IgG and IgE collaboratively accelerate expulsion of Strongyloides venezuelensis in a primary infection

Infect Immun. 2013 Jul;81(7):2518-27. doi: 10.1128/IAI.00285-13. Epub 2013 Apr 29.

Abstract

The host deploys a subset of immune responses to expel helminths, which differs depending on the nature of the helminth. Strongyloides venezuelensis, a counterpart of the human pathogen S. stercoralis, naturally infects rodents and has been used as an experimental model. Here we show that induction of immunoglobulin G (IgG) and IgE is a prerequisite for rapid expulsion of S. venezuelensis during a primary infection. Activation-induced cytidine deaminase-deficient (AID(-/-)) mice, which lack the ability to switch IgM to other isotypes, normally developed T-helper 2 (Th2) cells and intestinal mastocytosis after infection with S. venezuelensis. Although AID(-/-) mice expelled Nippostrongylus brasiliensis normally, they required a much longer period to expel S. venezuelensis than wild-type (WT) mice. Adoptive transfers of immune sera from S. venezuelensis-infected but not N. brasiliensis-infected mice restored the ability of AID(-/-) mice to promptly expel S. venezuelensis. Immune serum-derived IgG and IgE induced worm expulsion via Fc γ receptor III (FcγRIII) and Fc ε receptor I (FcεRI), respectively, and a mixture of IgG and IgE showed collaborative effects. Whereas FcγRIII(-/-) mice or FcεRIα(-/-) mice normally could expel S. venezuelensis, FcγRIII(-/-) mice, when their IgE was neutralized by anti-IgE, or FcεRIα(-/-) mice, when their IgG binding to FcγRIII was blocked by anti-FcγRIII, showed a markedly reduced ability to expel S. venezuelensis. These data reveal that IgG and IgE play redundant roles but act in concert to accelerate S. venezuelensis expulsion. Mast cell-deficient mice, even those equipped with immune serum-derived IgG or IgE, failed to expel S. venezuelensis promptly, suggesting that mast cells are cellular targets of IgG and IgE.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Proliferation
  • Immunization, Passive
  • Immunoglobulin Class Switching
  • Immunoglobulin E / administration & dosage
  • Immunoglobulin E / immunology*
  • Immunoglobulin G / administration & dosage
  • Immunoglobulin G / immunology*
  • Mast Cells / immunology
  • Mast Cells / parasitology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nippostrongylus / immunology
  • Protein Binding
  • Rats
  • Rats, Sprague-Dawley
  • Rats, Wistar
  • Receptors, IgE / immunology
  • Receptors, IgG / immunology
  • Strongylida Infections / immunology
  • Strongyloides / immunology*
  • Strongyloidiasis / immunology*
  • Strongyloidiasis / prevention & control
  • Th2 Cells / immunology

Substances

  • FcepsilonRIalpha protein, mouse
  • Fcgr3 protein, mouse
  • Immunoglobulin G
  • Receptors, IgE
  • Receptors, IgG
  • Immunoglobulin E