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The selective elimination of messenger RNA underlies the mitosis-meiosis switch in fission yeast.

Yamamoto M - Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci. (2010)

Bottom Line: Meiosis-inducing signals in this microbe emanating from environmental conditions including the nutrient status converge on the activity of an RRM-type RNA-binding protein, Mei2.Fission yeast contains an RNA degradation system that selectively eliminates meiosis-specific mRNAs during the mitotic cell cycle.Mmi1, a novel RNA-binding protein of the YTH-family, is essential for this process.

View Article: PubMed Central - PubMed

Affiliation: Department of Biophysics and Biochemistry, Graduate School of Science, University of Tokyo, Tokyo, Japan. yamamoto@biochem.s.u-tokyo.ac.jp

ABSTRACT
The cellular programs for meiosis and mitosis must be strictly distinguished but the mechanisms controlling the entry to meiosis remain largely elusive in higher organisms. In contrast, recent analyses in yeast have shed new light on the mechanisms underlying the mitosis-meiosis switch. In this review, the current understanding of these mechanisms in the fission yeast Schizosaccharomyces pombe is discussed. Meiosis-inducing signals in this microbe emanating from environmental conditions including the nutrient status converge on the activity of an RRM-type RNA-binding protein, Mei2. This protein plays pivotal roles in both the induction and progression of meiosis and has now been found to govern the meiotic program in a quite unexpected manner. Fission yeast contains an RNA degradation system that selectively eliminates meiosis-specific mRNAs during the mitotic cell cycle. Mmi1, a novel RNA-binding protein of the YTH-family, is essential for this process. Mei2 tethers Mmi1 and thereby stabilizes the transcripts necessary for the progression of meiosis.

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Function of the Mei2 dot as the mitosis–meiosis switch. Left panel: a number of meiosis-specific transcripts in fission yeast harbor a region designated the DSR. The DSR renders the selective elimination of these mRNAs if they are expressed during the mitotic cell cycle. Mmi1, a YTH-family RNA-binding protein localized in the nucleus, binds to the DSR and promotes the elimination of the corresponding transcript in cooperation with the RNA-degradation machinery exosome. Right panel: to promote meiosis, Mei2, which has an affinity for Mmi1, forms a dot structure in the nucleus together with meiRNA. Mmi1 is thereby sequestered to this structure so that meiosis-specific transcripts are shielded from Mmi1-dependent mRNA elimination and can function stably. Reproduced from Ref. 67 with some modifications.
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fig05: Function of the Mei2 dot as the mitosis–meiosis switch. Left panel: a number of meiosis-specific transcripts in fission yeast harbor a region designated the DSR. The DSR renders the selective elimination of these mRNAs if they are expressed during the mitotic cell cycle. Mmi1, a YTH-family RNA-binding protein localized in the nucleus, binds to the DSR and promotes the elimination of the corresponding transcript in cooperation with the RNA-degradation machinery exosome. Right panel: to promote meiosis, Mei2, which has an affinity for Mmi1, forms a dot structure in the nucleus together with meiRNA. Mmi1 is thereby sequestered to this structure so that meiosis-specific transcripts are shielded from Mmi1-dependent mRNA elimination and can function stably. Reproduced from Ref. 67 with some modifications.

Mentions: Unexpectedly, a direct link between the DSR–Mmi1 system and Mei2 was identified in our laboratory. Localization analysis of Mmi1 revealed that this protein is present in multiple nuclear foci during vegetative growth. Interestingly, these foci converge to a single dot in meiotic prophase, which we found to overlap with the Mei2 dot. The conversion of Mmi1 to a single dot did not occur however in the absence of Mei2 or meiRNA.67) These observations led us to speculate that the Mei2 dot may sequester Mmi1 and thus inhibit its function and ensure the stable expression of meiosis-specific transcripts (Fig. 5). Consistent with this idea, we observed that Mei2 and Mmi1 can physically interact. Furthermore, we found that the cell growth arrest prior to meiosis I caused by the loss of the Mei2 dot in fission yeast could be suppressed by an artificial reduction of Mmi1 activity.67) Hence, the key molecular function of the Mei2 dot in fission yeast is most likely to be the shutdown of the DSR–Mmi1 system during meiotic prophase.


The selective elimination of messenger RNA underlies the mitosis-meiosis switch in fission yeast.

