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The skin environment controls local dendritic cell differentiation and function through innate IL-13

View ORCID ProfileJohannes U Mayer, View ORCID ProfileOlivier Lamiable, View ORCID ProfileKerry L Hilligan, View ORCID ProfileJodie S Chandler, View ORCID ProfileSamuel I Old, View ORCID ProfileDavid A Eccles, View ORCID ProfileJianping Yang, Greta R Webb, Rita G Domingues, View ORCID ProfileLuis Munoz-Erazo, View ORCID ProfileKirsty A Wakelin, View ORCID ProfileEvelyn J Hyde, View ORCID ProfileShiau-Choot Tang, Sally C Chappell, View ORCID ProfileCharles R Mackay, View ORCID ProfileFrank Brombacher, View ORCID ProfileAlan Sher, View ORCID ProfileRoxane Tussiwand, View ORCID ProfileLisa M Connor, Dragana Jankovic, View ORCID ProfileMatthew R Hepworth, View ORCID ProfileGraham Le Gros, View ORCID ProfileFranca Ronchese
doi: https://doi.org/10.1101/2021.01.05.425466
Johannes U Mayer
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Olivier Lamiable
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Kerry L Hilligan
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
2Immunobiology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda 20892 MD, USA
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Jodie S Chandler
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Samuel I Old
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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David A Eccles
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Jianping Yang
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Greta R Webb
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Rita G Domingues
3Lydia Becker Institute of Immunology and Inflammation, Manchester Collaborative Centre for Inflammation Research, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK
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Luis Munoz-Erazo
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Kirsty A Wakelin
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Evelyn J Hyde
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Shiau-Choot Tang
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Sally C Chappell
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Charles R Mackay
4Infection and Immunity Program, Monash Biomedicine Discovery Institute, Monash University, Melbourne, Australia
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Frank Brombacher
5International Centre for Genetic Engineering and Biotechnology (ICGEB), Cape Town component & Institute of Infectious Diseases and Molecular Medicine (IDM), Division of Immunology, Health Science Faculty, University of Cape Town, South Africa
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Alan Sher
2Immunobiology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda 20892 MD, USA
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Roxane Tussiwand
6Department of Biomedicine, University of Basel, 4058 Basel, Switzerland
7Immune Regulation Unit, National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda 20892 MD, USA
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Lisa M Connor
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
8School of Biological Sciences, Victoria University of Wellington, Wellington 6012, New Zealand
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Dragana Jankovic
9Immunoparasitology Unit, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda 20892 MD, USA
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Matthew R Hepworth
3Lydia Becker Institute of Immunology and Inflammation, Manchester Collaborative Centre for Inflammation Research, Faculty of Biology, Medicine and Health, University of Manchester, Manchester Academic Health Science Centre, Manchester, UK
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Graham Le Gros
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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Franca Ronchese
1Malaghan Institute of Medical Research, Wellington 6012, New Zealand
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  • For correspondence: fronchese@malaghan.org.nz
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ABSTRACT

The signals driving the adaptation of type-2 dendritic cells (DC2s) to diverse peripheral environments are not well understood. We show that the development of CD11blow migratory DC2s, a DC2 population unique to the dermis, requires STAT6- and KLF4-dependent IL-13 signaling, whereas DC2s in lung and small intestine are STAT6-independent. Dermal IL-13 is mostly derived from innate lymphoid cells expressing a resting ICOS+ KLRG1-ST2-phenotype. Analysis of public datasets indicates that human skin DC2s also express an IL-4/IL-13 gene signature compared to blood or spleen, suggesting a similar developmental pathway in mice and humans. In the absence of IL-13 signaling, dermal DC2s are stable in number but remain CD11bhi and show defective activation in response to allergen with diminished ability to support IL-4+ GATA3+ Th development, whereas anti-fungal IL-17+ RORγt+ responses are increased. Thus, steady-state IL-13 fosters a non-inflammatory and pro-allergic environment in healthy skin via conditioning of local DC2s.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵** Lead contact.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 06, 2021.
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The skin environment controls local dendritic cell differentiation and function through innate IL-13
Johannes U Mayer, Olivier Lamiable, Kerry L Hilligan, Jodie S Chandler, Samuel I Old, David A Eccles, Jianping Yang, Greta R Webb, Rita G Domingues, Luis Munoz-Erazo, Kirsty A Wakelin, Evelyn J Hyde, Shiau-Choot Tang, Sally C Chappell, Charles R Mackay, Frank Brombacher, Alan Sher, Roxane Tussiwand, Lisa M Connor, Dragana Jankovic, Matthew R Hepworth, Graham Le Gros, Franca Ronchese
bioRxiv 2021.01.05.425466; doi: https://doi.org/10.1101/2021.01.05.425466
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The skin environment controls local dendritic cell differentiation and function through innate IL-13
Johannes U Mayer, Olivier Lamiable, Kerry L Hilligan, Jodie S Chandler, Samuel I Old, David A Eccles, Jianping Yang, Greta R Webb, Rita G Domingues, Luis Munoz-Erazo, Kirsty A Wakelin, Evelyn J Hyde, Shiau-Choot Tang, Sally C Chappell, Charles R Mackay, Frank Brombacher, Alan Sher, Roxane Tussiwand, Lisa M Connor, Dragana Jankovic, Matthew R Hepworth, Graham Le Gros, Franca Ronchese
bioRxiv 2021.01.05.425466; doi: https://doi.org/10.1101/2021.01.05.425466

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