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Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity

Although specialized mechanosensory cells are found across animal phylogeny, early evolutionary histories of mechanoreceptor development remain enigmatic. Cnidaria (e.g. sea anemones and jellyfishes) is the sister group to well-studied Bilateria (e.g. flies and vertebrates), and has two mechanosenso...

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Autores principales: Ozment, Ethan, Tamvacakis, Arianna N, Zhou, Jianhong, Rosiles-Loeza, Pablo Yamild, Escobar-Hernandez, Esteban Elías, Fernandez-Valverde, Selene L, Nakanishi, Nagayasu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8846589/
https://www.ncbi.nlm.nih.gov/pubmed/34939935
http://dx.doi.org/10.7554/eLife.74336
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author Ozment, Ethan
Tamvacakis, Arianna N
Zhou, Jianhong
Rosiles-Loeza, Pablo Yamild
Escobar-Hernandez, Esteban Elías
Fernandez-Valverde, Selene L
Nakanishi, Nagayasu
author_facet Ozment, Ethan
Tamvacakis, Arianna N
Zhou, Jianhong
Rosiles-Loeza, Pablo Yamild
Escobar-Hernandez, Esteban Elías
Fernandez-Valverde, Selene L
Nakanishi, Nagayasu
author_sort Ozment, Ethan
collection PubMed
description Although specialized mechanosensory cells are found across animal phylogeny, early evolutionary histories of mechanoreceptor development remain enigmatic. Cnidaria (e.g. sea anemones and jellyfishes) is the sister group to well-studied Bilateria (e.g. flies and vertebrates), and has two mechanosensory cell types – a lineage-specific sensory effector known as the cnidocyte, and a classical mechanosensory neuron referred to as the hair cell. While developmental genetics of cnidocytes is increasingly understood, genes essential for cnidarian hair cell development are unknown. Here, we show that the class IV POU homeodomain transcription factor (POU-IV) – an indispensable regulator of mechanosensory cell differentiation in Bilateria and cnidocyte differentiation in Cnidaria – controls hair cell development in the sea anemone cnidarian Nematostella vectensis. N. vectensis POU-IV is postmitotically expressed in tentacular hair cells, and is necessary for development of the apical mechanosensory apparatus, but not of neurites, in hair cells. Moreover, it binds to deeply conserved DNA recognition elements, and turns on a unique set of effector genes – including the transmembrane receptor-encoding gene polycystin 1 – specifically in hair cells. Our results suggest that POU-IV directs differentiation of cnidarian hair cells and cnidocytes via distinct gene regulatory mechanisms, and support an evolutionarily ancient role for POU-IV in defining the mature state of mechanosensory neurons.
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spelling pubmed-88465892022-02-16 Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity Ozment, Ethan Tamvacakis, Arianna N Zhou, Jianhong Rosiles-Loeza, Pablo Yamild Escobar-Hernandez, Esteban Elías Fernandez-Valverde, Selene L Nakanishi, Nagayasu eLife Developmental Biology Although specialized mechanosensory cells are found across animal phylogeny, early evolutionary histories of mechanoreceptor development remain enigmatic. Cnidaria (e.g. sea anemones and jellyfishes) is the sister group to well-studied Bilateria (e.g. flies and vertebrates), and has two mechanosensory cell types – a lineage-specific sensory effector known as the cnidocyte, and a classical mechanosensory neuron referred to as the hair cell. While developmental genetics of cnidocytes is increasingly understood, genes essential for cnidarian hair cell development are unknown. Here, we show that the class IV POU homeodomain transcription factor (POU-IV) – an indispensable regulator of mechanosensory cell differentiation in Bilateria and cnidocyte differentiation in Cnidaria – controls hair cell development in the sea anemone cnidarian Nematostella vectensis. N. vectensis POU-IV is postmitotically expressed in tentacular hair cells, and is necessary for development of the apical mechanosensory apparatus, but not of neurites, in hair cells. Moreover, it binds to deeply conserved DNA recognition elements, and turns on a unique set of effector genes – including the transmembrane receptor-encoding gene polycystin 1 – specifically in hair cells. Our results suggest that POU-IV directs differentiation of cnidarian hair cells and cnidocytes via distinct gene regulatory mechanisms, and support an evolutionarily ancient role for POU-IV in defining the mature state of mechanosensory neurons. eLife Sciences Publications, Ltd 2021-12-23 /pmc/articles/PMC8846589/ /pubmed/34939935 http://dx.doi.org/10.7554/eLife.74336 Text en © 2021, Ozment et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Ozment, Ethan
Tamvacakis, Arianna N
Zhou, Jianhong
Rosiles-Loeza, Pablo Yamild
Escobar-Hernandez, Esteban Elías
Fernandez-Valverde, Selene L
Nakanishi, Nagayasu
Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity
title Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity
title_full Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity
title_fullStr Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity
title_full_unstemmed Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity
title_short Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity
title_sort cnidarian hair cell development illuminates an ancient role for the class iv pou transcription factor in defining mechanoreceptor identity
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8846589/
https://www.ncbi.nlm.nih.gov/pubmed/34939935
http://dx.doi.org/10.7554/eLife.74336
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