Oral immunization of interleukin-4 (IL-4) knockout mice with a recombinant Salmonella strain or cholera toxin reveals that CD4+ Th2 cells producing IL-6 and IL-10 are associated with mucosal immunoglobulin A responses

Infection and Immunity

Volumn 64, Issue 5, 1996, Pages 1516-1525

  Okahashi, Nobuo ^a   Yamamoto, Masafumi ^a   Vancott, John L ^a   Chatfield, Steven N ^b   Roberts, Mark ^c   Bluethmann, Horst ^d   Hiroi, Takachika ^e   Kiyono, Hiroshi ^a,e   Mcghee, Jerry R ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d F HOFFMANN LA ROCHE LTD   (Switzerland)

^e OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CHOLERA TOXIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 6; SALMONELLOSIS VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNITY; IMMUNIZATION; IMMUNOGLOBULIN PRODUCTION; MOUSE; MUCOSA; NONHUMAN; PRIORITY JOURNAL; SALMONELLA; T LYMPHOCYTE SUBPOPULATION;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, ORAL; ANIMALS; ANTIGENS, BACTERIAL; CHOLERA TOXIN; CYTOKINES; IMMUNIZATION; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INTERLEUKIN-10; INTERLEUKIN-4; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUCOUS MEMBRANE; RATS; RATS, INBRED F344; RNA, MESSENGER; SALMONELLA; TETANUS TOXIN; TH2 CELLS;

EID: 0029874545     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.64.5.1516-1525.1996     Document Type: Article

References (38)

