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SOX2 regulates homeostasis of taste bud cells and lingual epithelial cells in posterior tongue

Taste bud cells arise from local epithelial stem cells in the oral cavity and are continuously replaced by newborn cells throughout an animal’s life. However, little is known about the molecular and cellular mechanisms of taste cell turnover. Recently, it has been demonstrated that SOX2, a transcrip...

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Autores principales: Ohmoto, Makoto, Lei, Weiwei, Yamashita, Junpei, Hirota, Junji, Jiang, Peihua, Matsumoto, Ichiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7561181/
https://www.ncbi.nlm.nih.gov/pubmed/33057384
http://dx.doi.org/10.1371/journal.pone.0240848
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author Ohmoto, Makoto
Lei, Weiwei
Yamashita, Junpei
Hirota, Junji
Jiang, Peihua
Matsumoto, Ichiro
author_facet Ohmoto, Makoto
Lei, Weiwei
Yamashita, Junpei
Hirota, Junji
Jiang, Peihua
Matsumoto, Ichiro
author_sort Ohmoto, Makoto
collection PubMed
description Taste bud cells arise from local epithelial stem cells in the oral cavity and are continuously replaced by newborn cells throughout an animal’s life. However, little is known about the molecular and cellular mechanisms of taste cell turnover. Recently, it has been demonstrated that SOX2, a transcription factor expressed in epithelial stem/progenitor cells of the oral cavity, regulates turnover of anterior tongue epithelium including gustatory and non-gustatory papillae. Yet, the role of SOX2 in regulating taste cell turnover in the posterior tongue is unclear. Prompted by the fact that there are regional differences in the cellular and molecular composition of taste buds and stem/progenitor cells in the anterior and posterior portions of tongue, which are derived from distinct embryonic origins, we set out to determine the role of SOX2 in epithelial tissue homeostasis in the posterior tongue. Here we report the differential requirement of SOX2 in the stem/progenitor cells for the normal turnover of lingual epithelial cells in the posterior tongue. Sox2 deletion in the stem/progenitor cells neither induced active caspase 3-mediated apoptotic cell death nor altered stem/progenitor cell population in the posterior tongue. Nevertheless, morphology and molecular feature of non-gustatory epithelial cells were impaired in the circumvallate papilla but not in the filiform papillae. Remarkably, taste buds became thinner, collapsed, and undetectable over time. Lineage tracing of Sox2-deleted stem/progenitor cells demonstrated an almost complete lack of newly generated basal precursor cells in the taste buds, suggesting mechanistically that Sox2 is involved in determining stem/progenitor cells to differentiate to gustatory lineage cells. Together, these results demonstrate that SOX2 plays key roles in regulating epithelial tissue homeostasis in the posterior tongue, similar but not identical to its function in the anterior tongue.
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spelling pubmed-75611812020-10-21 SOX2 regulates homeostasis of taste bud cells and lingual epithelial cells in posterior tongue Ohmoto, Makoto Lei, Weiwei Yamashita, Junpei Hirota, Junji Jiang, Peihua Matsumoto, Ichiro PLoS One Research Article Taste bud cells arise from local epithelial stem cells in the oral cavity and are continuously replaced by newborn cells throughout an animal’s life. However, little is known about the molecular and cellular mechanisms of taste cell turnover. Recently, it has been demonstrated that SOX2, a transcription factor expressed in epithelial stem/progenitor cells of the oral cavity, regulates turnover of anterior tongue epithelium including gustatory and non-gustatory papillae. Yet, the role of SOX2 in regulating taste cell turnover in the posterior tongue is unclear. Prompted by the fact that there are regional differences in the cellular and molecular composition of taste buds and stem/progenitor cells in the anterior and posterior portions of tongue, which are derived from distinct embryonic origins, we set out to determine the role of SOX2 in epithelial tissue homeostasis in the posterior tongue. Here we report the differential requirement of SOX2 in the stem/progenitor cells for the normal turnover of lingual epithelial cells in the posterior tongue. Sox2 deletion in the stem/progenitor cells neither induced active caspase 3-mediated apoptotic cell death nor altered stem/progenitor cell population in the posterior tongue. Nevertheless, morphology and molecular feature of non-gustatory epithelial cells were impaired in the circumvallate papilla but not in the filiform papillae. Remarkably, taste buds became thinner, collapsed, and undetectable over time. Lineage tracing of Sox2-deleted stem/progenitor cells demonstrated an almost complete lack of newly generated basal precursor cells in the taste buds, suggesting mechanistically that Sox2 is involved in determining stem/progenitor cells to differentiate to gustatory lineage cells. Together, these results demonstrate that SOX2 plays key roles in regulating epithelial tissue homeostasis in the posterior tongue, similar but not identical to its function in the anterior tongue. Public Library of Science 2020-10-15 /pmc/articles/PMC7561181/ /pubmed/33057384 http://dx.doi.org/10.1371/journal.pone.0240848 Text en © 2020 Ohmoto et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Ohmoto, Makoto
Lei, Weiwei
Yamashita, Junpei
Hirota, Junji
Jiang, Peihua
Matsumoto, Ichiro
SOX2 regulates homeostasis of taste bud cells and lingual epithelial cells in posterior tongue
title SOX2 regulates homeostasis of taste bud cells and lingual epithelial cells in posterior tongue
title_full SOX2 regulates homeostasis of taste bud cells and lingual epithelial cells in posterior tongue
title_fullStr SOX2 regulates homeostasis of taste bud cells and lingual epithelial cells in posterior tongue
title_full_unstemmed SOX2 regulates homeostasis of taste bud cells and lingual epithelial cells in posterior tongue
title_short SOX2 regulates homeostasis of taste bud cells and lingual epithelial cells in posterior tongue
title_sort sox2 regulates homeostasis of taste bud cells and lingual epithelial cells in posterior tongue
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7561181/
https://www.ncbi.nlm.nih.gov/pubmed/33057384
http://dx.doi.org/10.1371/journal.pone.0240848
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