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PMID: 15534372 Published · ppublish English Comparative Study Journal Article

T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation.

The Journal of experimental medicine ·Vol. 200 ·No. 10 ·2004-11-15 ·Pages 1289-97

Roers A, Siewe L, Strittmatter E, Deckert M, Schlüter D, Stenzel W, Gruber AD, Krieg T, Rajewsky K, Müller W

Abstract

Interleukin (IL)-10 is a regulator of inflammatory responses and is secreted by a variety of different cell types including T cells. T regulatory cells have been shown to suppress immune responses by IL-10-dependent, but also IL-10-independent, mechanisms. Herein, we address the role of T cell-derived IL-10 in mice with an inactivation of the IL-10 gene restricted to T cells generated by Cre/loxP-mediated targeting of the IL-10 gene. Splenocytes from this T cell-specific mutant secrete increased amounts of proinflammatory cytokines after activation in vitro compared with show enhanced contact hypersensitivity reactions, and succumb to severe immunopathology upon infection with Toxoplasma gondii. Despite intact IL-10 genes in other cell types, the dysregulation of T cell responses observed in the T cell-specific IL-10 mutant closely resembles the phenotype in complete IL-10 deficiency. However, in contrast to complete IL-10 deficiency, sensitivity to endotoxic shock and irritant responses of the skin are not enhanced in the T cell-specific IL-10 mutant. Our data highlight the importance of T cell-derived IL-10 in the regulation of T cell responses and demonstrate that endotoxic shock and the irritant response of the skin are controlled by IL-10 from other cell types.

