Intrinsic functional defects of type 2 innate lymphoid cells impair innate allergic inflammation in promyelocytic leukemia zinc finger (PLZF)-deficient mice

J Allergy Clin Immunol. 2016 Feb;137(2):591-600.e1. doi: 10.1016/j.jaci.2015.07.050. Epub 2015 Oct 23.

Abstract

Background: The transcription factor promyelocytic leukemia zinc finger (PLZF) is transiently expressed during development of type 2 innate lymphoid cells (ILC2s) but is not present at the mature stage. We hypothesized that PLZF-deficient ILC2s have functional defects in the innate allergic response and represent a tool for studying innate immunity in a mouse with a functional adaptive immune response.

Objective: We determined the consequences of PLZF deficiency on ILC2 function in response to innate and adaptive immune stimuli by using PLZF(-/-) mice and mixed wild-type:PLZF(-/-) bone marrow chimeras.

Methods: PLZF(-/-) mice, wild-type littermates, or mixed bone marrow chimeras were treated with the protease allergen papain or the cytokines IL-25 and IL-33 or infected with the helminth Nippostrongylus brasiliensis to induce innate type 2 allergic responses. Mice were sensitized with intraperitoneal ovalbumin-alum, followed by intranasal challenge with ovalbumin alone, to induce adaptive TH2 responses. Lungs were analyzed for immune cell subsets, and alveolar lavage fluid was analyzed for ILC2-derived cytokines. In addition, ILC2s were stimulated ex vivo for their capacity to release type 2 cytokines.

Results: PLZF-deficient lung ILC2s exhibit a cell-intrinsic defect in the secretion of IL-5 and IL-13 in response to innate stimuli, resulting in defective recruitment of eosinophils and goblet cell hyperplasia. In contrast, the adaptive allergic inflammatory response to ovalbumin and alum was unimpaired.

Conclusions: PLZF expression at the innate lymphoid cell precursor stage has a long-range effect on the functional properties of mature ILC2s and highlights the importance of these cells for innate allergic responses in otherwise immunocompetent mice.

Keywords: Allergic mechanisms; innate lymphoid cells; mouse models.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adaptive Immunity / genetics
  • Adaptive Immunity / immunology
  • Adoptive Transfer
  • Allergens / immunology
  • Animals
  • Antigens, Surface / metabolism
  • Biomarkers
  • Bone Marrow Transplantation
  • Bronchoalveolar Lavage Fluid / immunology
  • Cytokines / metabolism
  • Disease Models, Animal
  • Helminthiasis / genetics
  • Helminthiasis / immunology
  • Helminthiasis / pathology
  • Helminths / immunology
  • Hypersensitivity / drug therapy
  • Hypersensitivity / genetics*
  • Hypersensitivity / immunology*
  • Hypersensitivity / pathology
  • Immunity, Innate / genetics*
  • Immunophenotyping
  • Interleukin-33 / administration & dosage
  • Interleukin-33 / pharmacology
  • Interleukins / administration & dosage
  • Interleukins / pharmacology
  • Kruppel-Like Transcription Factors / deficiency
  • Kruppel-Like Transcription Factors / genetics*
  • Lymphocyte Activation
  • Lymphocyte Subsets / drug effects
  • Lymphocyte Subsets / immunology*
  • Lymphocyte Subsets / metabolism*
  • Mice
  • Mice, Knockout
  • Ovalbumin / immunology
  • Papain / administration & dosage
  • Papain / pharmacology
  • Promyelocytic Leukemia Zinc Finger Protein
  • Pulmonary Eosinophilia / genetics
  • Pulmonary Eosinophilia / immunology
  • Pulmonary Eosinophilia / pathology
  • Th2 Cells / immunology
  • Th2 Cells / metabolism

Substances

  • Allergens
  • Antigens, Surface
  • Biomarkers
  • Cytokines
  • Interleukin-33
  • Interleukins
  • Kruppel-Like Transcription Factors
  • Mydgf protein, mouse
  • Promyelocytic Leukemia Zinc Finger Protein
  • Zbtb16 protein, mouse
  • Ovalbumin
  • Papain