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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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Outline of the regulation of meiotic initiation by Pat1 kinase and its substrate Mei2. During vegetative growth, Pat1 kinase is functional and inactivates Mei2 by phosphorylation. In diploid cells exposed to nutritional starvation, an inhibitor of Pat1 kinase, Mei3, is produced and blocks the kinase activity of Pat1. This, together with enhanced transcription of the mei2 gene under starved conditions, results in the accumulation of the unphosphorylated form of Mei2, which then turns on meiosis.
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fig04: Outline of the regulation of meiotic initiation by Pat1 kinase and its substrate Mei2. During vegetative growth, Pat1 kinase is functional and inactivates Mei2 by phosphorylation. In diploid cells exposed to nutritional starvation, an inhibitor of Pat1 kinase, Mei3, is produced and blocks the kinase activity of Pat1. This, together with enhanced transcription of the mei2 gene under starved conditions, results in the accumulation of the unphosphorylated form of Mei2, which then turns on meiosis.

Mentions: Fission yeast cells initiate meiosis physiologically when two prerequisites are met. One is the heterozygosity of the mating-type loci, i.e. cells should carry both mat1-P and mat1-M. The other is a condition of nutrient deficiency, most notably a depletion of nitrogen with a reduction of glucose. When these conditions are satisfied, the gene products of mat1-P and mat1-M cooperatively induce expression of the mei3 gene, which encodes an inhibitor (pseudo-substrate) of Pat1 kinase.60–63) This process underpins why meiosis occurs only in diploid cells that are heterozygous for the P and M mating-type genes and are exposed to nutritional starvation. Nitrogen starvation also facilitates meiotic entry by enhancing the expression of ste11, the product of which in turn activates the transcription of mei2.12) The control of meiotic initiation by the Pat1–Mei2 system is schematically shown in Fig. 4.


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)

Outline of the regulation of meiotic initiation by Pat1 kinase and its substrate Mei2. During vegetative growth, Pat1 kinase is functional and inactivates Mei2 by phosphorylation. In diploid cells exposed to nutritional starvation, an inhibitor of Pat1 kinase, Mei3, is produced and blocks the kinase activity of Pat1. This, together with enhanced transcription of the mei2 gene under starved conditions, results in the accumulation of the unphosphorylated form of Mei2, which then turns on meiosis.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig04: Outline of the regulation of meiotic initiation by Pat1 kinase and its substrate Mei2. During vegetative growth, Pat1 kinase is functional and inactivates Mei2 by phosphorylation. In diploid cells exposed to nutritional starvation, an inhibitor of Pat1 kinase, Mei3, is produced and blocks the kinase activity of Pat1. This, together with enhanced transcription of the mei2 gene under starved conditions, results in the accumulation of the unphosphorylated form of Mei2, which then turns on meiosis.
Mentions: Fission yeast cells initiate meiosis physiologically when two prerequisites are met. One is the heterozygosity of the mating-type loci, i.e. cells should carry both mat1-P and mat1-M. The other is a condition of nutrient deficiency, most notably a depletion of nitrogen with a reduction of glucose. When these conditions are satisfied, the gene products of mat1-P and mat1-M cooperatively induce expression of the mei3 gene, which encodes an inhibitor (pseudo-substrate) of Pat1 kinase.60–63) This process underpins why meiosis occurs only in diploid cells that are heterozygous for the P and M mating-type genes and are exposed to nutritional starvation. Nitrogen starvation also facilitates meiotic entry by enhancing the expression of ste11, the product of which in turn activates the transcription of mei2.12) The control of meiotic initiation by the Pat1–Mei2 system is schematically shown in Fig. 4.

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