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

Makoto Matsumoto, Yuki Sasaki, Koubun Yasuda, Toshiyuki Takai, Masamichi Muramatsu, Tomohiro Yoshimoto, Kenji Nakanishi

Research output: Contribution to journalArticlepeer-review

26 Citations (Scopus)

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 ∈ receptor I (Fc∈RI), respectively, and a mixture of IgG and IgE showed collaborative effects. Whereas FcγRIII-/- mice or Fc∈RIα-/- mice normally could expel S. venezuelensis, FcγRIII-/- mice, when their IgE was neutralized by anti-IgE, or Fc∈RIα-/- 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.

Original languageEnglish
Pages (from-to)2518-2527
Number of pages10
JournalInfection and immunity
Volume81
Issue number7
DOIs
Publication statusPublished - 2013 Jul

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Immunology
  • Infectious Diseases

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