Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1995 Dec;63(12):4933–4938. doi: 10.1128/iai.63.12.4933-4938.1995

Immune responses to novel Escherichia coli and Salmonella typhimurium vectors that express colonization factor antigen I (CFA/I) of enterotoxigenic E. coli in the absence of the CFA/I positive regulator cfaR.

S Wu 1, D W Pascual 1, J L VanCott 1, J R McGhee 1, D R Maneval Jr 1, M M Levine 1, D M Hone 1
PMCID: PMC173709  PMID: 7591160

Abstract

An asd-stabilized plasmid carrying enterotoxigenic Escherichia coli cfaABCE genes was constructed and called pJGX15C-asd+. Expression of colonization factor antigen I (CFA/I) by this plasmid occurs independently of the cfaABCE positive regulator cfaR in attenuated Salmonella delta aro delta asd strain H683 and nonpathogenic laboratory E. coli asd strain chi 6212. Oral immunization of mice with nonpathogenic E. coli chi 6212 (pJGX15C-asd+) does not elicit significant serum or mucosal responses against CFA/I. In contrast, oral immunization with a single dose of attenuated S. typhimurium H683(pJGX15C-asd+) elicits a 10(5)-fold increase in CFA/I-specific serum immunoglobulin G and significant elevation of CFA/I-specific immunoglobulin A-secreting B cells in the lamina propria, mesenteric lymph nodes, and spleen. Thus, only the Salmonella-CFA/I construct effectively delivered CFA/I to the inductive sites of the gut-associated and systemic lymphoid tissues.

Full Text

The Full Text of this article is available as a PDF (270.3 KB).

