CD4+CD25+ T cell depletion impairs tolerance induction in a murine model of asthma

Clin Exp Allergy. 2009 Sep;39(9):1415-26. doi: 10.1111/j.1365-2222.2009.03314.x. Epub 2009 Jul 16.

Abstract

Background: Regulatory T cells (Tregs) are key players in controlling the development of airway inflammation. However, their role in the mechanisms leading to tolerance in established allergic asthma is unclear.

Objective: To examine the role of Tregs in tolerance induction in a murine model of asthma.

Methods: Ovalbumin (OVA) sensitized asthmatic mice were depleted or not of CD25(+) T cells by anti-CD25 PC61 monoclonal antibody (mAb) before intranasal treatment (INT) with OVA, then challenged with OVA aerosol. To further evaluate the respective regulatory activity of CD4(+)CD25(+) and CD4(+)CD25(-) T cells, both T cell subsets were transferred from tolerized or non-tolerized animals to asthmatic recipients. Bronchoalveolar lavage fluid (BALF), T cell proliferation and cytokine secretion were examined.

Results: Intranasal treatment with OVA led to increased levels of IL-10, TGF-beta and IL-17 in lung homogenates, inhibition of eosinophil recruitment into the BALF and antigen specific T cell hyporesponsiveness. CD4(+)CD25(+)Foxp3(+) T cells were markedly upregulated in lungs and suppressed in vitro and in vivo OVA-specific T cell responses. Depletion of CD25(+) cells before OVA INT severely hampered tolerance induction as indicated by a strong recruitment of eosinophils into BALF and a vigorous T cell response to OVA upon challenge. However, the transfer of CD4(+)CD25(-) T cells not only suppressed antigen specific T cell responsiveness but also significantly reduced eosinophil recruitment as opposed to CD4(+)CD25(+) T cells. As compared with control mice, a significantly higher proportion of CD4(+)CD25(-) T cells from OVA treated mice expressed mTGF-beta.

Conclusion: Both CD4(+)CD25(+) and CD4(+)CD25(-) T cells appear to be essential to tolerance induction. The relationship between both subsets and the mechanisms of their regulatory activity will have to be further analyzed.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / immunology
  • Antibodies, Monoclonal / pharmacology
  • Asthma / chemically induced
  • Asthma / immunology*
  • Asthma / metabolism
  • Bronchoalveolar Lavage
  • Cytokines / biosynthesis
  • Cytokines / immunology
  • Disease Models, Animal
  • Eosinophils / immunology
  • Eosinophils / metabolism
  • Female
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / immunology
  • Immune Tolerance*
  • Lymphocyte Depletion*
  • Mice
  • Mice, Inbred BALB C
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / immunology
  • T-Lymphocytes, Regulatory / immunology*
  • T-Lymphocytes, Regulatory / metabolism

Substances

  • Antibodies, Monoclonal
  • Cytokines
  • RNA, Messenger