Staphylococcus aureus Epicutaneous Exposure Drives Skin Inflammation via IL-36-Mediated T Cell Responses

Cell Host Microbe. 2017 Nov 8;22(5):653-666.e5. doi: 10.1016/j.chom.2017.10.006.

Abstract

Staphylococcus aureus colonization contributes to skin inflammation in diseases such as atopic dermatitis, but the signaling pathways involved are unclear. Herein, epicutaneous S. aureus exposure to mouse skin promoted MyD88-dependent skin inflammation initiated by IL-36, but not IL-1α/β, IL-18, or IL-33. By contrast, an intradermal S. aureus challenge promoted MyD88-dependent host defense initiated by IL-1β rather than IL-36, suggesting that different IL-1 cytokines trigger MyD88 signaling depending on the anatomical depth of S. aureus cutaneous exposure. The bacterial virulence factor PSMα, but not α-toxin or δ-toxin, contributed to the skin inflammation, which was driven by IL-17-producing γδ and CD4+ T cells via direct IL-36R signaling in the T cells. Finally, adoptive transfer of IL-36R-expressing T cells to IL-36R-deficient mice was sufficient for mediating S. aureus-induced skin inflammation. Together, this study defines a previously unknown pathway by which S. aureus epicutaneous exposure promotes skin inflammation involving IL-36R/MyD88-dependent IL-17 T cell responses.

Keywords: IL-17; IL-36; Staphylococcus aureus; T cell; atopic dermatitis; cutaneous; epicutaneous; inflammation; phenol soluble modulin; skin.

MeSH terms

  • Animals
  • Bacterial Toxins / immunology
  • CD4-Positive T-Lymphocytes / immunology
  • Cytokines / metabolism
  • Dermatitis, Atopic / immunology*
  • Dermatitis, Atopic / microbiology
  • Dermatitis, Atopic / pathology
  • Disease Models, Animal
  • Female
  • Hemolysin Proteins / immunology
  • Host-Parasite Interactions / immunology
  • Inflammation / immunology*
  • Inflammation / pathology
  • Interleukin-1 / immunology*
  • Interleukin-17
  • Interleukin-18 / metabolism
  • Interleukin-1alpha / metabolism
  • Interleukin-1beta / metabolism
  • Interleukin-33 / metabolism
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Myeloid Differentiation Factor 88 / metabolism
  • Receptors, Interleukin-1 / metabolism
  • Skin / immunology*
  • Skin / microbiology
  • Skin / pathology
  • Staphylococcal Infections / immunology*
  • Staphylococcal Infections / pathology
  • Staphylococcus aureus / pathogenicity*
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / microbiology
  • Virulence Factors / immunology

Substances

  • Bacterial Toxins
  • Cytokines
  • Hemolysin Proteins
  • Il33 protein, mouse
  • Interleukin-1
  • Interleukin-17
  • Interleukin-18
  • Interleukin-1alpha
  • Interleukin-1beta
  • Interleukin-33
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Receptors, Interleukin-1
  • Virulence Factors
  • interleukin-36 receptor, mouse
  • interleukin-36, mouse
  • staphylococcal alpha-toxin
  • staphylococcal delta toxin