Depletion of CD4+CD25+ T cells switches the whey-allergic response from immunoglobulin E- to immunoglobulin free light chain-dependent

Clin Exp Allergy. 2010 Sep;40(9):1414-21. doi: 10.1111/j.1365-2222.2010.03500.x. Epub 2010 Apr 19.

Abstract

Background: Symptoms of allergy are largely attributed to an IgE-mediated hypersensitivity response. However, a considerable number of patients also exhibit clinical features of allergy without detectable systemic IgE. Previous work showed that Ig-free light chains (IgLC) may act as an alternate mechanism to induce allergic responses. CD4+CD25+ T cells are crucial in the initiation and regulation of allergic responses and compromised function might affect the response to allergens.

Objective: To examine the contribution of CD4+CD25+ T cells and IgLC towards the whey-allergic response.

Methods: Mice were sensitized orally with whey using cholera toxin as an adjuvant. CD25+ T cells were depleted in vivo using a CD25 mAb. The acute allergic skin response to whey and ex vivo colon reactivity was measured in the presence or absence of F991, a specific inhibitor of IgLC. Serum whey-specific antibodies and IgLC in serum and mesenteric lymph node (MLN) supernatants were measured. Depletion of CD4+CD25+ T cells was confirmed in the spleen.

Results: Anti-CD25 treatment strongly reduced whey-specific antibody levels and resulted in a partial depletion of effector T cells and a major depletion of Foxp3(+) regulatory T cells. Surprisingly, despite the abolished specific IgE response, the acute allergic skin response to whey was not affected. IgLC levels were enhanced in the serum and MLN supernatants of CD25-depleted sensitized mice. F991 inhibited the acute skin response and colon hyperreactivity in anti-CD25-treated mice, indicating that these responses were mainly IgLC dependent.

Conclusions: Depletion of CD4+CD25+ T cells resulted in a switch from an IgE- to an IgLC-dependent acute skin response and functional hyperresponsiveness of the colon. Our data suggest that CD25+ T cells play a crucial role in balancing cow's milk allergy between IgE and IgE-independent responses and both mechanisms might play a role in allergic responses to the same allergen.

MeSH terms

  • Animals
  • CD4-Positive T-Lymphocytes / immunology*
  • Cattle
  • Immunoglobulin E / immunology*
  • Immunoglobulin kappa-Chains / immunology*
  • Immunoglobulin lambda-Chains / immunology*
  • Interleukin-2 Receptor alpha Subunit / immunology
  • Lymph Nodes / immunology
  • Lymphocyte Depletion*
  • Mesentery
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C3H
  • Milk Hypersensitivity / immunology*
  • Milk Proteins / adverse effects
  • Milk Proteins / immunology
  • Whey Proteins

Substances

  • Immunoglobulin kappa-Chains
  • Immunoglobulin lambda-Chains
  • Interleukin-2 Receptor alpha Subunit
  • Milk Proteins
  • Whey Proteins
  • Immunoglobulin E