MeSH Terms
Animals Gene Silencing/immunology Histological Techniques Immunity, Cellular/immunology Immunity, Innate/immunology Interleukin-10/genetics,metabolism Intestinal Mucosa/pathology Lipopolysaccharides/immunology Mice Mice, Transgenic Mutagenesis, Insertional Skin Irritancy Tests Spleen/cytology,metabolism T-Lymphocytes/immunology,metabolism Toxoplasma/immunology
Chemicals
Lipopolysaccharides Interleukin-10
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Roers Axel
Dept. of Dermatology, University of Cologne, Josef Stelzmann Str. 9, 50931 Cologne, Germany. axel.roers@uni-koeln.de
Siewe Lisa
Strittmatter Elke
Deckert Martina
Schlüter Dirk
Stenzel Werner
Gruber Achim D
Krieg Thomas
Rajewsky Klaus
Müller Werner
References (44)
44 references, click to expand
  1. An essential role for Scurfin in CD4+CD25+ T regulatory cells.
    Nat Immunol. 2003 Apr;4(4):337-42 PMID: 12612581
  2. Helicobacter hepaticus-induced colitis in interleukin-10-deficient mice: cytokine requirements for the induction and maintenance of intestinal inflammation.
    Infect Immun. 2001 Jul;69(7):4232-41 PMID: 11401959
  3. Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones.
    J Exp Med. 1989 Dec 1;170(6):2081-95 PMID: 2531194
  4. Toxoplasma encephalitis of immunocompetent and nude mice: immunohistochemical characterisation of Toxoplasma antigen, infiltrates and major histocompatibility complex gene products.
    J Neuroimmunol. 1991 Mar;31(3):185-98 PMID: 1995650
  5. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes.
    J Exp Med. 1991 Nov 1;174(5):1209-20 PMID: 1940799
  6. Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10.
    Eur J Immunol. 1992 Mar;22(3):711-7 PMID: 1547817
  7. Identification and induction of keratinocyte-derived IL-10.
    J Immunol. 1992 Jul 1;149(1):92-5 PMID: 1607665
  8. Systemic suppression of delayed-type hypersensitivity by supernatants from UV-irradiated keratinocytes. An essential role for keratinocyte-derived IL-10.
    J Immunol. 1992 Dec 15;149(12):3865-71 PMID: 1460278
  9. Interleukin-10-deficient mice develop chronic enterocolitis.
    Cell. 1993 Oct 22;75(2):263-74 PMID: 8402911
  10. Interleukin 10 but not interleukin 4 is a natural suppressant of cutaneous inflammatory responses.
    J Exp Med. 1995 Jul 1;182(1):99-108 PMID: 7790826
  11. IL-10 mediates immunosuppression following primary infection with Toxoplasma gondii in mice.
    Parasite Immunol. 1995 Apr;17(4):185-95 PMID: 7624159
  12. TGF-beta enhances macrophage ability to produce IL-10 in normal and tumor-bearing mice.
    J Immunol. 1995 Nov 15;155(10):4926-32 PMID: 7594497
  13. Interleukin-10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Shwartzman reaction but not endotoxin tolerance.
    J Clin Invest. 1995 Nov;96(5):2339-47 PMID: 7593621
  14. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells.
    Nucleic Acids Res. 1995 Dec 25;23(24):5080-1 PMID: 8559668
  15. Biochemical characterization and protein kinase C dependency of monokine-inducing activities of Toxoplasma gondii.
    Infect Immun. 1996 Jun;64(6):2010-8 PMID: 8675301
  16. In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha.
    J Immunol. 1996 Jul 15;157(2):798-805 PMID: 8752931
  17. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis.
    Nature. 1997 Oct 16;389(6652):737-42 PMID: 9338786
  18. In situ expression of interleukin-10 in noninflamed human gut and in inflammatory bowel disease.
    Am J Pathol. 1998 Jul;153(1):121-30 PMID: 9665472
  19. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production.
    J Exp Med. 1998 Jul 20;188(2):287-96 PMID: 9670041
  20. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism.
    Infect Immun. 1998 Nov;66(11):5157-66 PMID: 9784517
  21. Resting respiratory tract dendritic cells preferentially stimulate T helper cell type 2 (Th2) responses and require obligatory cytokine signals for induction of Th1 immunity.
    J Exp Med. 1998 Dec 7;188(11):2019-31 PMID: 9841916
  22. Endogenous interleukin-10 is required for prevention of a hyperinflammatory intracerebral immune response in Listeria monocytogenes meningoencephalitis.
    Infect Immun. 2001 Jul;69(7):4561-71 PMID: 11402000
  23. Regulatory T cells in the control of immune pathology.
    Nat Immunol. 2001 Sep;2(9):816-22 PMID: 11526392
  24. Helicobacter ganmani sp. nov., a urease-negative anaerobe isolated from the intestines of laboratory mice.
    Int J Syst Evol Microbiol. 2001 Sep;51(Pt 5):1881-9 PMID: 11594622
  25. Control of T-cell activation by CD4+ CD25+ suppressor T cells.
    Immunol Rev. 2001 Aug;182:58-67 PMID: 11722623
  26. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival.
    Immunity. 2001 Nov;15(5):763-74 PMID: 11728338
  27. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis.
    J Exp Med. 2002 Jan 21;195(2):221-31 PMID: 11805149
  28. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation.
    Immunity. 2002 Feb;16(2):219-30 PMID: 11869683
  29. Th2 cytokine production from mast cells is directly induced by lipopolysaccharide and distinctly regulated by c-Jun N-terminal kinase and p38 pathways.
    J Immunol. 2002 Oct 1;169(7):3801-10 PMID: 12244175
  30. B cells regulate autoimmunity by provision of IL-10.
    Nat Immunol. 2002 Oct;3(10):944-50 PMID: 12244307
  31. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity.
    Nature. 2002 Dec 5;420(6915):502-7 PMID: 12466842
  32. CD4+CD25+ T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms.
    J Exp Med. 2003 Jan 6;197(1):111-9 PMID: 12515818
  33. Antigen-specific suppression of a primed immune response by dendritic cells mediated by regulatory T cells secreting interleukin-10.
    Immunity. 2003 Jan;18(1):155-67 PMID: 12530984
  34. Control of regulatory T cell development by the transcription factor Foxp3.
    Science. 2003 Feb 14;299(5609):1057-61 PMID: 12522256
  35. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells.
    Nat Immunol. 2003 Apr;4(4):330-6 PMID: 12612578
  36. Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells.
    J Exp Med. 1999 Jul 19;190(2):229-39 PMID: 10432286
  37. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation.
    J Exp Med. 1999 Oct 4;190(7):995-1004 PMID: 10510089
  38. Effects of liver-derived dendritic cell progenitors on Th1- and Th2-like cytokine responses in vitro and in vivo.
    J Immunol. 2000 Feb 1;164(3):1346-54 PMID: 10640749
  39. Regulatory T cells in autoimmmunity*.
    Annu Rev Immunol. 2000;18:423-49 PMID: 10837065
  40. Interleukin-10 and the interleukin-10 receptor.
    Annu Rev Immunol. 2001;19:683-765 PMID: 11244051
  41. Differential cytokine requirements for regulation of autoimmune gastritis and colitis by CD4(+)CD25(+) T cells.
    J Autoimmun. 2001 Mar;16(2):115-23 PMID: 11247637
  42. Inactivation of Notch 1 in immature thymocytes does not perturb CD4 or CD8T cell development.
    Nat Immunol. 2001 Mar;2(3):235-41 PMID: 11224523
  43. Relative contribution of interferon-gamma and interleukin-10 to resistance to murine African trypanosomosis.
    J Infect Dis. 2001 Jun 15;183(12):1794-800 PMID: 11372033
  44. Colitogenic Th1 cells are present in the antigen-experienced T cell pool in normal mice: control by CD4+ regulatory T cells and IL-10.
    J Immunol. 2003 Jul 15;171(2):971-8 PMID: 12847269
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
2004-11-15
Epub
2004-00-08
Pages
1289-97
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2211912
Subset
IM
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