Homeostatic IL-13 in healthy skin directs dendritic cell differentiation to promote TH2 and inhibit TH17 cell polarization

The signals driving the adaptation of type 2 dendritic cells (DC2s) to diverse peripheral environments remain mostly undefined. We show that differentiation of CD11b lo migratory DC2s—a DC2 population unique to the dermis—required IL-13 signaling dependent on the transcription factors STAT6 and KLF4...

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Published inNature immunology Vol. 22; no. 12; pp. 1538 - 1550
Main Authors Mayer, Johannes U., Hilligan, Kerry L., Chandler, Jodie S., Eccles, David A., Old, Samuel I., Domingues, Rita G., Yang, Jianping, Webb, Greta R., Munoz-Erazo, Luis, Hyde, Evelyn J., Wakelin, Kirsty A., Tang, Shiau-Choot, Chappell, Sally C., von Daake, Sventja, Brombacher, Frank, Mackay, Charles R., Sher, Alan, Tussiwand, Roxane, Connor, Lisa M., Gallego-Ortega, David, Jankovic, Dragana, Le Gros, Graham, Hepworth, Matthew R., Lamiable, Olivier, Ronchese, Franca
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.12.2021
Nature Publishing Group
Subjects
631/250/2152/1566
631/250/2504/133/2505
631/250/2504/2506
Allergens
Biomedical and Life Sciences
Biomedicine
CD11b antigen
Cell differentiation
Dendritic cells
Dermis
GATA-3 protein
Helper cells
Immunology
Infectious Diseases
Interleukin 13
Interleukin 17
Interleukin 4
KLF4 protein
Lungs
Lymphocytes T
Lymphoid cells
Microbiota
Skin
Small intestine
Spleen
Stat6 protein
Thymic stromal lymphopoietin
Transcription factors
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Abstract The signals driving the adaptation of type 2 dendritic cells (DC2s) to diverse peripheral environments remain mostly undefined. We show that differentiation of CD11b lo migratory DC2s—a DC2 population unique to the dermis—required IL-13 signaling dependent on the transcription factors STAT6 and KLF4, whereas DC2s in lung and small intestine were STAT6-independent. Similarly, human DC2s in skin expressed an IL-4 and IL-13 gene signature that was not found in blood, spleen and lung DCs. In mice, IL-13 was secreted homeostatically by dermal innate lymphoid cells and was independent of microbiota, TSLP or IL-33. In the absence of IL-13 signaling, dermal DC2s were stable in number but remained CD11b hi and showed defective activation in response to allergens, with diminished ability to support the development of IL-4 + GATA3 + helper T cells (T H ), whereas antifungal IL-17 + RORγt + T H cells were increased. Therefore, homeostatic IL-13 fosters a noninflammatory skin environment that supports allergic sensitization. Ronchese and colleagues show that IL-13 secreted homeostatically by dermal ILCs contributes to the differentiation of a CD11b lo type 2 dendritic cell subset, which supports the development of T H 2 cells and curtails the development of T H 17 cells in the skin of mice and humans.
AbstractList The signals driving the adaptation of type 2 dendritic cells (DC2s) to diverse peripheral environments remain mostly undefined. We show that differentiation of CD11blo migratory DC2s—a DC2 population unique to the dermis—required IL-13 signaling dependent on the transcription factors STAT6 and KLF4, whereas DC2s in lung and small intestine were STAT6-independent. Similarly, human DC2s in skin expressed an IL-4 and IL-13 gene signature that was not found in blood, spleen and lung DCs. In mice, IL-13 was secreted homeostatically by dermal innate lymphoid cells and was independent of microbiota, TSLP or IL-33. In the absence of IL-13 signaling, dermal DC2s were stable in number but remained CD11bhi and showed defective activation in response to allergens, with diminished ability to support the development of IL-4+GATA3+ helper T cells (TH), whereas antifungal IL-17+RORγt+ TH cells were increased. Therefore, homeostatic IL-13 fosters a noninflammatory skin environment that supports allergic sensitization.Ronchese and colleagues show that IL-13 secreted homeostatically by dermal ILCs contributes to the differentiation of a CD11blo type 2 dendritic cell subset, which supports the development of TH2 cells and curtails the development of TH17 cells in the skin of mice and humans.