Selected References

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

  1. Alpuche-Aranda C. M., Racoosin E. L., Swanson J. A., Miller S. I. Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes. J Exp Med. 1994 Feb 1;179(2):601–608. doi: 10.1084/jem.179.2.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beagley K. W., Eldridge J. H., Kiyono H., Everson M. P., Koopman W. J., Honjo T., McGhee J. R. Recombinant murine IL-5 induces high rate IgA synthesis in cycling IgA-positive Peyer's patch B cells. J Immunol. 1988 Sep 15;141(6):2035–2042. [PubMed] [Google Scholar]
  3. Bäumler A. J., Kusters J. G., Stojiljkovic I., Heffron F. Salmonella typhimurium loci involved in survival within macrophages. Infect Immun. 1994 May;62(5):1623–1630. doi: 10.1128/iai.62.5.1623-1630.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chatfield S. N., Charles I. G., Makoff A. J., Oxer M. D., Dougan G., Pickard D., Slater D., Fairweather N. F. Use of the nirB promoter to direct the stable expression of heterologous antigens in Salmonella oral vaccine strains: development of a single-dose oral tetanus vaccine. Biotechnology (N Y) 1992 Aug;10(8):888–892. doi: 10.1038/nbt0892-888. [DOI] [PubMed] [Google Scholar]
  5. Evans D. G., Evans D. J., Jr, Tjoa W. Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun. 1977 Nov;18(2):330–337. doi: 10.1128/iai.18.2.330-337.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Evans D. G., Silver R. P., Evans D. J., Jr, Chase D. G., Gorbach S. L. Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans. Infect Immun. 1975 Sep;12(3):656–667. doi: 10.1128/iai.12.3.656-667.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Francis C. L., Ryan T. A., Jones B. D., Smith S. J., Falkow S. Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature. 1993 Aug 12;364(6438):639–642. doi: 10.1038/364639a0. [DOI] [PubMed] [Google Scholar]
  8. Galán J. E., Nakayama K., Curtiss R., 3rd Cloning and characterization of the asd gene of Salmonella typhimurium: use in stable maintenance of recombinant plasmids in Salmonella vaccine strains. Gene. 1990 Sep 28;94(1):29–35. doi: 10.1016/0378-1119(90)90464-3. [DOI] [PubMed] [Google Scholar]
  9. Gonzalez C., Hone D., Noriega F. R., Tacket C. O., Davis J. R., Losonsky G., Nataro J. P., Hoffman S., Malik A., Nardin E. Salmonella typhi vaccine strain CVD 908 expressing the circumsporozoite protein of Plasmodium falciparum: strain construction and safety and immunogenicity in humans. J Infect Dis. 1994 Apr;169(4):927–931. doi: 10.1093/infdis/169.4.927. [DOI] [PubMed] [Google Scholar]
  10. Hall R. H., Maneval D. R., Jr, Collins J. H., Theibert J. L., Levine M. M. Purification and analysis of colonization factor antigen I, coli surface antigen 1, and coli surface antigen 3 fimbriae from enterotoxigenic Escherichia coli. J Bacteriol. 1989 Nov;171(11):6372–6374. doi: 10.1128/jb.171.11.6372-6374.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hamers A. M., Pel H. J., Willshaw G. A., Kusters J. G., van der Zeijst B. A., Gaastra W. The nucleotide sequence of the first two genes of the CFA/I fimbrial operon of human enterotoxigenic Escherichia coli. Microb Pathog. 1989 Apr;6(4):297–309. doi: 10.1016/0882-4010(89)90103-4. [DOI] [PubMed] [Google Scholar]
  12. Hone D. M., Harris A. M., Chatfield S., Dougan G., Levine M. M. Construction of genetically defined double aro mutants of Salmonella typhi. Vaccine. 1991 Nov;9(11):810–816. doi: 10.1016/0264-410x(91)90218-u. [DOI] [PubMed] [Google Scholar]
  13. Hone D., Attridge S., van den Bosch L., Hackett J. A chromosomal integration system for stabilization of heterologous genes in Salmonella based vaccine strains. Microb Pathog. 1988 Dec;5(6):407–418. doi: 10.1016/0882-4010(88)90002-2. [DOI] [PubMed] [Google Scholar]
  14. Jordi B. J., Willshaw G. A., van der Zeijst B. A., Gaastra W. The complete nucleotide sequence of region 1 of the CFA/I fimbrial operon of human enterotoxigenic Escherichia coli. DNA Seq. 1992;2(4):257–263. doi: 10.3109/10425179209020811. [DOI] [PubMed] [Google Scholar]
  15. Kaper J. B., Levine M. M. Progress towards a vaccine against enterotoxigenic Escherichia coli. Vaccine. 1988 Apr;6(2):197–199. doi: 10.1016/s0264-410x(88)80028-8. [DOI] [PubMed] [Google Scholar]
  16. Kohbata S., Yokoyama H., Yabuuchi E. Cytopathogenic effect of Salmonella typhi GIFU 10007 on M cells of murine ileal Peyer's patches in ligated ileal loops: an ultrastructural study. Microbiol Immunol. 1986;30(12):1225–1237. doi: 10.1111/j.1348-0421.1986.tb03055.x. [DOI] [PubMed] [Google Scholar]
  17. Levine M. M. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J Infect Dis. 1987 Mar;155(3):377–389. doi: 10.1093/infdis/155.3.377. [DOI] [PubMed] [Google Scholar]
  18. Levine M. M. Travellers' diarrhoea: prospects for successful immunoprophylaxis. Scand J Gastroenterol Suppl. 1983;84:121–134. [PubMed] [Google Scholar]
  19. Libby S. J., Goebel W., Ludwig A., Buchmeier N., Bowe F., Fang F. C., Guiney D. G., Songer J. G., Heffron F. A cytolysin encoded by Salmonella is required for survival within macrophages. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):489–493. doi: 10.1073/pnas.91.2.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Miller S. I., Kukral A. M., Mekalanos J. J. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci U S A. 1989 Jul;86(13):5054–5058. doi: 10.1073/pnas.86.13.5054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Savelkoul P. H., Willshaw G. A., McConnell M. M., Smith H. R., Hamers A. M., van der Zeijst B. A., Gaastra W. Expression of CFA/I fimbriae is positively regulated. Microb Pathog. 1990 Feb;8(2):91–99. doi: 10.1016/0882-4010(90)90073-y. [DOI] [PubMed] [Google Scholar]
  22. Tacket C. O., Hone D. M., Curtiss R., 3rd, Kelly S. M., Losonsky G., Guers L., Harris A. M., Edelman R., Levine M. M. Comparison of the safety and immunogenicity of delta aroC delta aroD and delta cya delta crp Salmonella typhi strains in adult volunteers. Infect Immun. 1992 Feb;60(2):536–541. doi: 10.1128/iai.60.2.536-541.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Tacket C. O., Hone D. M., Losonsky G. A., Guers L., Edelman R., Levine M. M. Clinical acceptability and immunogenicity of CVD 908 Salmonella typhi vaccine strain. Vaccine. 1992;10(7):443–446. doi: 10.1016/0264-410x(92)90392-w. [DOI] [PubMed] [Google Scholar]
  24. Tacket C. O., Reid R. H., Boedeker E. C., Losonsky G., Nataro J. P., Bhagat H., Edelman R. Enteral immunization and challenge of volunteers given enterotoxigenic E. coli CFA/II encapsulated in biodegradable microspheres. Vaccine. 1994 Nov;12(14):1270–1274. doi: 10.1016/s0264-410x(94)80038-2. [DOI] [PubMed] [Google Scholar]
  25. Van Ginkel F. W., Liu C., Simecka J. W., Dong J. Y., Greenway T., Frizzell R. A., Kiyono H., McGhee J. R., Pascual D. W. Intratracheal gene delivery with adenoviral vector induces elevated systemic IgG and mucosal IgA antibodies to adenovirus and beta-galactosidase. Hum Gene Ther. 1995 Jul;6(7):895–903. doi: 10.1089/hum.1995.6.7-895. [DOI] [PubMed] [Google Scholar]
  26. Willshaw G. A., Smith H. R., McConnell M. M., Rowe B. Expression of cloned plasmid regions encoding colonization factor antigen I (CFA/I) in Escherichia coli. Plasmid. 1985 Jan;13(1):8–16. doi: 10.1016/0147-619x(85)90051-4. [DOI] [PubMed] [Google Scholar]
  27. Yamamoto T., Tamura Y., Yokota T. Enteroadhesion fimbriae and enterotoxin of Escherichia coli: genetic transfer to a streptomycin-resistant mutant of the galE oral-route live-vaccine Salmonella typhi Ty21a. Infect Immun. 1985 Dec;50(3):925–928. doi: 10.1128/iai.50.3.925-928.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. de Aizpurua H. J., Russell-Jones G. J. Oral vaccination. Identification of classes of proteins that provoke an immune response upon oral feeding. J Exp Med. 1988 Feb 1;167(2):440–451. doi: 10.1084/jem.167.2.440. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES