Skin damage signals mediate allergic sensitization to spatially unlinked antigen

Our current understanding of immunity to pathogens suggests that anatomic coupling of antigens with danger signals is a required feature for the formation of immune memory. However, in the context of pathogen-independent inflammation, the stringency of this anatomical coupling is unclear. Here, we demonstrate that multiple modes of skin injury were sufficient to induce a humoral response to antigens introduced in the gut. Skin damage induced a narrow subset of endocrine cytokines that were necessary and sufficient for the priming of antigens introduced at various distal tissues. Thus, in addition to "local priming" of antigen entering through damaged skin, there also exists another paradigm of "remote priming" where anatomical coupling is not essential because of the dissemination of damage-associated intermediaries. Our findings have implications for understanding the fundamental mechanisms of the formation of humoral memory with wide implications for diseases such as food allergy and in vaccinology.

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Publication Details

Journal
Science Immunology
Published
2025-04-04
DOI
https://doi.org/10.1126/sciimmunol.adn0688
Citations
10
Primary Topic
Asthma and respiratory diseases
Type
article
Field-Weighted Citation Impact
11.64
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article

Skin damage signals mediate allergic sensitization to spatially unlinked antigen

Kavita Israni-Winger, Joseph Craft, Noah W. Palm, Kenneth Zhou et al.
10 citations
Science Immunology
Asthma and respiratory diseases
11.64
article

Skin damage signals mediate allergic sensitization to spatially unlinked antigen

Kavita Israni-Winger, Joseph Craft, Noah W. Palm, Kenneth Zhou, Anna Eisenstein, Ruslan M. Medzhitov, Anjelica Martin, Pierre Launay, Yifan Ma, Daniel A. Waizman, Michaël F. Michieletto, Jorge Henao‐Mejia, Andrew Wang, Cuiling Zhang, Isabela Brown‐Soler
article en
10 citations

Abstract

Our current understanding of immunity to pathogens suggests that anatomic coupling of antigens with danger signals is a required feature for the formation of immune memory. However, in the context of pathogen-independent inflammation, the stringency of this anatomical coupling is unclear. Here, we demonstrate that multiple modes of skin injury were sufficient to induce a humoral response to antigens introduced in the gut. Skin damage induced a narrow subset of endocrine cytokines that were necessary and sufficient for the priming of antigens introduced at various distal tissues. Thus, in addition to "local priming" of antigen entering through damaged skin, there also exists another paradigm of "remote priming" where anatomical coupling is not essential because of the dissemination of damage-associated intermediaries. Our findings have implications for understanding the fundamental mechanisms of the formation of humoral memory with wide implications for diseases such as food allergy and in vaccinology.

Science ImmunologyVol. 10(106)
Centre National de la Recherche Scientifique (FR), Children's Hospital of Philadelphia (US), Inserm (FR), Université Paris Cité (FR), Yale University (US), Centre de Recherche sur l'Inflammation (FR), University of Pennsylvania (US)
Zero hunger
Openalex Percentile: Top 1%
Asthma and respiratory diseases
11.64
DOIOpen Access PDFOpenAlex
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