Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1992 Aug;60(8):3193–3200. doi: 10.1128/iai.60.8.3193-3200.1992

Adhesion of Salmonella typhimurium to porcine intestinal epithelial surfaces: identification and characterization of two phenotypes.

R E Isaacson 1, M Kinsel 1
PMCID: PMC257301  PMID: 1639489

Abstract

Salmonella typhimurium 798 is known to persistently colonize swine. A key step required to initiate colonization of intestines is adhesion of the organism to the intestinal epithelium. However, S. typhimurium 798 initially failed to attach to porcine enterocytes in vitro. An enrichment procedure was used to select adhesive S. typhimurium, and when cells of one colony type were grown in tryptone phosphate broth they were adhesive. Cells from a colony with a different morphology were not adhesive. Adhesion was time dependent, with maximal adhesion occurring at 1 h. As determined by electron microscopy, cells of the adhesive phenotype had pili while none of the cells with the nonadhesive phenotype produced pili. The pili on the adhesive cells were morphologically similar to type 1 pili. Mannose (0.5%) did not affect adhesion, suggesting that the adhesin on strain 798 did not recognize mannose as a receptor. An analysis of envelope proteins from cells of both phenotypes showed that the adhesive-phenotype cells expressed at least 10 unique proteins ranging in size from 20 to 60 kDa. Absorbed antiserum against cells of the adhesive phenotype agglutinated adhesive cells and was used to detect unique surface antigens on the cells of the adhesive phenotype by Western blots (immunoblots). These antigens were in the range of 30 kDa in size. An envelope extract competitively inhibited the binding of S. typhimurium to enterocytes, as did Fab fragments prepared from the absorbed serum. Cells of both phenotypes contained two plasmids, and each had identical restriction digestion patterns. Cells of the adhesive phenotype consistently were found to be more readily phagocytosed by pig leukocytes, and once in the phagocytes they survived better than cells of the nonadhesive phenotype.

