Type II taste cells participate in mucosal immune surveillance

• Published in: PLoS biology Vol. 21; no. 1; p. e3001647
• Main Authors: Qin, Yumei, Palayyan, Salin Raj, Zheng, Xin, Tian, Shiyi, Margolskee, Robert F, Sukumaran, Sunil K
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 12.01.2023; Public Library of Science (PLoS)
• Subjects: Animals; Antibodies; Antigens; Biology and Life Sciences; Cell differentiation; Cell proliferation; Cytokines; Cytokines - metabolism; Dendritic cells; Engineering and Technology; Gene expression; Growth factors; Immune system; Immunosurveillance; Inflammation; Intestines; Lipopolysaccharides; M cells; Medicine and Health Sciences; Mice; Mice, Inbred C57BL; Mice, Knockout; Microbiomes; Microbiota; Microorganisms; Microspheres; Mucosal immunity; Mucosal-associated lymphoid tissue; Mucous Membrane; Nanoparticles; NF-κB protein; Organoids; Papillae; Proteins; Receptors; Research and Analysis Methods; Short Reports; Signal transduction; Signaling; Social Sciences; Surveillance; Sweet taste; Taste; Taste Buds; Taste receptors; Taste stimuli; Tongue; TRANCE protein; Tumor necrosis factor-TNF; Umami
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3001647

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.