Abstract
T cells in cooperation with macrophages play an important role in resolution of primary Yersinia enterocolitica infection in mice. Previous work from this laboratory demonstrated that gamma interferon (IFN-gamma) and tumor necrosis factor alpha (TNF-alpha) are essential mediators of these processes. In an attempt to elucidate early mechanisms of resistance, we investigated cytokine mRNA production, including that for interleukin-1 beta (IL-1 beta), IL-2, IL-4, IL-6, IL-10, TNF-alpha, and IFN-gamma, after primary as well as secondary Y. enterocolitica infection in Yersinia-susceptible BALB/c mice and Yersinia-resistant C57BL/6 mice. In both strains of mice, proinflammatory cytokines such as IL-1 beta, IL-6, and TNF-alpha were expressed rapidly and to comparable degrees, while IFN-gamma expression was enhanced two- to eightfold in C57BL/6 mice, as revealed by semiquantitative reverse transcription PCR. Similar results were found in both mouse strains after secondary Y. enterocolitica infection. IL-2 mRNA was detected only during secondary infection and disappeared rapidly in BALB/c mice. IL-4 mRNA expression was detectable in C57BL/6 but not BALB/c mice. The levels of cytokine mRNA expression correlated closely with the number of injected bacteria. The findings reported here support the hypothesis that early and enhanced production of IFN-gamma may be associated with a state of heightened resistance against Y. enterocolitica infection.
Full text
PDF





Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Autenrieth I. B., Beer M., Bohn E., Kaufmann S. H., Heesemann J. Immune responses to Yersinia enterocolitica in susceptible BALB/c and resistant C57BL/6 mice: an essential role for gamma interferon. Infect Immun. 1994 Jun;62(6):2590–2599. doi: 10.1128/iai.62.6.2590-2599.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Autenrieth I. B., Hantschmann P., Heymer B., Heesemann J. Immunohistological characterization of the cellular immune response against Yersinia enterocolitica in mice: evidence for the involvement of T lymphocytes. Immunobiology. 1993 Jan;187(1-2):1–16. doi: 10.1016/S0171-2985(11)80241-X. [DOI] [PubMed] [Google Scholar]
- Autenrieth I. B., Heesemann J. In vivo neutralization of tumor necrosis factor-alpha and interferon-gamma abrogates resistance to Yersinia enterocolitica infection in mice. Med Microbiol Immunol. 1992;181(6):333–338. doi: 10.1007/BF00191545. [DOI] [PubMed] [Google Scholar]
- Autenrieth I. B., Tingle A., Reske-Kunz A., Heesemann J. T lymphocytes mediate protection against Yersinia enterocolitica in mice: characterization of murine T-cell clones specific for Y. enterocolitica. Infect Immun. 1992 Mar;60(3):1140–1149. doi: 10.1128/iai.60.3.1140-1149.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Autenrieth I. B., Vogel U., Preger S., Heymer B., Heesemann J. Experimental Yersinia enterocolitica infection in euthymic and T-cell-deficient athymic nude C57BL/6 mice: comparison of time course, histomorphology, and immune response. Infect Immun. 1993 Jun;61(6):2585–2595. doi: 10.1128/iai.61.6.2585-2595.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bogdan C., Gessner A., Röllinghoff M. Cytokines in leishmaniasis: a complex network of stimulatory and inhibitory interactions. Immunobiology. 1993 Nov;189(3-4):356–396. doi: 10.1016/S0171-2985(11)80366-9. [DOI] [PubMed] [Google Scholar]
- Carter P. B. Animal model of human disease. Yersinia enteritis. Animal model: oral Yersinia enterocolitica infection of mice. Am J Pathol. 1975 Dec;81(3):703–706. [PMC free article] [PubMed] [Google Scholar]
- Carter P. B. Pathogenecity of Yersinia enterocolitica for mice. Infect Immun. 1975 Jan;11(1):164–170. doi: 10.1128/iai.11.1.164-170.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carter P. B., Varga C. F., Keet E. E. New strain of Yersinia enterocolitica pathogenic for rodents. Appl Microbiol. 1973 Dec;26(6):1016–1018. doi: 10.1128/am.26.6.1016-1018.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carter P. B., Zahorchak R. J., Brubaker R. R. Plague virulence antigens from Yersinia enterocolitica. Infect Immun. 1980 May;28(2):638–640. doi: 10.1128/iai.28.2.638-640.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
- Ehlers S., Mielke M. E., Blankenstein T., Hahn H. Kinetic analysis of cytokine gene expression in the livers of naive and immune mice infected with Listeria monocytogenes. The immediate early phase in innate resistance and acquired immunity. J Immunol. 1992 Nov 1;149(9):3016–3022. [PubMed] [Google Scholar]
- Fiorentino D. F., Zlotnik A., Mosmann T. R., Howard M., O'Garra A. IL-10 inhibits cytokine production by activated macrophages. J Immunol. 1991 Dec 1;147(11):3815–3822. [PubMed] [Google Scholar]
- Flesch I. E., Kaufmann S. H. Role of cytokines in tuberculosis. Immunobiology. 1993 Nov;189(3-4):316–339. doi: 10.1016/S0171-2985(11)80364-5. [DOI] [PubMed] [Google Scholar]
