Cited by 264Dermatology and Skin DiseasesPsoriasis: Treatment and PathogenesisAntimicrobial Resistance in Staphylococcus

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

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Liu, Haiyun, Archer, Nathan K., Dillen, Carly A., Wang, Yu, Ashbaugh, Alyssa G., Ortines, Roger V., Kao, Tracy, Lee, Steven K., Cai, Shuting S., Miller, Robert J., Marchitto, Mark C., Zhang, Emily, Riggins, Daniel P., Plaut, Roger D., Stibitz, Scott, Geha, Raif S., Miller, Lloyd S.·2017·Cell Host & Microbe

DOI 10.1016/j.chom.2017.10.006PMC PMC5774218

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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.

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Authors: Liu, H., Archer, N. K., Dillen, C. A., Wang, Y., Ashbaugh, A. G., Ortines, R. V., Kao, T., Lee, S. K., Cai, S. S., Miller, R. J., Marchitto, M. C., Zhang, E., Riggins, D. P., Plaut, R. D., Stibitz, S., Geha, R. S., & Miller, L. S.
Affiliations: Johns Hopkins University (US)
Center for Biologics Evaluation and Research (US)
Boston Children's Hospital (US)
Corresponding author: Miller, Lloyd S.
ORCID: Liu, Haiyun
Archer, Nathan K.
Dillen, Carly A.
Wang, Yu
Ashbaugh, Alyssa G.
Ortines, Roger V.
Cai, Shuting S.
Miller, Robert J.
Marchitto, Mark C.
Riggins, Daniel P.
Plaut, Roger D.
Geha, Raif S.
Miller, Lloyd S.
Venue: Cell Host & Microbe
Publisher: Elsevier BV
Published: 2017-11
Volume: 22
Issue: 5
Pages: 653-666.e5
ISSN: 1931-3128 (ISSN-L)
DOI: 10.1016/j.chom.2017.10.006
PMC: PMC5774218
OpenAlex: W2767217104
Cited by: 263
References: 64
Citations by year: 2026: 26 · 2025: 27 · 2024: 41 · 2023: 33 · 2022: 30 · 2021: 29 · 2020: 27 · 2019: 31 · 2018: 16 · 2017: 3
FWCI: 23.92
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 372 d)
Locations: Cell Host & Microbe (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Allergy and Infectious Diseases (UM2AI117870)
NIH (R01AR069502)
Pfizer (WI214880)
Topics: Health Sciences › Medicine › Dermatology › Dermatology and Skin Diseases
Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
Keywords: Staphylococcus aureus, skin inflammation, IL-36, IL-36 receptor, MyD88 signaling, IL-17, γδ T cells, CD4+ T cells, staphylococcal virulence factors, atopic dermatitis, IL-1β, intradermal challenge, adoptive transfer
MeSH terms: Interleukin-33, Animals, Bacterial Toxins, Dermatitis, Atopic, Disease Models, Animal, Female, Hemolysin Proteins, Host-Parasite Interactions, Inflammation, Interleukin-1, Male, Mice, Inbred BALB C, Skin, Staphylococcal Infections, Staphylococcus aureus, T-Lymphocytes, CD4-Positive T-Lymphocytes, Cytokines, Receptors, Interleukin-1, Interleukin-17, Interleukin-18, Virulence Factors, Mice, Interleukin-1alpha, Interleukin-1beta, Myeloid Differentiation Factor 88

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

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