Europe PMC

This website requires cookies, and the limited processing of your personal data in order to function. By using the site you are agreeing to this as outlined in our privacy notice and cookie policy.

Immune responses to Yersinia enterocolitica in susceptible BALB/c and resistant C57BL/6 mice: an essential role for gamma interferon.

Author information

Affiliations

  • 1. Institute for Hygiene and Microbiology, University of Würzburg, Federal Republic of Germany.
      Authors
    • Autenrieth IB 1
    (1 author)

Infection and Immunity, 01 Jun 1994, 62(6):2590-2599
https://doi.org/10.1128/iai.62.6.2590-2599.1994 PMID: 8188382 PMCID: PMC186549

Free full text in Europe PMC

Abstract 

Susceptibility of mice to infection with Yersinia enterocolitica has been shown to be related to neither the Ity locus encoding for resistance to Salmonella typhimurium and other pathogens nor the H-2 locus. Recent studies in our laboratory have demonstrated that T-cell-mediated immune responses are required for overcoming primary Yersinia infection. In the present study, we investigated the course of infection with Y. enterocolitica and the resulting immune responses in Yersinia-susceptible BALB/c and Yersinia-resistant C57BL/6 mice. In the early phase of infection, the clearance of the pathogen was comparable in both strains of mice, suggesting similar mechanisms of innate resistance. Splenic T cells from Yersinia-infected C57BL/6 mice exhibited marked proliferative responses and produced gamma interferon (IFN-gamma) upon exposure to heat-killed yersiniae. By contrast, the Yersinia-specific T-cell response in BALB/c mice was weak, and IFN-gamma production could not be detected before day 21 postinfection. T cells isolated from C57BL/6 mice 7 days after infection mediated immunity to Y. enterocolitica but those from BALB/c mice did not, while at 21 days postinfection T cells from both strains mediated protection. Neutralization of IFN-gamma abrogated resistance to yersiniae in C57BL/6 mice but to a far smaller extent in BALB/c mice. Administration of recombinant IFN-gamma or anti-interleukin-4 antibodies rendered BALB/c mice resistant to yersiniae, whereas this treatment did not significantly affect the course of the infection in C57BL/6 mice. These results indicate that the cellular immune response, in particular the production of IFN-gamma by Yersinia-specific T cells, is associated with resistance of mice to Y. enterocolitica.

Free full text 

Logo of iaiLink to Publisher's site
Infect Immun. 1994 Jun; 62(6): 2590–2599.
PMCID: PMC186549
PMID: 8188382

Immune responses to Yersinia enterocolitica in susceptible BALB/c and resistant C57BL/6 mice: an essential role for gamma interferon.

I B Autenrieth, M Beer, E Bohn, S H Kaufmann, and J Heesemann
Author information Copyright and License information Disclaimer

Abstract

Susceptibility of mice to infection with Yersinia enterocolitica has been shown to be related to neither the Ity locus encoding for resistance to Salmonella typhimurium and other pathogens nor the H-2 locus. Recent studies in our laboratory have demonstrated that T-cell-mediated immune responses are required for overcoming primary Yersinia infection. In the present study, we investigated the course of infection with Y. enterocolitica and the resulting immune responses in Yersinia-susceptible BALB/c and Yersinia-resistant C57BL/6 mice. In the early phase of infection, the clearance of the pathogen was comparable in both strains of mice, suggesting similar mechanisms of innate resistance. Splenic T cells from Yersinia-infected C57BL/6 mice exhibited marked proliferative responses and produced gamma interferon (IFN-gamma) upon exposure to heat-killed yersiniae. By contrast, the Yersinia-specific T-cell response in BALB/c mice was weak, and IFN-gamma production could not be detected before day 21 postinfection. T cells isolated from C57BL/6 mice 7 days after infection mediated immunity to Y. enterocolitica but those from BALB/c mice did not, while at 21 days postinfection T cells from both strains mediated protection. Neutralization of IFN-gamma abrogated resistance to yersiniae in C57BL/6 mice but to a far smaller extent in BALB/c mice. Administration of recombinant IFN-gamma or anti-interleukin-4 antibodies rendered BALB/c mice resistant to yersiniae, whereas this treatment did not significantly affect the course of the infection in C57BL/6 mice. These results indicate that the cellular immune response, in particular the production of IFN-gamma by Yersinia-specific T cells, is associated with resistance of mice to Y. enterocolitica.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.6M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.
 
icon of scanned page 2590
2590
icon of scanned page 2591
2591
icon of scanned page 2592
2592
icon of scanned page 2593
2593
icon of scanned page 2594
2594
icon of scanned page 2595
2595
icon of scanned page 2596
2596
icon of scanned page 2597
2597
icon of scanned page 2598
2598
icon of scanned page 2599
2599
 