Yamamoto M - Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci. (2010)

Function of the Mei2 dot as the mitosis–meiosis switch. Left panel: a number of meiosis-specific transcripts in fission yeast harbor a region designated the DSR. The DSR renders the selective elimination of these mRNAs if they are expressed during the mitotic cell cycle. Mmi1, a YTH-family RNA-binding protein localized in the nucleus, binds to the DSR and promotes the elimination of the corresponding transcript in cooperation with the RNA-degradation machinery exosome. Right panel: to promote meiosis, Mei2, which has an affinity for Mmi1, forms a dot structure in the nucleus together with meiRNA. Mmi1 is thereby sequestered to this structure so that meiosis-specific transcripts are shielded from Mmi1-dependent mRNA elimination and can function stably. Reproduced from Ref. 67 with some modifications.
© Copyright Policy - open-access
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3037521&req=5

fig05: Function of the Mei2 dot as the mitosis–meiosis switch. Left panel: a number of meiosis-specific transcripts in fission yeast harbor a region designated the DSR. The DSR renders the selective elimination of these mRNAs if they are expressed during the mitotic cell cycle. Mmi1, a YTH-family RNA-binding protein localized in the nucleus, binds to the DSR and promotes the elimination of the corresponding transcript in cooperation with the RNA-degradation machinery exosome. Right panel: to promote meiosis, Mei2, which has an affinity for Mmi1, forms a dot structure in the nucleus together with meiRNA. Mmi1 is thereby sequestered to this structure so that meiosis-specific transcripts are shielded from Mmi1-dependent mRNA elimination and can function stably. Reproduced from Ref. 67 with some modifications.
Mentions: Unexpectedly, a direct link between the DSR–Mmi1 system and Mei2 was identified in our laboratory. Localization analysis of Mmi1 revealed that this protein is present in multiple nuclear foci during vegetative growth. Interestingly, these foci converge to a single dot in meiotic prophase, which we found to overlap with the Mei2 dot. The conversion of Mmi1 to a single dot did not occur however in the absence of Mei2 or meiRNA.67) These observations led us to speculate that the Mei2 dot may sequester Mmi1 and thus inhibit its function and ensure the stable expression of meiosis-specific transcripts (Fig. 5). Consistent with this idea, we observed that Mei2 and Mmi1 can physically interact. Furthermore, we found that the cell growth arrest prior to meiosis I caused by the loss of the Mei2 dot in fission yeast could be suppressed by an artificial reduction of Mmi1 activity.67) Hence, the key molecular function of the Mei2 dot in fission yeast is most likely to be the shutdown of the DSR–Mmi1 system during meiotic prophase.

Bottom Line: Meiosis-inducing signals in this microbe emanating from environmental conditions including the nutrient status converge on the activity of an RRM-type RNA-binding protein, Mei2.Fission yeast contains an RNA degradation system that selectively eliminates meiosis-specific mRNAs during the mitotic cell cycle.Mmi1, a novel RNA-binding protein of the YTH-family, is essential for this process.

View Article: PubMed Central - PubMed

Affiliation: Department of Biophysics and Biochemistry, Graduate School of Science, University of Tokyo, Tokyo, Japan. yamamoto@biochem.s.u-tokyo.ac.jp

ABSTRACT
The cellular programs for meiosis and mitosis must be strictly distinguished but the mechanisms controlling the entry to meiosis remain largely elusive in higher organisms. In contrast, recent analyses in yeast have shed new light on the mechanisms underlying the mitosis-meiosis switch. In this review, the current understanding of these mechanisms in the fission yeast Schizosaccharomyces pombe is discussed. Meiosis-inducing signals in this microbe emanating from environmental conditions including the nutrient status converge on the activity of an RRM-type RNA-binding protein, Mei2. This protein plays pivotal roles in both the induction and progression of meiosis and has now been found to govern the meiotic program in a quite unexpected manner. Fission yeast contains an RNA degradation system that selectively eliminates meiosis-specific mRNAs during the mitotic cell cycle. Mmi1, a novel RNA-binding protein of the YTH-family, is essential for this process. Mei2 tethers Mmi1 and thereby stabilizes the transcripts necessary for the progression of meiosis.

Show MeSH
Related in: MedlinePlus