Type II taste cells participate in mucosal immune surveillance.
The oral microbiome is second only to its intestinal counterpart in diversity and abundance, but its effects on taste cells remains largely unexplored. Using single-cell RNASeq, we found that mouse taste cells, in particular, sweet and umami receptor cells that express taste 1 receptor member 3 (Tas...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2023-01-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3001647 |
| _version_ | 1797852109294534656 |
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| author | Yumei Qin Salin Raj Palayyan Xin Zheng Shiyi Tian Robert F Margolskee Sunil K Sukumaran |
| author_facet | Yumei Qin Salin Raj Palayyan Xin Zheng Shiyi Tian Robert F Margolskee Sunil K Sukumaran |
| author_sort | Yumei Qin |
| collection | DOAJ |
| description | The oral microbiome is second only to its intestinal counterpart in diversity and abundance, but its effects on taste cells remains largely unexplored. Using single-cell RNASeq, we found that mouse taste cells, in particular, sweet and umami receptor cells that express taste 1 receptor member 3 (Tas1r3), have a gene expression signature reminiscent of Microfold (M) cells, a central player in immune surveillance in the mucosa-associated lymphoid tissue (MALT) such as those in the Peyer's patch and tonsils. Administration of tumor necrosis factor ligand superfamily member 11 (TNFSF11; also known as RANKL), a growth factor required for differentiation of M cells, dramatically increased M cell proliferation and marker gene expression in the taste papillae and in cultured taste organoids from wild-type (WT) mice. Taste papillae and organoids from knockout mice lacking Spib (SpibKO), a RANKL-regulated transcription factor required for M cell development and regeneration on the other hand, failed to respond to RANKL. Taste papillae from SpibKO mice also showed reduced expression of NF-κB signaling pathway components and proinflammatory cytokines and attracted fewer immune cells. However, lipopolysaccharide-induced expression of cytokines was strongly up-regulated in SpibKO mice compared to their WT counterparts. Like M cells, taste cells from WT but not SpibKO mice readily took up fluorescently labeled microbeads, a proxy for microbial transcytosis. The proportion of taste cell subtypes are unaltered in SpibKO mice; however, they displayed increased attraction to sweet and umami taste stimuli. We propose that taste cells are involved in immune surveillance and may tune their taste responses to microbial signaling and infection. |
| first_indexed | 2024-04-09T19:28:48Z |
| format | Article |
| id | doaj.art-56b24ee2f40c4e9d96385328b603d379 |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-04-09T19:28:48Z |
| publishDate | 2023-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-56b24ee2f40c4e9d96385328b603d3792023-04-05T05:30:22ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852023-01-01211e300164710.1371/journal.pbio.3001647Type II taste cells participate in mucosal immune surveillance.Yumei QinSalin Raj PalayyanXin ZhengShiyi TianRobert F MargolskeeSunil K SukumaranThe oral microbiome is second only to its intestinal counterpart in diversity and abundance, but its effects on taste cells remains largely unexplored. Using single-cell RNASeq, we found that mouse taste cells, in particular, sweet and umami receptor cells that express taste 1 receptor member 3 (Tas1r3), have a gene expression signature reminiscent of Microfold (M) cells, a central player in immune surveillance in the mucosa-associated lymphoid tissue (MALT) such as those in the Peyer's patch and tonsils. Administration of tumor necrosis factor ligand superfamily member 11 (TNFSF11; also known as RANKL), a growth factor required for differentiation of M cells, dramatically increased M cell proliferation and marker gene expression in the taste papillae and in cultured taste organoids from wild-type (WT) mice. Taste papillae and organoids from knockout mice lacking Spib (SpibKO), a RANKL-regulated transcription factor required for M cell development and regeneration on the other hand, failed to respond to RANKL. Taste papillae from SpibKO mice also showed reduced expression of NF-κB signaling pathway components and proinflammatory cytokines and attracted fewer immune cells. However, lipopolysaccharide-induced expression of cytokines was strongly up-regulated in SpibKO mice compared to their WT counterparts. Like M cells, taste cells from WT but not SpibKO mice readily took up fluorescently labeled microbeads, a proxy for microbial transcytosis. The proportion of taste cell subtypes are unaltered in SpibKO mice; however, they displayed increased attraction to sweet and umami taste stimuli. We propose that taste cells are involved in immune surveillance and may tune their taste responses to microbial signaling and infection.https://doi.org/10.1371/journal.pbio.3001647 |
| spellingShingle | Yumei Qin Salin Raj Palayyan Xin Zheng Shiyi Tian Robert F Margolskee Sunil K Sukumaran Type II taste cells participate in mucosal immune surveillance. PLoS Biology |
| title | Type II taste cells participate in mucosal immune surveillance. |
| title_full | Type II taste cells participate in mucosal immune surveillance. |
| title_fullStr | Type II taste cells participate in mucosal immune surveillance. |
| title_full_unstemmed | Type II taste cells participate in mucosal immune surveillance. |
| title_short | Type II taste cells participate in mucosal immune surveillance. |
| title_sort | type ii taste cells participate in mucosal immune surveillance |
| url | https://doi.org/10.1371/journal.pbio.3001647 |
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