Immunity to commensal skin fungi promotes psoriasiform skin inflammation

Under steady-state conditions, the immune system is poised to sense and respond to the microbiota. As such, immunity to the microbiota, including T cell responses, is expected to precede any inflammatory trigger. How this pool of preformed microbiotaspecific T cells contributes to tissue pathologies...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 117; no. 28; pp. 16465 - 16474
Main Authors Hurabielle, Charlotte, Link, Verena M., Bouladoux, Nicolas, Han, Seong-Ji, Merrill, Eric Dean, Lightfoot, Yaima L., Seto, Nickie, Bleck, Christopher K. E., Smelkinson, Margery, Harrison, Oliver J., Linehan, Jonathan L., Tamoutounour, Samira, Lionakis, Michail S., Kaplan, Mariana J., Nakajima, Saeko, Belkaid, Yasmine
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 14.07.2020
Subjects
Animals
Arthrodermataceae - classification
Arthrodermataceae - genetics
Arthrodermataceae - isolation & purification
Arthrodermataceae - physiology
Biological Sciences
Extracellular Traps - immunology
Extracellular Traps - microbiology
Female
Fungi
Helper cells
Humans
Immune system
Immunity
Inflammation
Lymphocytes
Lymphocytes T
Male
Mice
Mice, Inbred C57BL
Microbiota
Psoriasis
Psoriasis - immunology
Psoriasis - microbiology
Psoriasis - pathology
Recall
Skin - immunology
Skin - microbiology
Skin - pathology
Skin diseases
Symbiosis
Th17 Cells - immunology
Tissues
Transcription
microbiota
skin
fungi
Th17
psoriasis
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Summary:Under steady-state conditions, the immune system is poised to sense and respond to the microbiota. As such, immunity to the microbiota, including T cell responses, is expected to precede any inflammatory trigger. How this pool of preformed microbiotaspecific T cells contributes to tissue pathologies remains unclear. Here, using an experimental model of psoriasis, we show that recall responses to commensal skin fungi can significantly aggravate tissue inflammation. Enhanced pathology caused by fungi preexposure depends on Th17 responses and neutrophil extracellular traps and recapitulates features of the transcriptional landscape of human lesional psoriatic skin. Together, our results propose that recall responses directed to skin fungi can directly promote skin inflammation and that exploration of tissue inflammation should be assessed in the context of recall responses to the microbiota.
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2Present address: L’Oréal Advanced Research, L’Oréal Research and Innovation, 93600 Aulnay-sous-Bois, France.
1C.H. and V.M.L. contributed equally to this work.
Reviewers: D.K., University of Pittsburgh; and E.V.S.-B., University of Cologne.
Author contributions: C.H., V.M.L., S.N., and Y.B. designed research; C.H., V.M.L., N.B., S.-J.H., E.D.M., Y.L.L., N.S., C.K.E.B., M.S., O.J.H., J.L.L., S.T., and S.N. performed research; M.S.L. and M.J.K. contributed new reagents/analytic tools; C.H., V.M.L., N.B., S.-J.H., E.D.M., Y.L.L., N.S., C.K.E.B., M.S., O.J.H., S.T., and S.N. analyzed data; and C.H., V.M.L., S.N., and Y.B. wrote the paper.
Contributed by Yasmine Belkaid, May 17, 2020 (sent for review February 24, 2020; reviewed by Daniel Kaplan and Esther von Stebut-Borschitz)
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2003022117