The signals driving the adaptation of type 2 dendritic cells (DC2s) to diverse peripheral environments remain mostly undefined. We show that differentiation of CD11b lo migratory DC2s—a DC2 population unique to the dermis—required IL-13 signaling dependent on the transcription factors STAT6 and KLF4, whereas DC2s in lung and small intestine were STAT6-independent. Similarly, human DC2s in skin expressed an IL-4 and IL-13 gene signature that was not found in blood, spleen and lung DCs. In mice, IL-13 was secreted homeostatically by dermal innate lymphoid cells and was independent of microbiota, TSLP or IL-33. In the absence of IL-13 signaling, dermal DC2s were stable in number but remained CD11b hi and showed defective activation in response to allergens, with diminished ability to support the development of IL-4 + GATA3 + helper T cells (T H ), whereas antifungal IL-17 + RORγt + T H cells were increased. Therefore, homeostatic IL-13 fosters a noninflammatory skin environment that supports allergic sensitization. Ronchese and colleagues show that IL-13 secreted homeostatically by dermal ILCs contributes to the differentiation of a CD11b lo type 2 dendritic cell subset, which supports the development of T H 2 cells and curtails the development of T H 17 cells in the skin of mice and humans.
The signals driving the adaptation of type 2 dendritic cells (DC2s) to diverse peripheral environments remain mostly undefined. We show that differentiation of CD11blo migratory DC2s-a DC2 population unique to the dermis-required IL-13 signaling dependent on the transcription factors STAT6 and KLF4, whereas DC2s in lung and small intestine were STAT6-independent. Similarly, human DC2s in skin expressed an IL-4 and IL-13 gene signature that was not found in blood, spleen and lung DCs. In mice, IL-13 was secreted homeostatically by dermal innate lymphoid cells and was independent of microbiota, TSLP or IL-33. In the absence of IL-13 signaling, dermal DC2s were stable in number but remained CD11bhi and showed defective activation in response to allergens, with diminished ability to support the development of IL-4+GATA3+ helper T cells (TH), whereas antifungal IL-17+RORγt+ TH cells were increased. Therefore, homeostatic IL-13 fosters a noninflammatory skin environment that supports allergic sensitization.
Author Mackay, Charles R.
Gallego-Ortega, David
Yang, Jianping
Mayer, Johannes U.
Hilligan, Kerry L.
Connor, Lisa M.
Ronchese, Franca
Chandler, Jodie S.
Tussiwand, Roxane
von Daake, Sventja
Chappell, Sally C.
Le Gros, Graham
Old, Samuel I.
Wakelin, Kirsty A.
Brombacher, Frank
Munoz-Erazo, Luis
Tang, Shiau-Choot
Hepworth, Matthew R.
Hyde, Evelyn J.
Eccles, David A.
Jankovic, Dragana
Webb, Greta R.
Lamiable, Olivier
Domingues, Rita G.
Sher, Alan
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Copyright The Author(s), under exclusive licence to Springer Nature America, Inc. 2021. corrected publication 2022
The Author(s), under exclusive licence to Springer Nature America, Inc. 2021. corrected publication 2022.
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  year: 2019
  ident: 1067_CR1
  publication-title: Nat. Rev. Immunol.
  doi: 10.1038/s41577-018-0088-1
  contributor:
    fullname: SC Eisenbarth
– volume: 98
  start-page: 807
  year: 2020
  ident: 1067_CR20
  publication-title: Immunol. Cell Biol.
  doi: 10.1111/imcb.12387
  contributor:
    fullname: O Lamiable
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Snippet The signals driving the adaptation of type 2 dendritic cells (DC2s) to diverse peripheral environments remain mostly undefined. We show that differentiation of...
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SubjectTerms 631/250/2152/1566
631/250/2504/133/2505
631/250/2504/2506
Allergens
Biomedical and Life Sciences
Biomedicine
CD11b antigen
Cell differentiation
Dendritic cells
Dermis
GATA-3 protein
Helper cells
Immunology
Infectious Diseases
Interleukin 13
Interleukin 17
Interleukin 4
KLF4 protein
Lungs
Lymphocytes T
Lymphoid cells
Microbiota
Skin
Small intestine
Spleen
Stat6 protein
Thymic stromal lymphopoietin
Transcription factors
Title Homeostatic IL-13 in healthy skin directs dendritic cell differentiation to promote TH2 and inhibit TH17 cell polarization
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Volume 22
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