia coli BJ4 growing in the large intestines of streptomycin-treated mice. J Bacteriol. 1995 Oct;177(20):5840–5845. doi: 10.1128/jb.177.20.5840-5845.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Robbins J. B., McCracken G. H., Jr, Gotschlich E. C., Orskov F., Orskov I., Hanson L. A. Escherichia coli K1 capsular polysaccharide associated with neonatal meningitis. N Engl J Med. 1974 May 30;290(22):1216–1220. doi: 10.1056/NEJM197405302902202. [DOI] [PubMed] [Google Scholar]
  29. SEARS H. J., BROWNLEE I. Further observations on the persistence of individual strains of Escherichia coli in the intestinal tract of man. J Bacteriol. 1952 Jan;63(1):47–57. doi: 10.1128/jb.63.1.47-57.1952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. SEARS H. J., BROWNLEE I., UCHIYAMA J. K. Persistence of individual strains of Escherichia coli in the intestinal tract of man. J Bacteriol. 1950 Feb;59(2):293–301. doi: 10.1128/jb.59.2.293-301.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. SEARS H. J., JANES H., SALOUM R., BROWNLEE I., LAMOREAUX L. F. Persistence of individual strains of Escherichia coli in man and dog under varying conditions. J Bacteriol. 1956 Mar;71(3):370–372. doi: 10.1128/jb.71.3.370-372.1956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sarff L. D., McCracken G. H., Schiffer M. S., Glode M. P., Robbins J. B., Orskov I., Orskov F. Epidemiology of Escherichia coli K1 in healthy and diseased newborns. Lancet. 1975 May 17;1(7916):1099–1104. doi: 10.1016/s0140-6736(75)92496-4. [DOI] [PubMed] [Google Scholar]
  33. Steffen E. K., Berg R. D. Relationship between cecal population levels of indigenous bacteria and translocation to the mesenteric lymph nodes. Infect Immun. 1983 Mar;39(3):1252–1259. doi: 10.1128/iai.39.3.1252-1259.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Svanborg Edén C., Hull R., Falkow S., Leffler H. Target cell specificity of wild-type E. coli and mutants and clones with genetically defined adhesins. Prog Food Nutr Sci. 1983;7(3-4):75–89. [PubMed] [Google Scholar]
  35. Svanborg-Edén C., Hagberg L., Hull R., Hull S., Magnusson K. E., Ohman L. Bacterial virulence versus host resistance in the urinary tracts of mice. Infect Immun. 1987 May;55(5):1224–1232. doi: 10.1128/iai.55.5.1224-1232.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tancrède C. H., Andremont A. O. Bacterial translocation and gram-negative bacteremia in patients with hematological malignancies. J Infect Dis. 1985 Jul;152(1):99–103. doi: 10.1093/infdis/152.1.99. [DOI] [PubMed] [Google Scholar]
  37. Tullus K., Kühn I., Orskov I., Orskov F., Möllby R. The importance of P and type 1 fimbriae for the persistence of Escherichia coli in the human gut. Epidemiol Infect. 1992 Jun;108(3):415–421. doi: 10.1017/s095026880004992x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Vann W. F., Schmidt M. A., Jann B., Jann K. The structure of the capsular polysaccharide (K5 antigen) of urinary-tract-infective Escherichia coli 010:K5:H4. A polymer similar to desulfo-heparin. Eur J Biochem. 1981 May 15;116(2):359–364. doi: 10.1111/j.1432-1033.1981.tb05343.x. [DOI] [PubMed] [Google Scholar]
  39. Wells C. L., Maddaus M. A., Simmons R. L. Proposed mechanisms for the translocation of intestinal bacteria. Rev Infect Dis. 1988 Sep-Oct;10(5):958–979. doi: 10.1093/clinids/10.5.958. [DOI] [PubMed] [Google Scholar]
  40. Wessels M. R., Bronze M. S. Critical role of the group A streptococcal capsule in pharyngeal colonization and infection in mice. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):12238–12242. doi: 10.1073/pnas.91.25.12238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wold A. E., Caugant D. A., Lidin-Janson G., de Man P., Svanborg C. Resident colonic Escherichia coli strains frequently display uropathogenic characteristics. J Infect Dis. 1992 Jan;165(1):46–52. doi: 10.1093/infdis/165.1.46. [DOI] [PubMed] [Google Scholar]
  42. Wold A. E., Mestecky J., Tomana M., Kobata A., Ohbayashi H., Endo T., Edén C. S. Secretory immunoglobulin A carries oligosaccharide receptors for Escherichia coli type 1 fimbrial lectin. Infect Immun. 1990 Sep;58(9):3073–3077. doi: 10.1128/iai.58.9.3073-3077.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

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