Critical Role for Interleukin-25 in Host Protective Th2 Memory Response against Heligmosomoides polygyrus bakeri

Infect Immun. 2016 Nov 18;84(12):3328-3337. doi: 10.1128/IAI.00180-16. Print 2016 Dec.

Abstract

Infection with parasitic nematodes, especially gastrointestinal geohelminths, affects hundreds of millions of people worldwide and thus poses a major risk to global health. The host mechanism of defense against enteric nematode infection remains to be fully understood, but it involves a polarized type 2 immunity leading to alterations in intestinal function that facilitate worm expulsion. We investigated the role of interleukin-25 (IL-25) in host protection against Heligmosomoides polygyrus bakeri infection in mice. Our results showed that Il25 and its receptor subunit, Il17rb, were upregulated during a primary infection and a secondary challenge infection with H. polygyrus bakeri Genetic deletion of IL-25 (IL-25-/-) led to an attenuated type 2 cytokine response and increased worm fecundity in mice with a primary H. polygyrus bakeri infection. In addition, the full spectrum of the host memory response against a secondary infection with H. polygyrus bakeri was severely impaired in IL-25-/- mice, including delayed type 2 cytokine responses, an attenuated functional response of the intestinal smooth muscle and epithelium, diminished intestinal smooth muscle hypertrophy/hyperplasia, and impaired worm expulsion. Furthermore, exogenous administration of IL-25 restored the host protective memory response against H. polygyrus bakeri infection in IL-25-/- mice. These data demonstrate that IL-25 is critical for host protective immunity against H. polygyrus bakeri infection, highlighting its potential application as a therapeutic agent against parasitic nematode infection worldwide.

MeSH terms

  • Animals
  • Arginase / genetics
  • Arginase / metabolism
  • Gene Expression Regulation / immunology
  • Hormones, Ectopic / genetics
  • Hormones, Ectopic / metabolism
  • Immunologic Memory / physiology*
  • Intercellular Signaling Peptides and Proteins
  • Interleukins / genetics
  • Interleukins / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nematospiroides dubius / immunology*
  • Receptors, Interleukin-17 / genetics
  • Receptors, Interleukin-17 / metabolism
  • Strongylida Infections / immunology
  • Strongylida Infections / veterinary*
  • Th2 Cells / physiology*
  • Up-Regulation

Substances

  • Hormones, Ectopic
  • Il17rb protein, mouse
  • Intercellular Signaling Peptides and Proteins
  • Interleukins
  • Mydgf protein, mouse
  • Receptors, Interleukin-17
  • Retnlb protein, mouse
  • Arg1 protein, mouse
  • Arginase