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Autenrieth IB, 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. [Abstract] [Google Scholar]
  • Autenrieth IB, 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. [Abstract] [Google Scholar]
  • Autenrieth IB, 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Autenrieth IB, 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. [Europe PMC free article] [Abstract] [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. [Abstract] [Google Scholar]
  • Bottomly K. A functional dichotomy in CD4+ T lymphocytes. Immunol Today. 1988 Sep;9(9):268–274. [Abstract] [Google Scholar]
  • Bretscher PA, Wei G, Menon JN, Bielefeldt-Ohmann H. Establishment of stable, cell-mediated immunity that makes "susceptible" mice resistant to Leishmania major. Science. 1992 Jul 24;257(5069):539–542. [Abstract] [Google Scholar]
  • Chatelain R, Varkila K, Coffman RL. IL-4 induces a Th2 response in Leishmania major-infected mice. J Immunol. 1992 Feb 15;148(4):1182–1187. [Abstract] [Google Scholar]
  • Cornelis G, Laroche Y, Balligand G, Sory MP, Wauters G. Yersinia enterocolitica, a primary model for bacterial invasiveness. Rev Infect Dis. 1987 Jan-Feb;9(1):64–87. [Abstract] [Google Scholar]
  • Cover TL, Aber RC. Yersinia enterocolitica. N Engl J Med. 1989 Jul 6;321(1):16–24. [Abstract] [Google Scholar]
  • Haak-Frendscho M, Brown JF, Iizawa Y, Wagner RD, Czuprynski CJ. 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. [Abstract] [Google Scholar]
  • Hancock GE, Schaedler RW, MacDonald TT. Yersinia enterocolitica infection in resistant and susceptible strains of mice. Infect Immun. 1986 Jul;53(1):26–31. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hancock GE, Schaedler RW, MacDonald TT. Multigenic control of resistance to Yersinia enterocolitica in inbred strains of mice. Infect Immun. 1988 Feb;56(2):532–533. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hanski C, Kutschka U, Schmoranzer HP, Naumann M, Stallmach A, Hahn H, Menge H, Riecken EO. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Heeg K, Reimann J, Kabelitz D, Hardt C, Wagner H. A rapid colorimetric assay for the determination of IL-2-producing helper T cell frequencies. J Immunol Methods. 1985 Mar 18;77(2):237–246. [Abstract] [Google Scholar]
  • Heesemann J, Gaede K, Autenrieth IB. Experimental Yersinia enterocolitica infection in rodents: a model for human yersiniosis. APMIS. 1993 Jun;101(6):417–429. [Abstract] [Google Scholar]
  • Heesemann J, Laufs R. Construction of a mobilizable Yersinia enterocolitica virulence plasmid. J Bacteriol. 1983 Aug;155(2):761–767. [Europe PMC free article] [Abstract] [Google Scholar]
  • Heinzel FP, Sadick MD, Holaday BJ, Coffman RL, Locksley RM. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Heinzel FP, Sadick MD, Mutha SS, Locksley RM. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hsieh CS, Macatonia SE, Tripp CS, Wolf SF, O'Garra A, Murphy KM. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science. 1993 Apr 23;260(5107):547–549. [Abstract] [Google Scholar]
  • Julius MH, Simpson E, Herzenberg LA. A rapid method for the isolation of functional thymus-derived murine lymphocytes. Eur J Immunol. 1973 Oct;3(10):645–649. [Abstract] [Google Scholar]
  • Kaye PM, Curry AJ, Blackwell JM. Differential production of Th1- and Th2-derived cytokines does not determine the genetically controlled or vaccine-induced rate of cure in murine visceral leishmaniasis. J Immunol. 1991 Apr 15;146(8):2763–2770. [Abstract] [Google Scholar]
  • Kiderlen AF, Kaufmann SH, Lohmann-Matthes ML. Protection of mice against the intracellular bacterium Listeria monocytogenes by recombinant immune interferon. Eur J Immunol. 1984 Oct;14(10):964–967. [Abstract] [Google Scholar]
  • Kono DH, Ogasawara M, Yu DT. An animal model to study serum immunoglobulin response to infection by Yersinia enterocolitica. Clin Exp Rheumatol. 1985 Apr-Jun;3(2):117–121. [Abstract] [Google Scholar]
  • Leiby DA, Fortier AH, Crawford RM, Schreiber RD, Nacy CA. In vivo modulation of the murine immune response to Francisella tularensis LVS by administration of anticytokine antibodies. Infect Immun. 1992 Jan;60(1):84–89. [Europe PMC free article] [Abstract] [Google Scholar]
  • Lian CJ, Hwang WS, Pai CH. Plasmid-mediated resistance to phagocytosis in Yersinia enterocolitica. Infect Immun. 1987 May;55(5):1176–1183. [Europe PMC free article] [Abstract] [Google Scholar]
  • Locksley RM, Louis JA. Immunology of leishmaniasis. Curr Opin Immunol. 1992 Aug;4(4):413–418. [Abstract] [Google Scholar]
  • Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol. 1986 Apr 1;136(7):2348–2357. [Abstract] [Google Scholar]
  • Müller I, Fruth U, Louis JA. Immunobiology of experimental leishmaniasis. Med Microbiol Immunol. 1992;181(1):1–12. [Abstract] [Google Scholar]
  • Pearce EJ, Caspar P, Grzych JM, Lewis FA, Sher A. Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med. 1991 Jan 1;173(1):159–166. [Europe PMC free article] [Abstract] [Google Scholar]
  • Pond L, Wassom DL, Hayes CE. Evidence for differential induction of helper T cell subsets during Trichinella spiralis infection. J Immunol. 1989 Dec 15;143(12):4232–4237. [Abstract] [Google Scholar]
  • Powrie F, Coffman RL. Cytokine regulation of T-cell function: potential for therapeutic intervention. Immunol Today. 1993 Jun;14(6):270–274. [Abstract] [Google Scholar]
  • Reiner SL, Locksley RM. The worm and the protozoa: stereotyped responses or distinct antigens? Parasitol Today. 1993 Jul;9(7):258–260. [Abstract] [Google Scholar]
  • Rodrigues M, Nussenzweig RS, Romero P, Zavala F. The in vivo cytotoxic activity of CD8+ T cell clones correlates with their levels of expression of adhesion molecules. J Exp Med. 1992 Apr 1;175(4):895–905. [Europe PMC free article] [Abstract] [Google Scholar]
  • Rosqvist R, Bölin I, Wolf-Watz H. Inhibition of phagocytosis in Yersinia pseudotuberculosis: a virulence plasmid-encoded ability involving the Yop2b protein. Infect Immun. 1988 Aug;56(8):2139–2143. [Europe PMC free article] [Abstract] [Google Scholar]
  • Sadick MD, Heinzel FP, Holaday BJ, Pu RT, Dawkins RS, Locksley RM. Cure of murine leishmaniasis with anti-interleukin 4 monoclonal antibody. Evidence for a T cell-dependent, interferon gamma-independent mechanism. J Exp Med. 1990 Jan 1;171(1):115–127. [Europe PMC free article] [Abstract] [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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Slade SJ, Langhorne J. Production of interferon-gamma during infection of mice with Plasmodium chabaudi chabaudi. Immunobiology. 1989 Oct;179(4-5):353–365. [Abstract] [Google Scholar]
  • Springer TA. Adhesion receptors of the immune system. Nature. 1990 Aug 2;346(6283):425–434. [Abstract] [Google Scholar]
  • Tripp CS, Wolf SF, Unanue ER. Interleukin 12 and tumor necrosis factor alpha are costimulators of interferon gamma production by natural killer cells in severe combined immunodeficiency mice with listeriosis, and interleukin 10 is a physiologic antagonist. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3725–3729. [Europe PMC free article] [Abstract] [Google Scholar]
  • Vogel U, Autenrieth IB, Berner R, Heesemann J. Role of plasmid-encoded antigens of Yersinia enterocolitica in humoral immunity against secondary Y. enterocolitica infection in mice. Microb Pathog. 1993 Jul;15(1):23–36. [Abstract] [Google Scholar]
  • Yamamura M, Uyemura K, Deans RJ, Weinberg K, Rea TH, Bloom BR, Modlin RL. Defining protective responses to pathogens: cytokine profiles in leprosy lesions. Science. 1991 Oct 11;254(5029):277–279. [Abstract] [Google Scholar]
Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

Full text links 

Read article at publisher's site: https://doi.org/10.1128/iai.62.6.2590-2599.1994

Read article for free, from open access legal sources, via Unpaywall: https://iai.asm.org/content/iai/62/6/2590.full.pdfUnpaywall

Free after 4 months at iai.asm.org
http://iai.asm.org/cgi/reprint/62/6/2590

Free to read at iai.asm.org
http://iai.asm.org/cgi/content/abstract/62/6/2590

Citations & impact 

Impact metrics

123
Citations
Jump to Citations
1
Data citation
Jump to Data

Citations of article over time

Alternative metrics

Altmetric item for https://www.altmetric.com/details/107851164
Altmetric
Discover the attention surrounding your research
https://www.altmetric.com/details/107851164

Smart citations by scite.ai
Smart citations by scite.ai include citation statements extracted from the full text of the citing article. The number of the statements may be higher than the number of citations provided by EuropePMC if one paper cites another multiple times or lower if scite has not yet processed some of the citing articles.
Explore citation contexts and check if this article has been supported or disputed.
https://scite.ai/reports/10.1128/iai.62.6.2590-2599.1994

Supporting
Mentioning
Contrasting
5
69
2

Article citations

Go to all (123) article citations

Data 

Similar Articles 

To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.