1. Beagley, K. W., J. H. Eldridge, H. Kiyono, M. P. Everson, W. J. Koopman, T. Honjo, and J. R. McGhee. 1988. Recombinant murine IL-5 induces high rate IgA synthesis in cycling IgA-positive Peyer's patch B cells. J. Immunol. 141:2035-2042.
2. Beagley, K. W., J. H. Eldridge, F. Lee, H. Kiyono, M. P. Everson, W. J. Koopman, T. Hirano, T. Kishimoto, and J. R. McGhee. 1989. Interleukins and IgA synthesis: human and murine interleukin 6 induce high rate IgA secretion in IgA-committed B cells. J. Exp. Med. 169:2133-2148.
3. Brenner, C. A, A. W. Tam, P. A. Nelson, E. G. Engleman, N. Suzuki, K. E. Fry, and J. W. Larrick, 1989. Message amplification phenotyping (MAP-Ping): a technique to simultaneously measure multiple mRNAs from small numbers of cells. BioTechniques 7:1096-1103,
4. Chatfield, S. N., I. G. Charles, A. J. Makoff, M. D. Oxer, G. Dougan, D. Pickard, D. Slater, and N. F. Fairweather. 1992. 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. Bio/ Technology 10:888-892
5. Chatfield, S. N., R. A. Strugnell, and G. Dougan. 1989. Live Salmonella as vaccines and carriers of foreign antigenic determinants. Vaccine 7:495-498.
6. Chomezynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guamdinium thiocyanate-phenol-chloroform extraction. Anal. Biochem 162:156-159.
7. Czerkinsky, C. C., L. A. Nilsson, H. Nygren, O. Ouehterlony, and A. Tarkowski. 1983. A solid phase enzyme-linked immunospot (ELISPOT) assay for enumeration of specific antibody secreting cells. J Immunol Methods 65:109-121
8. deVos, T., and T. A. Dick. 1991. A rapid method to determine the isotype and specificity of coproantibodies in mice infected with Trichinella or fed cholera toxin. J. Immunol. Methods 141:285-288.
9. Elson, C. O., and W. Ealding. 1984. Generalized systemic and mucosal immunity in mice after mucosal stimulation with cholera toxin. J Immunol. 132:2736-2741.
10. Finkelman, F. D., J. Holmes. I. M. Katun, J. Urban, M. P. Beckman, L. S. Park, K. A. Schooley, R. L. Coffman, T. R. Mosmann, and W. E. Paul. 1990. Lymphokme control of in vivo immunogiobulin isotype selection. Annu. Rev. Immunol. 8:303-333.
11. Jackson, R. J., K. Fujihashi, J. Xu-Amano, H. Kiyuno, C. O. Elson, and J. R. McGhee. 1993. Optimizing oral vaccines: induction of systemic and mucosal B-cell and antibody responses to tetanus toxoid by use of cholera toxin as an adjuvant. Infect. Immun. 61:4272-4279
12. Kagaya, K., K. Watanabe, and Y. Fukazawa. 1989. Capacity of recombinant gamma Interferon to activate macrophages for Salmonella-killig activity. Infect. Immun. 57:609-615.
13. Kiyono, H., J. Bienenstock, J. R. McGhee, and P. B. Ernst. 1992. The mucosal immune system: features of inductive and effector sites to consider in mucosal immunization and vaccine development. Reg. Immunol. 4:54-62.
14. Kopf, M., G. L. Gros, M. Bachmann, M. C. Lamers, H. Bluethmann, and G. Kohler. 1993. Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature (London) 362:245-248.
15. Kuhn, R., K. Rajewsky, and W. Muller. 1991. Generation and analysis of interleukin-4 deficient mice Science 254:707-710
16. LeGros, G., S. Z. Ben-Sasson, R. Seder, F. D. Finkelman, and W. E. Paul. 1990. Generation of interleukin 4 (IL-4)-producing cells in vivo and in vitro. IL-2 and IL-4 are required form vitro generation of IL-4-producing cells. J. Exp. Med. 172:921-929.
17. Lu, W., D.-S. Han, J. Yuan, and J.-M. Andrien. 1994. Multi-target PCR analysis by capillary electrophoresis and laser-induced fluorescence Nature (London) 368:269-271.
18. Lycke, N., and J. Holmgren. 1986 Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens. Immunology 59:301-308.
19. Marinaro, M., H. F. Staats, T. Hiroi, M. Coste, R. J. Jackson, P. N. Boyaka, N. Okahashi, M. Yamamoto, K. Fujihashi, H. Kiyono, H. Bluethmann, and J. R. McGhee. 1995. The mucosal adjuvant effect of cholera toxin in mice results from induction of T helper (Th2) cells and IL-4 J. Immunol 155:4621-4629.
20. McGhee, J. R., J. Mestecky, M. T. Uertzbaugh, J. H. Eldridge, M. Hirasawa, and H. Kiyono. 1992. The mucosal immune system: from fundamental concepts to vaccine development. Vaccine 10:75-99.
21. Mestecky, J., and J. R. McGhee. 1987. Immunoglobulin A (IgA): molecular and cellular interactions involved in IgA biosynthesis and immune response. Adv. Immunol. 40:153-245.
22. Mosman, T. R., and R. L. Coffman. 1989. TH1 and Th2 cells different patterns of lymphokine secretion lead to different functional properties Annu. Rev. Immunol. 7:145-173
23. Muotiala, A., and P. H. Makela. 1990. The role of IFN-γ in murine Salmonella typhimurium infection. Microb. Pathog. 8:135-141.
24. Ramarathinam, L., R. A. Shaban, D. W. Niesel, and G. R. Klimpel. 1991. Interferon gamma (IFN-γ) production by gut-associated lymphoid tissue and spleen following oral Salmonella typhimurium challenge Microb Pathog. 11:347-356.
25. Ramsay, A. J., A. J. Husband, I. A. Ramshaw, S. Bao, K. I. Matthaei, C. Koehler, and M. Kopf. 1994. The role of interleukin-6 in mucosal IgA antibody responses in vivo. Science 264:561-563.
26. Roberts, M., S. N. Chatfield, and G. Dougan. 1994. Salmonella as carriers of heterologous antigens, p. 27-58. In D. T. O'Hagan (ed). Novel delivery systems for oral vaccines. CRC Press, Inc., Ann Arbor. Mich
27. Sad, S., and T. R. Mosmann. 1994. Single IL-2-secretmg precursor CD4 T cell can develop into either Th1 or Th2 cytokine secretion phenotype. J. Immunol 153:3514-3522.
28. Scott, P., and S. H. E. Kaufmann. 1991 The role of T-cell subsets and cytokines in the regulation of infection. Immunol. Today 12:346-349.
29. Sher, A., and R. L. Coffman. 1992. Regulation of immunity to parasites by T cells and T cell-derived cytokines. Annu. Rev. Immunol. 10:385-409.
30. Srinivasan, K. 1993. Electrophoretic separations of polymerase chain reaction-amplified DNA fragments in DNA typing using a capillary electrophoresis-laser induced fluorescence system. J. Chromatogr 652:83-91.
31. Staats, H. F., R. J. Jackson, M. Marinaro, I. Takahashi, H. Kiyono, and J. R. McGhee. 1994 Mucosal immunity to infection with implications for vaccine development. CUIT. Opin. Immunol. 6:572-583.
32. Street, N. E., and T. R. Mosmann. 1991. Functional diversity of T lymphocytes due to secretion of different cytokine patterns. FASEB J. 5:171-177.
33. Swain, S. L., A. D. Weinberg, M. English, and G. Huston. 1990 IL-4 directs the development of Th2-like helper effectors. J. Immunol. 145:3796-3806.
34. Vajdy, M., M. H., Kosco-Vilbois, M. Kopf, G. Köhler, and N. Lycke. 1995. Impaired mucosal immune responses in interleukin-4-targeted mice. J. Exp Med. 181:41-53.
35. 34a VanCott. J. L., et al. Unpublished data
36. VanCott, J. L., H. F. Staats, D. W. Pascual, M. Roberts, S. N. Chatfteld, M. Yamamoto, M. Coste, P. B. Carter, H. Kiyono, and J. R. McGhee. 1996. Regulation of mucosal and systemic antibody responses by T helper cell subsets, macrophages, and derived cytokines following oral immunization with live recombinant Salmonella. J. Immunol 156:1504-1514.
37. Xu-Amano, J., W. K. Aicher, T. Taguchi, H. Kiyono, and J. R. McGhee. 1992. Selective induction of Th2 cells in murine Peyer's patches by oral immunization. Int. Immunol. 4:433-445.
38. Xu-Amano, J., H. Kiyono, R. J. Jackson, H. F. Staats, K. Fujihashi, P. D. Burrows, C. O. Elson, S. Pillai, and J. R. McGhee. 1993. Helper T cell subsets for immunoglobulin A responses: oral immunization with tetanus toxoid and cholera toxin as adjuvant selectively induces Th2 cells in mucosa associated tissues. J. Exp. Med. 178:1309-1320