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Skin autonomous antibody production regulates host-microbiota interactions

Gribonika, Inta LU orcid ; Band, Victor I ; Chi, Liang ; Perez-Chaparro, Paula Juliana ; Link, Verena M ; Ansaldo, Eduard ; Oguz, Cihan ; Bousbaine, Djenet ; Fischbach, Michael A and Belkaid, Yasmine (2025) In Nature 638(8052). p.1043-1053
Abstract

The microbiota colonizes each barrier site and broadly controls host physiology1. However, when uncontrolled, microbial colonists can also promote inflammation and induce systemic infection2. The unique strategies used at each barrier tissue to control the coexistence of the host with its microbiota remain largely elusive. Here we uncover that, in the skin, host-microbiota symbiosis depends on the ability of the skin to act as an autonomous lymphoid organ. Notably, an encounter with a new skin commensal promotes two parallel responses, both under the control of Langerhans cells. On one hand, skin commensals induce the formation of classical germinal centres in the lymph node associated with immunoglobulin G1 (IgG1) and IgG3 antibody... (More)

The microbiota colonizes each barrier site and broadly controls host physiology1. However, when uncontrolled, microbial colonists can also promote inflammation and induce systemic infection2. The unique strategies used at each barrier tissue to control the coexistence of the host with its microbiota remain largely elusive. Here we uncover that, in the skin, host-microbiota symbiosis depends on the ability of the skin to act as an autonomous lymphoid organ. Notably, an encounter with a new skin commensal promotes two parallel responses, both under the control of Langerhans cells. On one hand, skin commensals induce the formation of classical germinal centres in the lymph node associated with immunoglobulin G1 (IgG1) and IgG3 antibody responses. On the other hand, microbial colonization also leads to the development of tertiary lymphoid organs in the skin that can locally sustain IgG2b and IgG2c responses. These phenomena are supported by the ability of regulatory T cells to convert into T follicular helper cells. Skin autonomous production of antibodies is sufficient to control local microbial biomass, as well as subsequent systemic infection with the same microorganism. Collectively, these results reveal a compartmentalization of humoral responses to the microbiota allowing for control of both microbial symbiosis and potential pathogenesis.

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author
; ; ; ; ; ; ; ; and
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Animals, Skin/immunology, Mice, Immunoglobulin G/immunology, Microbiota/immunology, Symbiosis/immunology, Female, Male, Germinal Center/immunology, Host Microbial Interactions/immunology, T-Lymphocytes, Regulatory/immunology, Antibody Formation/immunology, Langerhans Cells/immunology, Mice, Inbred C57BL, Lymph Nodes/immunology, T Follicular Helper Cells/immunology
in
Nature
volume
638
issue
8052
pages
11 pages
publisher
Nature Publishing Group
external identifiers
  • scopus:85212510619
  • pmid:39662506
ISSN
0028-0836
DOI
10.1038/s41586-024-08376-y
language
English
LU publication?
no
additional info
© 2024. The Author(s).
id
9cc03520-ad5b-4c53-8779-50df6ed495c1
date added to LUP
2025-12-20 13:20:29
date last changed
2025-12-22 14:39:54
@article{9cc03520-ad5b-4c53-8779-50df6ed495c1,
  abstract     = {{<p>The microbiota colonizes each barrier site and broadly controls host physiology1. However, when uncontrolled, microbial colonists can also promote inflammation and induce systemic infection2. The unique strategies used at each barrier tissue to control the coexistence of the host with its microbiota remain largely elusive. Here we uncover that, in the skin, host-microbiota symbiosis depends on the ability of the skin to act as an autonomous lymphoid organ. Notably, an encounter with a new skin commensal promotes two parallel responses, both under the control of Langerhans cells. On one hand, skin commensals induce the formation of classical germinal centres in the lymph node associated with immunoglobulin G1 (IgG1) and IgG3 antibody responses. On the other hand, microbial colonization also leads to the development of tertiary lymphoid organs in the skin that can locally sustain IgG2b and IgG2c responses. These phenomena are supported by the ability of regulatory T cells to convert into T follicular helper cells. Skin autonomous production of antibodies is sufficient to control local microbial biomass, as well as subsequent systemic infection with the same microorganism. Collectively, these results reveal a compartmentalization of humoral responses to the microbiota allowing for control of both microbial symbiosis and potential pathogenesis.</p>}},
  author       = {{Gribonika, Inta and Band, Victor I and Chi, Liang and Perez-Chaparro, Paula Juliana and Link, Verena M and Ansaldo, Eduard and Oguz, Cihan and Bousbaine, Djenet and Fischbach, Michael A and Belkaid, Yasmine}},
  issn         = {{0028-0836}},
  keywords     = {{Animals; Skin/immunology; Mice; Immunoglobulin G/immunology; Microbiota/immunology; Symbiosis/immunology; Female; Male; Germinal Center/immunology; Host Microbial Interactions/immunology; T-Lymphocytes, Regulatory/immunology; Antibody Formation/immunology; Langerhans Cells/immunology; Mice, Inbred C57BL; Lymph Nodes/immunology; T Follicular Helper Cells/immunology}},
  language     = {{eng}},
  number       = {{8052}},
  pages        = {{1043--1053}},
  publisher    = {{Nature Publishing Group}},
  series       = {{Nature}},
  title        = {{Skin autonomous antibody production regulates host-microbiota interactions}},
  url          = {{http://dx.doi.org/10.1038/s41586-024-08376-y}},
  doi          = {{10.1038/s41586-024-08376-y}},
  volume       = {{638}},
  year         = {{2025}},
}