Langerhans cells shape postnatal oral homeostasis in a mechanical-force-dependent but microbiota and IL17-independent manner
Abstract The postnatal interaction between microbiota and the immune system establishes lifelong homeostasis at mucosal epithelial barriers, however, the barrier-specific physiological activities that drive the equilibrium are hardly known. During weaning, the oral epithelium, which is monitored by...
| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-09-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-41409-0 |
| _version_ | 1797558470713540608 |
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| author | Yasmin Jaber Yasmine Netanely Reem Naamneh Or Saar Khaled Zubeidat Yasmin Saba Olga Georgiev Paz Kles Or Barel Yael Horev Omri Yosef Luba Eli-Berchoer Chen Nadler Gili Betser-Cohen Hagit Shapiro Eran Elinav Asaf Wilensky Avi-Hai Hovav |
| author_facet | Yasmin Jaber Yasmine Netanely Reem Naamneh Or Saar Khaled Zubeidat Yasmin Saba Olga Georgiev Paz Kles Or Barel Yael Horev Omri Yosef Luba Eli-Berchoer Chen Nadler Gili Betser-Cohen Hagit Shapiro Eran Elinav Asaf Wilensky Avi-Hai Hovav |
| author_sort | Yasmin Jaber |
| collection | DOAJ |
| description | Abstract The postnatal interaction between microbiota and the immune system establishes lifelong homeostasis at mucosal epithelial barriers, however, the barrier-specific physiological activities that drive the equilibrium are hardly known. During weaning, the oral epithelium, which is monitored by Langerhans cells (LC), is challenged by the development of a microbial plaque and the initiation of masticatory forces capable of damaging the epithelium. Here we show that microbial colonization following birth facilitates the differentiation of oral LCs, setting the stage for the weaning period, in which adaptive immunity develops. Despite the presence of the challenging microbial plaque, LCs mainly respond to masticatory mechanical forces, inducing adaptive immunity, to maintain epithelial integrity that is also associated with naturally occurring alveolar bone loss. Mechanistically, masticatory forces induce the migration of LCs to the lymph nodes, and in return, LCs support the development of immunity to maintain epithelial integrity in a microbiota-independent manner. Unlike in adult life, this bone loss is IL-17-independent, suggesting that the establishment of oral mucosal homeostasis after birth and its maintenance in adult life involve distinct mechanisms. |
| first_indexed | 2024-03-10T17:31:52Z |
| format | Article |
| id | doaj.art-ac25d743859648f581eb8c7e71667088 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:31:52Z |
| publishDate | 2023-09-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-ac25d743859648f581eb8c7e716670882023-11-20T10:00:37ZengNature PortfolioNature Communications2041-17232023-09-0114111510.1038/s41467-023-41409-0Langerhans cells shape postnatal oral homeostasis in a mechanical-force-dependent but microbiota and IL17-independent mannerYasmin Jaber0Yasmine Netanely1Reem Naamneh2Or Saar3Khaled Zubeidat4Yasmin Saba5Olga Georgiev6Paz Kles7Or Barel8Yael Horev9Omri Yosef10Luba Eli-Berchoer11Chen Nadler12Gili Betser-Cohen13Hagit Shapiro14Eran Elinav15Asaf Wilensky16Avi-Hai Hovav17Institute of Biomedical and Oral Research, Faculty of Dental Medicine, Hebrew UniversityInstitute of Biomedical and Oral Research, Faculty of Dental Medicine, Hebrew UniversityInstitute of Biomedical and Oral Research, Faculty of Dental Medicine, Hebrew UniversityFaculty of Dental Medicine, Hebrew University, Jerusalem, Israel; Department of Periodontology, Hadassah Medical CenterInstitute of Biomedical and Oral Research, Faculty of Dental Medicine, Hebrew UniversityInstitute of Biomedical and Oral Research, Faculty of Dental Medicine, Hebrew UniversityInstitute of Biomedical and Oral Research, Faculty of Dental Medicine, Hebrew UniversityFaculty of Dental Medicine, Hebrew University, Jerusalem, Israel; Department of Periodontology, Hadassah Medical CenterInstitute of Biomedical and Oral Research, Faculty of Dental Medicine, Hebrew UniversityFaculty of Dental Medicine, Hebrew University, Jerusalem, Israel; Department of Periodontology, Hadassah Medical CenterThe Lautenberg Center for Immunology and Cancer Research, Israel-Canada Medical Research Institute, Faculty of Medicine, Hebrew UniversityInstitute of Biomedical and Oral Research, Faculty of Dental Medicine, Hebrew UniversityFaculty of Dental Medicine, Hebrew UniversityDivision of Identification and Forensic Science, Police National HQSystem Immunology Department, Weizmann Institute of ScienceSystem Immunology Department, Weizmann Institute of ScienceFaculty of Dental Medicine, Hebrew University, Jerusalem, Israel; Department of Periodontology, Hadassah Medical CenterInstitute of Biomedical and Oral Research, Faculty of Dental Medicine, Hebrew UniversityAbstract The postnatal interaction between microbiota and the immune system establishes lifelong homeostasis at mucosal epithelial barriers, however, the barrier-specific physiological activities that drive the equilibrium are hardly known. During weaning, the oral epithelium, which is monitored by Langerhans cells (LC), is challenged by the development of a microbial plaque and the initiation of masticatory forces capable of damaging the epithelium. Here we show that microbial colonization following birth facilitates the differentiation of oral LCs, setting the stage for the weaning period, in which adaptive immunity develops. Despite the presence of the challenging microbial plaque, LCs mainly respond to masticatory mechanical forces, inducing adaptive immunity, to maintain epithelial integrity that is also associated with naturally occurring alveolar bone loss. Mechanistically, masticatory forces induce the migration of LCs to the lymph nodes, and in return, LCs support the development of immunity to maintain epithelial integrity in a microbiota-independent manner. Unlike in adult life, this bone loss is IL-17-independent, suggesting that the establishment of oral mucosal homeostasis after birth and its maintenance in adult life involve distinct mechanisms.https://doi.org/10.1038/s41467-023-41409-0 |
| spellingShingle | Yasmin Jaber Yasmine Netanely Reem Naamneh Or Saar Khaled Zubeidat Yasmin Saba Olga Georgiev Paz Kles Or Barel Yael Horev Omri Yosef Luba Eli-Berchoer Chen Nadler Gili Betser-Cohen Hagit Shapiro Eran Elinav Asaf Wilensky Avi-Hai Hovav Langerhans cells shape postnatal oral homeostasis in a mechanical-force-dependent but microbiota and IL17-independent manner Nature Communications |
| title | Langerhans cells shape postnatal oral homeostasis in a mechanical-force-dependent but microbiota and IL17-independent manner |
| title_full | Langerhans cells shape postnatal oral homeostasis in a mechanical-force-dependent but microbiota and IL17-independent manner |
| title_fullStr | Langerhans cells shape postnatal oral homeostasis in a mechanical-force-dependent but microbiota and IL17-independent manner |
| title_full_unstemmed | Langerhans cells shape postnatal oral homeostasis in a mechanical-force-dependent but microbiota and IL17-independent manner |
| title_short | Langerhans cells shape postnatal oral homeostasis in a mechanical-force-dependent but microbiota and IL17-independent manner |
| title_sort | langerhans cells shape postnatal oral homeostasis in a mechanical force dependent but microbiota and il17 independent manner |
| url | https://doi.org/10.1038/s41467-023-41409-0 |
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