- Haak-Frendscho M., Brown J. F., Iizawa Y., Wagner R. D., Czuprynski C. J. Administration of anti-IL-4 monoclonal antibody 11B11 increases the resistance of mice to Listeria monocytogenes infection. J Immunol. 1992 Jun 15;148(12):3978–3985. [PubMed] [Google Scholar]
- Hancock G. E., Schaedler R. W., MacDonald T. T. Multigenic control of resistance to Yersinia enterocolitica in inbred strains of mice. Infect Immun. 1988 Feb;56(2):532–533. doi: 10.1128/iai.56.2.532-533.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hancock G. E., Schaedler R. W., MacDonald T. T. Yersinia enterocolitica infection in resistant and susceptible strains of mice. Infect Immun. 1986 Jul;53(1):26–31. doi: 10.1128/iai.53.1.26-31.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hanski C., Kutschka U., Schmoranzer H. P., Naumann M., Stallmach A., Hahn H., Menge H., Riecken E. O. Immunohistochemical and electron microscopic study of interaction of Yersinia enterocolitica serotype O8 with intestinal mucosa during experimental enteritis. Infect Immun. 1989 Mar;57(3):673–678. doi: 10.1128/iai.57.3.673-678.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Havell E. A. Evidence that tumor necrosis factor has an important role in antibacterial resistance. J Immunol. 1989 Nov 1;143(9):2894–2899. [PubMed] [Google Scholar]
- Heesemann J., Gaede K., Autenrieth I. B. Experimental Yersinia enterocolitica infection in rodents: a model for human yersiniosis. APMIS. 1993 Jun;101(6):417–429. [PubMed] [Google Scholar]
- Heesemann J., Laufs R. Construction of a mobilizable Yersinia enterocolitica virulence plasmid. J Bacteriol. 1983 Aug;155(2):761–767. doi: 10.1128/jb.155.2.761-767.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heinzel F. P., Sadick M. D., Holaday B. J., Coffman R. L., Locksley R. M. Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. J Exp Med. 1989 Jan 1;169(1):59–72. doi: 10.1084/jem.169.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heinzel F. P., Sadick M. D., Mutha S. S., Locksley R. M. Production of interferon gamma, interleukin 2, interleukin 4, and interleukin 10 by CD4+ lymphocytes in vivo during healing and progressive murine leishmaniasis. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7011–7015. doi: 10.1073/pnas.88.16.7011. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Howard M., O'Garra A. Biological properties of interleukin 10. Immunol Today. 1992 Jun;13(6):198–200. doi: 10.1016/0167-5699(92)90153-X. [DOI] [PubMed] [Google Scholar]
- Iizawa Y., Brown J. F., Czuprynski C. J. Early expression of cytokine mRNA in mice infected with Listeria monocytogenes. Infect Immun. 1992 Oct;60(10):4068–4073. doi: 10.1128/iai.60.10.4068-4073.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Iizawa Y., Wagner R. D., Czuprynski C. J. Analysis of cytokine mRNA expression in Listeria-resistant C57BL/6 and Listeria-susceptible A/J mice during Listeria monocytogenes infection. Infect Immun. 1993 Sep;61(9):3739–3744. doi: 10.1128/iai.61.9.3739-3744.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lian C. J., Hwang W. S., Pai C. H. Plasmid-mediated resistance to phagocytosis in Yersinia enterocolitica. Infect Immun. 1987 May;55(5):1176–1183. doi: 10.1128/iai.55.5.1176-1183.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Locksley R. M., Louis J. A. Immunology of leishmaniasis. Curr Opin Immunol. 1992 Aug;4(4):413–418. doi: 10.1016/s0952-7915(06)80032-4. [DOI] [PubMed] [Google Scholar]
- Mielke M. E., Ehlers S., Hahn H. The role of cytokines in experimental listeriosis. Immunobiology. 1993 Nov;189(3-4):285–315. doi: 10.1016/S0171-2985(11)80363-3. [DOI] [PubMed] [Google Scholar]
- Nakane A., Minagawa T., Kohanawa M., Chen Y., Sato H., Moriyama M., Tsuruoka N. Interactions between endogenous gamma interferon and tumor necrosis factor in host resistance against primary and secondary Listeria monocytogenes infections. Infect Immun. 1989 Nov;57(11):3331–3337. doi: 10.1128/iai.57.11.3331-3337.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakane A., Numata A., Minagawa T. Endogenous tumor necrosis factor, interleukin-6, and gamma interferon levels during Listeria monocytogenes infection in mice. Infect Immun. 1992 Feb;60(2):523–528. doi: 10.1128/iai.60.2.523-528.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Platzer C., Richter G., Uberla K., Müller W., Blöcker H., Diamantstein T., Blankenstein T. Analysis of cytokine mRNA levels in interleukin-4-transgenic mice by quantitative polymerase chain reaction. Eur J Immunol. 1992 May;22(5):1179–1184. doi: 10.1002/eji.1830220511. [DOI] [PubMed] [Google Scholar]
- Simonet M., Richard S., Berche P. Electron microscopic evidence for in vivo extracellular localization of Yersinia pseudotuberculosis harboring the pYV plasmid. Infect Immun. 1990 Mar;58(3):841–845. doi: 10.1128/iai.58.3.841-845.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]