Full text

PDF
3193

Images in this article

Selected References

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

  1. Collinson S. K., Emödy L., Müller K. H., Trust T. J., Kay W. W. Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J Bacteriol. 1991 Aug;173(15):4773–4781. doi: 10.1128/jb.173.15.4773-4781.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Duguid J. P., Darekar M. R., Wheater D. W. Fimbriae and infectivity in Salmonella typhimurium. J Med Microbiol. 1976 Nov;9(4):459–473. doi: 10.1099/00222615-9-4-459. [DOI] [PubMed] [Google Scholar]
  3. Ernst R. K., Dombroski D. M., Merrick J. M. Anaerobiosis, type 1 fimbriae, and growth phase are factors that affect invasion of HEp-2 cells by Salmonella typhimurium. Infect Immun. 1990 Jun;58(6):2014–2016. doi: 10.1128/iai.58.6.2014-2016.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Finlay B. B., Heffron F., Falkow S. Epithelial cell surfaces induce Salmonella proteins required for bacterial adherence and invasion. Science. 1989 Feb 17;243(4893):940–943. doi: 10.1126/science.2919285. [DOI] [PubMed] [Google Scholar]
  5. Gahring L. C., Heffron F., Finlay B. B., Falkow S. Invasion and replication of Salmonella typhimurium in animal cells. Infect Immun. 1990 Feb;58(2):443–448. doi: 10.1128/iai.58.2.443-448.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Galán J. E., Curtiss R., 3rd Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect Immun. 1990 Jun;58(6):1879–1885. doi: 10.1128/iai.58.6.1879-1885.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Groisman E. A., Chiao E., Lipps C. J., Heffron F. Salmonella typhimurium phoP virulence gene is a transcriptional regulator. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7077–7081. doi: 10.1073/pnas.86.18.7077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gulig P. A. Virulence plasmids of Salmonella typhimurium and other salmonellae. Microb Pathog. 1990 Jan;8(1):3–11. doi: 10.1016/0882-4010(90)90003-9. [DOI] [PubMed] [Google Scholar]
  9. Isaacson R. E., Fusco P. C., Brinton C. C., Moon H. W. In vitro adhesion of Escherichia coli to porcine small intestinal epithelial cells: pili as adhesive factors. Infect Immun. 1978 Aug;21(2):392–397. doi: 10.1128/iai.21.2.392-397.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Isaacson R. E., Nagy B., Moon H. W. Colonization of porcine small intestine by Escherichia coli: colonization and adhesion factors of pig enteropathogens that lack K88. J Infect Dis. 1977 Apr;135(4):531–539. doi: 10.1093/infdis/135.4.531. [DOI] [PubMed] [Google Scholar]
  11. Ish-Horowicz D., Burke J. F. Rapid and efficient cosmid cloning. Nucleic Acids Res. 1981 Jul 10;9(13):2989–2998. doi: 10.1093/nar/9.13.2989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jones G. W., Rabert D. K., Svinarich D. M., Whitfield H. J. Association of adhesive, invasive, and virulent phenotypes of Salmonella typhimurium with autonomous 60-megadalton plasmids. Infect Immun. 1982 Nov;38(2):476–486. doi: 10.1128/iai.38.2.476-486.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jones G. W., Richardson L. A. The attachment to, and invasion of HeLa cells by Salmonella typhimurium: the contribution of mannose-sensitive and mannose-resistant haemagglutinating activities. J Gen Microbiol. 1981 Dec;127(2):361–370. doi: 10.1099/00221287-127-2-361. [DOI] [PubMed] [Google Scholar]
  14. Jones G. W., Rutter J. M. The association of K88 antigen with haemagglutinating activity in porcine strains of Escherichia coli. J Gen Microbiol. 1974 Sep;84(1):135–144. doi: 10.1099/00221287-84-1-135. [DOI] [PubMed] [Google Scholar]
  15. Kier L. D., Weppelman R. M., Ames B. N. Regulation of nonspecific acid phosphatase in Salmonella: phoN and phoP genes. J Bacteriol. 1979 Apr;138(1):155–161. doi: 10.1128/jb.138.1.155-161.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Korhonen T. K., Lounatmaa K., Ranta H., Kuusi N. Characterization of type 1 pili of Salmonella typhimurium LT2. J Bacteriol. 1980 Nov;144(2):800–805. doi: 10.1128/jb.144.2.800-805.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lee C. A., Falkow S. The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4304–4308. doi: 10.1073/pnas.87.11.4304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Levisohn R., Konisky J., Nomura M. Interaction of colicins with bacterial cells. IV. Immunity breakdown studied with colicins Ia and Ib. J Bacteriol. 1968 Sep;96(3):811–821. doi: 10.1128/jb.96.3.811-821.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lindquist B. L., Lebenthal E., Lee P. C., Stinson M. W., Merrick J. M. Adherence of Salmonella typhimurium to small-intestinal enterocytes of the rat. Infect Immun. 1987 Dec;55(12):3044–3050. doi: 10.1128/iai.55.12.3044-3050.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lugtenberg B., Meijers J., Peters R., van der Hoek P., van Alphen L. Electrophoretic resolution of the "major outer membrane protein" of Escherichia coli K12 into four bands. FEBS Lett. 1975 Oct 15;58(1):254–258. doi: 10.1016/0014-5793(75)80272-9. [DOI] [PubMed] [Google Scholar]
  21. Müller K. H., Collinson S. K., Trust T. J., Kay W. W. Type 1 fimbriae of Salmonella enteritidis. J Bacteriol. 1991 Aug;173(15):4765–4772. doi: 10.1128/jb.173.15.4765-4772.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Old D. C. Inhibition of the interaction between fimbrial haemagglutinins and erythrocytes by D-mannose and other carbohydrates. J Gen Microbiol. 1972 Jun;71(1):149–157. doi: 10.1099/00221287-71-1-149. [DOI] [PubMed] [Google Scholar]
  23. PORTER R. R. The hydrolysis of rabbit y-globulin and antibodies with crystalline papain. Biochem J. 1959 Sep;73:119–126. doi: 10.1042/bj0730119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Purcell B. K., Pruckler J., Clegg S. Nucleotide sequences of the genes encoding type 1 fimbrial subunits of Klebsiella pneumoniae and Salmonella typhimurium. J Bacteriol. 1987 Dec;169(12):5831–5834. doi: 10.1128/jb.169.12.5831-5834.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schiemann D. A., Shope S. R. Anaerobic growth of Salmonella typhimurium results in increased uptake by Henle 407 epithelial and mouse peritoneal cells in vitro and repression of a major outer membrane protein. Infect Immun. 1991 Jan;59(1):437–440. doi: 10.1128/iai.59.1.437-440.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wood R. L., Pospischil A., Rose R. Distribution of persistent Salmonella typhimurium infection in internal organs of swine. Am J Vet Res. 1989 Jul;50(7):1015–1021. [PubMed] [Google Scholar]

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

RESOURCES