Tongue immune compartment analysis reveals spatial macrophage heterogeneity
The tongue is a unique muscular organ situated in the oral cavity where it is involved in taste sensation, mastication, and articulation. As a barrier organ, which is constantly exposed to environmental pathogens, the tongue is expected to host an immune cell network ensuring local immune defence. H...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-06-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/77490 |
| _version_ | 1811252713985409024 |
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| author | Ekaterini Maria Lyras Karin Zimmermann Lisa Katharina Wagner Dorothea Dörr Christoph SN Klose Cornelius Fischer Steffen Jung Simon Yona Avi-Hai Hovav Werner Stenzel Steffen Dommerich Thomas Conrad Achim Leutz Alexander Mildner |
| author_facet | Ekaterini Maria Lyras Karin Zimmermann Lisa Katharina Wagner Dorothea Dörr Christoph SN Klose Cornelius Fischer Steffen Jung Simon Yona Avi-Hai Hovav Werner Stenzel Steffen Dommerich Thomas Conrad Achim Leutz Alexander Mildner |
| author_sort | Ekaterini Maria Lyras |
| collection | DOAJ |
| description | The tongue is a unique muscular organ situated in the oral cavity where it is involved in taste sensation, mastication, and articulation. As a barrier organ, which is constantly exposed to environmental pathogens, the tongue is expected to host an immune cell network ensuring local immune defence. However, the composition and the transcriptional landscape of the tongue immune system are currently not completely defined. Here, we characterised the tissue-resident immune compartment of the murine tongue during development, health and disease, combining single-cell RNA-sequencing with in situ immunophenotyping. We identified distinct local immune cell populations and described two specific subsets of tongue-resident macrophages occupying discrete anatomical niches. Cx3cr1+ macrophages were located specifically in the highly innervated lamina propria beneath the tongue epidermis and at times in close proximity to fungiform papillae. Folr2+ macrophages were detected in deeper muscular tissue. In silico analysis indicated that the two macrophage subsets originate from a common proliferative precursor during early postnatal development and responded differently to systemic LPS in vivo. Our description of the under-investigated tongue immune system sets a starting point to facilitate research on tongue immune-physiology and pathology including cancer and taste disorders. |
| first_indexed | 2024-04-12T16:38:52Z |
| format | Article |
| id | doaj.art-bdec5d45da9b4982bda0ef6698f9511b |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:38:52Z |
| publishDate | 2022-06-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-bdec5d45da9b4982bda0ef6698f9511b2022-12-22T03:24:53ZengeLife Sciences Publications LtdeLife2050-084X2022-06-011110.7554/eLife.77490Tongue immune compartment analysis reveals spatial macrophage heterogeneityEkaterini Maria Lyras0https://orcid.org/0000-0003-3269-0854Karin Zimmermann1Lisa Katharina Wagner2Dorothea Dörr3Christoph SN Klose4Cornelius Fischer5Steffen Jung6https://orcid.org/0000-0003-4290-5716Simon Yona7https://orcid.org/0000-0002-3984-2008Avi-Hai Hovav8Werner Stenzel9Steffen Dommerich10Thomas Conrad11Achim Leutz12Alexander Mildner13https://orcid.org/0000-0002-2019-8427Max-Delbrück-Center for Molecular Medicine Berlin, Berlin, GermanyMax-Delbrück-Center for Molecular Medicine Berlin, Berlin, GermanyMax-Delbrück-Center for Molecular Medicine Berlin, Berlin, GermanyMax-Delbrück-Center for Molecular Medicine Berlin, Berlin, Germany; Institute of Biology, Humboldt University of Berlin, Berlin, GermanyUniversitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Microbiology, Infectious Diseases and Immunology, Charité Berlin, Berlin, GermanyMax-Delbrück-Center for Molecular Medicine Berlin, Berlin, GermanyWeizmann Institute of Science, Rehovot, IsraelInstitute of Dental Sciences, The Hebrew University of Jerusalem, Jerusalem, IsraelInstitute of Dental Sciences, The Hebrew University of Jerusalem, Jerusalem, IsraelUniversitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Neuropathology, Charité Berlin, Berlin, GermanyUniversitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Department of Otorhinolaryngology, Charité Berlin, Berlin, GermanyMax-Delbrück-Center for Molecular Medicine Berlin, Berlin, GermanyMax-Delbrück-Center for Molecular Medicine Berlin, Berlin, Germany; Institute of Biology, Humboldt University of Berlin, Berlin, GermanyMax-Delbrück-Center for Molecular Medicine Berlin, Berlin, Germany; InFLAMES Research Flagship Center, University of Turku, Turku, Finland; Institute of Biomedicine, Medicity, University of Turku, Turku, FinlandThe tongue is a unique muscular organ situated in the oral cavity where it is involved in taste sensation, mastication, and articulation. As a barrier organ, which is constantly exposed to environmental pathogens, the tongue is expected to host an immune cell network ensuring local immune defence. However, the composition and the transcriptional landscape of the tongue immune system are currently not completely defined. Here, we characterised the tissue-resident immune compartment of the murine tongue during development, health and disease, combining single-cell RNA-sequencing with in situ immunophenotyping. We identified distinct local immune cell populations and described two specific subsets of tongue-resident macrophages occupying discrete anatomical niches. Cx3cr1+ macrophages were located specifically in the highly innervated lamina propria beneath the tongue epidermis and at times in close proximity to fungiform papillae. Folr2+ macrophages were detected in deeper muscular tissue. In silico analysis indicated that the two macrophage subsets originate from a common proliferative precursor during early postnatal development and responded differently to systemic LPS in vivo. Our description of the under-investigated tongue immune system sets a starting point to facilitate research on tongue immune-physiology and pathology including cancer and taste disorders.https://elifesciences.org/articles/77490Tonguemacrophagessingle cell sequencingcell development |
| spellingShingle | Ekaterini Maria Lyras Karin Zimmermann Lisa Katharina Wagner Dorothea Dörr Christoph SN Klose Cornelius Fischer Steffen Jung Simon Yona Avi-Hai Hovav Werner Stenzel Steffen Dommerich Thomas Conrad Achim Leutz Alexander Mildner Tongue immune compartment analysis reveals spatial macrophage heterogeneity eLife Tongue macrophages single cell sequencing cell development |
| title | Tongue immune compartment analysis reveals spatial macrophage heterogeneity |
| title_full | Tongue immune compartment analysis reveals spatial macrophage heterogeneity |
| title_fullStr | Tongue immune compartment analysis reveals spatial macrophage heterogeneity |
| title_full_unstemmed | Tongue immune compartment analysis reveals spatial macrophage heterogeneity |
| title_short | Tongue immune compartment analysis reveals spatial macrophage heterogeneity |
| title_sort | tongue immune compartment analysis reveals spatial macrophage heterogeneity |
| topic | Tongue macrophages single cell sequencing cell development |
| url | https://elifesciences.org/articles/77490 |
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