Species-specific formation of paraspeckles in intestinal epithelium revealed by characterization of NEAT1 in naked mole-rat

Paraspeckles are mammalian-specific nuclear bodies built on the long noncoding RNA NEAT1_2. The molecular mechanisms of paraspeckle formation have been mainly studied using human or mouse cells, and it is not known if the same molecular components are involved in the formation of paraspeckles in oth...

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Autores principales: Yamada, Akihiro, Toya, Hikaru, Tanahashi, Mayuko, Kurihara, Misuzu, Mito, Mari, Iwasaki, Shintaro, Kurosaka, Satoshi, Takumi, Toru, Fox, Archa, Kawamura, Yoshimi, Miura, Kyoko, Nakagawa, Shinichi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9297846/
https://www.ncbi.nlm.nih.gov/pubmed/35654483
http://dx.doi.org/10.1261/rna.079135.122
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author Yamada, Akihiro
Toya, Hikaru
Tanahashi, Mayuko
Kurihara, Misuzu
Mito, Mari
Iwasaki, Shintaro
Kurosaka, Satoshi
Takumi, Toru
Fox, Archa
Kawamura, Yoshimi
Miura, Kyoko
Nakagawa, Shinichi
author_facet Yamada, Akihiro
Toya, Hikaru
Tanahashi, Mayuko
Kurihara, Misuzu
Mito, Mari
Iwasaki, Shintaro
Kurosaka, Satoshi
Takumi, Toru
Fox, Archa
Kawamura, Yoshimi
Miura, Kyoko
Nakagawa, Shinichi
author_sort Yamada, Akihiro
collection PubMed
description Paraspeckles are mammalian-specific nuclear bodies built on the long noncoding RNA NEAT1_2. The molecular mechanisms of paraspeckle formation have been mainly studied using human or mouse cells, and it is not known if the same molecular components are involved in the formation of paraspeckles in other mammalian species. We thus investigated the expression pattern of NEAT1_2 in naked mole-rats (nNEAT1_2), which exhibit extreme longevity and lower susceptibility to cancer. In the intestine, nNEAT1_2 is widely expressed along the entire intestinal epithelium, which is different from the expression of mNeat1_2 that is restricted to the cells of the distal tip in mice. Notably, the expression of FUS, a FET family RNA binding protein, essential for the formation of paraspeckles both in humans and mice, was absent in the distal part of the intestinal epithelium in naked mole-rats. Instead, mRNAs of other FET family proteins EWSR1 and TAF15 were expressed in the distal region. Exogenous expression of these proteins in Fus-deficient murine embryonic fibroblast cells rescued the formation of paraspeckles. These observations suggest that nNEAT1_2 recruits a different set of RNA binding proteins in a cell type-specific manner during the formation of paraspeckles in different organisms.
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spelling pubmed-92978462023-08-01 Species-specific formation of paraspeckles in intestinal epithelium revealed by characterization of NEAT1 in naked mole-rat Yamada, Akihiro Toya, Hikaru Tanahashi, Mayuko Kurihara, Misuzu Mito, Mari Iwasaki, Shintaro Kurosaka, Satoshi Takumi, Toru Fox, Archa Kawamura, Yoshimi Miura, Kyoko Nakagawa, Shinichi RNA Article Paraspeckles are mammalian-specific nuclear bodies built on the long noncoding RNA NEAT1_2. The molecular mechanisms of paraspeckle formation have been mainly studied using human or mouse cells, and it is not known if the same molecular components are involved in the formation of paraspeckles in other mammalian species. We thus investigated the expression pattern of NEAT1_2 in naked mole-rats (nNEAT1_2), which exhibit extreme longevity and lower susceptibility to cancer. In the intestine, nNEAT1_2 is widely expressed along the entire intestinal epithelium, which is different from the expression of mNeat1_2 that is restricted to the cells of the distal tip in mice. Notably, the expression of FUS, a FET family RNA binding protein, essential for the formation of paraspeckles both in humans and mice, was absent in the distal part of the intestinal epithelium in naked mole-rats. Instead, mRNAs of other FET family proteins EWSR1 and TAF15 were expressed in the distal region. Exogenous expression of these proteins in Fus-deficient murine embryonic fibroblast cells rescued the formation of paraspeckles. These observations suggest that nNEAT1_2 recruits a different set of RNA binding proteins in a cell type-specific manner during the formation of paraspeckles in different organisms. Cold Spring Harbor Laboratory Press 2022-08 /pmc/articles/PMC9297846/ /pubmed/35654483 http://dx.doi.org/10.1261/rna.079135.122 Text en © 2022 Yamada et al.; Published by Cold Spring Harbor Laboratory Press for the RNA Society https://creativecommons.org/licenses/by-nc/4.0/This article is distributed exclusively by the RNA Society for the first 12 months after the full-issue publication date (see http://rnajournal.cshlp.org/site/misc/terms.xhtml). After 12 months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) .
spellingShingle Article
Yamada, Akihiro
Toya, Hikaru
Tanahashi, Mayuko
Kurihara, Misuzu
Mito, Mari
Iwasaki, Shintaro
Kurosaka, Satoshi
Takumi, Toru
Fox, Archa
Kawamura, Yoshimi
Miura, Kyoko
Nakagawa, Shinichi
Species-specific formation of paraspeckles in intestinal epithelium revealed by characterization of NEAT1 in naked mole-rat
title Species-specific formation of paraspeckles in intestinal epithelium revealed by characterization of NEAT1 in naked mole-rat
title_full Species-specific formation of paraspeckles in intestinal epithelium revealed by characterization of NEAT1 in naked mole-rat
title_fullStr Species-specific formation of paraspeckles in intestinal epithelium revealed by characterization of NEAT1 in naked mole-rat
title_full_unstemmed Species-specific formation of paraspeckles in intestinal epithelium revealed by characterization of NEAT1 in naked mole-rat
title_short Species-specific formation of paraspeckles in intestinal epithelium revealed by characterization of NEAT1 in naked mole-rat
title_sort species-specific formation of paraspeckles in intestinal epithelium revealed by characterization of neat1 in naked mole-rat
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9297846/
https://www.ncbi.nlm.nih.gov/pubmed/35654483
http://dx.doi.org/10.1261/rna.079135.122
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