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An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis

An ancient evolutionary innovation of a novel cell type, the stinging cell (cnidocyte), appeared >600 million years ago in the phylum Cnidaria (sea anemones, corals, hydroids, and jellyfish). A complex bursting nano-injector of venom, the cnidocyst, is embedded in cnidocytes and enables cnidarian...

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Autores principales: Fridrich, Arie, Salinas-Saaverda, Miguel, Kozlolvski, Itamar, Surm, Joachim M., Chrysostomou, Eleni, Tripathi, Abhinandan M., Frank, Uri, Moran, Yehu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10548089/
https://www.ncbi.nlm.nih.gov/pubmed/37676763
http://dx.doi.org/10.1016/j.celrep.2023.113072
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author Fridrich, Arie
Salinas-Saaverda, Miguel
Kozlolvski, Itamar
Surm, Joachim M.
Chrysostomou, Eleni
Tripathi, Abhinandan M.
Frank, Uri
Moran, Yehu
author_facet Fridrich, Arie
Salinas-Saaverda, Miguel
Kozlolvski, Itamar
Surm, Joachim M.
Chrysostomou, Eleni
Tripathi, Abhinandan M.
Frank, Uri
Moran, Yehu
author_sort Fridrich, Arie
collection PubMed
description An ancient evolutionary innovation of a novel cell type, the stinging cell (cnidocyte), appeared >600 million years ago in the phylum Cnidaria (sea anemones, corals, hydroids, and jellyfish). A complex bursting nano-injector of venom, the cnidocyst, is embedded in cnidocytes and enables cnidarians to paralyze their prey and predators, contributing to this phylum’s evolutionary success. In this work, we show that post-transcriptional regulation by a pan-cnidarian microRNA, miR-2022, is essential for biogenesis of these cells in the sea anemone Nematostella vectensis. By manipulation of miR-2022 levels in a transgenic reporter line of cnidocytes, followed by transcriptomics, single-cell data analysis, prey paralysis assays, and cell sorting of transgenic cnidocytes, we reveal that miR-2022 enables cnidocyte biogenesis in Nematostella, while exhibiting a conserved expression domain with its targets in cnidocytes of other cnidarian species. Thus, here we revealed a functional basis to the conservation of one of nature’s most ancient microRNAs.
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spelling pubmed-105480892023-10-05 An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis Fridrich, Arie Salinas-Saaverda, Miguel Kozlolvski, Itamar Surm, Joachim M. Chrysostomou, Eleni Tripathi, Abhinandan M. Frank, Uri Moran, Yehu Cell Rep Report An ancient evolutionary innovation of a novel cell type, the stinging cell (cnidocyte), appeared >600 million years ago in the phylum Cnidaria (sea anemones, corals, hydroids, and jellyfish). A complex bursting nano-injector of venom, the cnidocyst, is embedded in cnidocytes and enables cnidarians to paralyze their prey and predators, contributing to this phylum’s evolutionary success. In this work, we show that post-transcriptional regulation by a pan-cnidarian microRNA, miR-2022, is essential for biogenesis of these cells in the sea anemone Nematostella vectensis. By manipulation of miR-2022 levels in a transgenic reporter line of cnidocytes, followed by transcriptomics, single-cell data analysis, prey paralysis assays, and cell sorting of transgenic cnidocytes, we reveal that miR-2022 enables cnidocyte biogenesis in Nematostella, while exhibiting a conserved expression domain with its targets in cnidocytes of other cnidarian species. Thus, here we revealed a functional basis to the conservation of one of nature’s most ancient microRNAs. Cell Press 2023-09-06 /pmc/articles/PMC10548089/ /pubmed/37676763 http://dx.doi.org/10.1016/j.celrep.2023.113072 Text en © 2023 The Authors https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Report
Fridrich, Arie
Salinas-Saaverda, Miguel
Kozlolvski, Itamar
Surm, Joachim M.
Chrysostomou, Eleni
Tripathi, Abhinandan M.
Frank, Uri
Moran, Yehu
An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis
title An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis
title_full An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis
title_fullStr An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis
title_full_unstemmed An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis
title_short An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis
title_sort ancient pan-cnidarian microrna regulates stinging capsule biogenesis in nematostella vectensis
topic Report
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10548089/
https://www.ncbi.nlm.nih.gov/pubmed/37676763
http://dx.doi.org/10.1016/j.celrep.2023.113072
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