HpARI Protein Secreted by a Helminth Parasite Suppresses Interleukin-33

Immunity. 2017 Oct 17;47(4):739-751.e5. doi: 10.1016/j.immuni.2017.09.015.

Abstract

Infection by helminth parasites is associated with amelioration of allergic reactivity, but mechanistic insights into this association are lacking. Products secreted by the mouse parasite Heligmosomoides polygyrus suppress type 2 (allergic) immune responses through interference in the interleukin-33 (IL-33) pathway. Here, we identified H. polygyrus Alarmin Release Inhibitor (HpARI), an IL-33-suppressive 26-kDa protein, containing three predicted complement control protein (CCP) modules. In vivo, recombinant HpARI abrogated IL-33, group 2 innate lymphoid cell (ILC2) and eosinophilic responses to Alternaria allergen administration, and diminished eosinophilic responses to Nippostrongylus brasiliensis, increasing parasite burden. HpARI bound directly to both mouse and human IL-33 (in the cytokine's activated state) and also to nuclear DNA via its N-terminal CCP module pair (CCP1/2), tethering active IL-33 within necrotic cells, preventing its release, and forestalling initiation of type 2 allergic responses. Thus, HpARI employs a novel molecular strategy to suppress type 2 immunity in both infection and allergy.

Keywords: IL-33; allergy; asthma; helminth; immunomodulation; parasite.

MeSH terms

  • Allergens / immunology
  • Alternaria / immunology
  • Amino Acid Sequence
  • Animals
  • Blotting, Western
  • Eosinophils / immunology
  • Helminth Proteins / genetics
  • Helminth Proteins / immunology*
  • Helminth Proteins / metabolism
  • Host-Parasite Interactions / immunology
  • Humans
  • Immunity, Innate / immunology
  • Interleukin-1 Receptor-Like 1 Protein
  • Interleukin-33 / genetics
  • Interleukin-33 / immunology*
  • Interleukin-33 / metabolism
  • Lymphocytes / immunology
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nematospiroides dubius / genetics
  • Nematospiroides dubius / immunology*
  • Nematospiroides dubius / metabolism
  • Protein Binding / immunology
  • Receptors, Interleukin / immunology
  • Receptors, Interleukin / metabolism
  • Sequence Homology, Amino Acid
  • Strongylida Infections / immunology*
  • Strongylida Infections / metabolism
  • Strongylida Infections / parasitology

Substances

  • Allergens
  • Helminth Proteins
  • Il1rl1 protein, mouse
  • Interleukin-1 Receptor-Like 1 Protein
  • Interleukin-33
  • Receptors, Interleukin