Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes

The selective elimination system blocks the accumulation of meiosis-specific mRNAs during the mitotic cell cycle in fission yeast. These mRNAs harbour a region, the determinant of selective removal (DSR), which is recognized by a YTH-family RNA-binding protein, Mmi1. Mmi1 directs target transcripts...

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Main Authors: Akira Yamashita, Yuichi Shichino, Hirotsugu Tanaka, Edwige Hiriart, Leila Touat-Todeschini, Aurélia Vavasseur, Da-Qiao Ding, Yasushi Hiraoka, André Verdel, Masayuki Yamamoto
Format: Article
Language:English
Published: The Royal Society 2012-01-01
Series:Open Biology
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Online Access:https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.120014
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author Akira Yamashita
Yuichi Shichino
Hirotsugu Tanaka
Edwige Hiriart
Leila Touat-Todeschini
Aurélia Vavasseur
Da-Qiao Ding
Yasushi Hiraoka
André Verdel
Masayuki Yamamoto
author_facet Akira Yamashita
Yuichi Shichino
Hirotsugu Tanaka
Edwige Hiriart
Leila Touat-Todeschini
Aurélia Vavasseur
Da-Qiao Ding
Yasushi Hiraoka
André Verdel
Masayuki Yamamoto
author_sort Akira Yamashita
collection DOAJ
description The selective elimination system blocks the accumulation of meiosis-specific mRNAs during the mitotic cell cycle in fission yeast. These mRNAs harbour a region, the determinant of selective removal (DSR), which is recognized by a YTH-family RNA-binding protein, Mmi1. Mmi1 directs target transcripts to destruction in association with nuclear exosomes. Hence, the interaction between DSR and Mmi1 is crucial to discriminate mitosis from meiosis. Here, we show that Mmi1 interacts with repeats of the hexanucleotide U(U/C)AAAC that are enriched in the DSR. Disruption of this ‘DSR core motif’ in a target mRNA inhibits its elimination. Tandem repeats of the motif can function as an artificial DSR. Mmi1 binds to it in vitro. Thus, a core motif cluster is responsible for the DSR activity. Furthermore, certain variant hexanucleotide motifs can augment the function of the DSR core motif. Notably, meiRNA, which composes the nuclear Mei2 dot required to suppress Mmi1 activity during meiosis, carries numerous copies of the core/augmenting motifs on its tail and is indeed degraded by the Mmi1/exosome system, indicating its likely role as decoy bait for Mmi1.
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spelling doaj.art-c35987d7a00b4565b59cff0585e69d642022-12-21T23:47:46ZengThe Royal SocietyOpen Biology2046-24412012-01-012310.1098/rsob.120014120014Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genesAkira YamashitaYuichi ShichinoHirotsugu TanakaEdwige HiriartLeila Touat-TodeschiniAurélia VavasseurDa-Qiao DingYasushi HiraokaAndré VerdelMasayuki YamamotoThe selective elimination system blocks the accumulation of meiosis-specific mRNAs during the mitotic cell cycle in fission yeast. These mRNAs harbour a region, the determinant of selective removal (DSR), which is recognized by a YTH-family RNA-binding protein, Mmi1. Mmi1 directs target transcripts to destruction in association with nuclear exosomes. Hence, the interaction between DSR and Mmi1 is crucial to discriminate mitosis from meiosis. Here, we show that Mmi1 interacts with repeats of the hexanucleotide U(U/C)AAAC that are enriched in the DSR. Disruption of this ‘DSR core motif’ in a target mRNA inhibits its elimination. Tandem repeats of the motif can function as an artificial DSR. Mmi1 binds to it in vitro. Thus, a core motif cluster is responsible for the DSR activity. Furthermore, certain variant hexanucleotide motifs can augment the function of the DSR core motif. Notably, meiRNA, which composes the nuclear Mei2 dot required to suppress Mmi1 activity during meiosis, carries numerous copies of the core/augmenting motifs on its tail and is indeed degraded by the Mmi1/exosome system, indicating its likely role as decoy bait for Mmi1.https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.120014mrna degradationrna-binding proteinexosomemeiosismmi1
spellingShingle Akira Yamashita
Yuichi Shichino
Hirotsugu Tanaka
Edwige Hiriart
Leila Touat-Todeschini
Aurélia Vavasseur
Da-Qiao Ding
Yasushi Hiraoka
André Verdel
Masayuki Yamamoto
Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes
Open Biology
mrna degradation
rna-binding protein
exosome
meiosis
mmi1
title Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes
title_full Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes
title_fullStr Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes
title_full_unstemmed Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes
title_short Hexanucleotide motifs mediate recruitment of the RNA elimination machinery to silent meiotic genes
title_sort hexanucleotide motifs mediate recruitment of the rna elimination machinery to silent meiotic genes
topic mrna degradation
rna-binding protein
exosome
meiosis
mmi1
url https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.120014
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