Spo5 phosphorylation is essential for its own timely degradation and for successful meiosis in<i>Schizosaccharomyces pombe</i>

Okuzaki, Daisuke; Kasama, Toshio; Hirata, Aiko; Ohtaka, Ayami; Kakegawa, Reiko; Nishimura, Hiroshi

doi:10.4161/cc.9.18.12937

Cited by 8 publications

(8 citation statements)

References 16 publications

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“…Another study has shown that the N‐terminal region of Spo5 is phosphorylated, which contributes to the timely degradation and proper function of the protein (Okuzaki et al . ). We confirmed the previous findings that the unphosphorylatable mutant spo5‐4A is dysfunctional and that the phosphomimetic spo5‐4D is functional (Fig.…”

Section: Resultsmentioning

confidence: 97%

The RNA‐binding protein Spo5 promotes meiosis II by regulating cyclin Cdc13 in fission yeast

et al. 2014

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Meiosis comprises two consecutive nuclear divisions, meiosis I and II. Despite this unique progression through the cell cycle, little is known about the mechanisms controlling the sequential divisions. In this study, we carried out a genetic screen to identify factors that regulate the initiation of meiosis II in the fission yeast Schizosaccharomyces pombe. We identified mutants deficient in meiosis II progression and repeatedly isolated mutants defective in spo5, which encodes an RNA-binding protein. Using fluorescence microscopy to visualize YFP-tagged protein, we found that spo5 mutant cells precociously lost Cdc13, the major B-type cyclin in fission yeast, before meiosis II. Importantly, the defect in meiosis II was rescued by increasing CDK activity. In wild-type cells, cdc13 transcripts increased during meiosis II, but this increase in cdc13 expression was weaker in spo5 mutants. Thus, Spo5 is a novel regulator of meiosis II that controls the level of cdc13 expression and promotes de novo synthesis of Cdc13. We previously reported that inhibition of Cdc13 degradation is necessary to initiate meiosis II; together with the previous information, the current findings indicate that the dual control of Cdc13 by de novo synthesis and suppression of proteolysis ensures the progression of meiosis II.

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Section: Resultsmentioning

confidence: 97%

The RNA‐binding protein Spo5 promotes meiosis II by regulating cyclin Cdc13 in fission yeast

et al. 2014

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“…Several RNA-binding proteins, including Mei2, Spo5 and Meu5, have been implicated in meiosis in fission yeast (39–41). When meiosis was induced in three homothallic strains—parental (FY12806), red5 + (SP1428) and red5-2 (SP1479)—by nitrogen depletion, we found that red5-2 cells hardly mated and produced fewer asci compared with parental or red5 + cells (Figure 3A, left).…”

Section: Resultsmentioning

confidence: 99%

Red5 and three nuclear pore components are essential for efficient suppression of specific mRNAs during vegetative growth of fission yeast

Sugiyama

Wanatabe

Kitahata

et al. 2013

Nucleic Acids Research

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Zinc-finger domains are found in many nucleic acid-binding proteins in both prokaryotes and eukaryotes. Proteins carrying zinc-finger domains have important roles in various nuclear transactions, including transcription, mRNA processing and mRNA export; however, for many individual zinc-finger proteins in eukaryotes, the exact function of the protein is not fully understood. Here, we report that Red5 is involved in efficient suppression of specific mRNAs during vegetative growth of Schizosaccharomyces pombe. Red5, which contains five C3H1-type zinc-finger domains, localizes to the nucleus where it forms discrete dots. A red5 point mutation, red5-2, results in the upregulation of specific meiotic mRNAs in vegetative mutant red5-2 cells; northern blot data indicated that these meiotic mRNAs in red5-2 cells have elongated poly(A) tails. RNA-fluorescence in situ hybridization results demonstrate that poly(A)+ RNA species accumulate in the nucleolar regions of red5-deficient cells. Moreover, Red5 genetically interacts with several mRNA export factors. Unexpectedly, three components of the nuclear pore complex also suppress a specific set of meiotic mRNAs. These results indicate that Red5 function is important to meiotic mRNA degradation; they also suggest possible connections among selective mRNA decay, mRNA export and the nuclear pore complex in vegetative fission yeast.

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“…The spo5 mutant was isolated as a sporulation-deficient mutant in the original genetic screen of defective mutants in meiotic progression and/or sporulation, performed nearly half a century ago [ 15 ]. Previous studies have indicated that the spo5 + gene encodes a meiosis-specific RNA-binding protein, carrying two RNA-recognition motifs (RRMs) in the C-terminal part (aas 192–567), and regulates the progression of meiosis II and spore formation [ 16 - 20 ]. Although it seems apparent that Spo5 plays an essential role to coordinate meiosis and sporulation, controlling a number of targets, the RNA molecules that bind to Spo5 have not yet been identified, except for our recent finding that cdc13 + mRNA, encoding cyclin B, can do so [ 21 ].…”

Section: Introductionmentioning

confidence: 99%

Functional significance of nuclear export and mRNA binding of meiotic regulator Spo5 in fission yeast

et al. 2014

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BackgroundMeiotic cells undergo two rounds of nuclear division and generate gametes. Previous studies have indicated that a number of transcription factors modulate the transcriptome in successive waves during meiosis and spore formation in fission yeast. However, the mechanisms underlying the post-transcriptional regulation in meiosis are not fully understood. The fission yeast spo5 + gene encodes a meiosis-specific RNA-binding protein, which is required for the progression of meiosis II and spore formation. However, the target RNA molecules of Spo5 are yet to be identified. Characterization of meiosis-specific RNA-binding proteins will provide insight into how post-transcriptional regulation influence gene expression during sexual differentiation.ResultsTo assess the functional significance of RNA-recognition motifs (RRMs) of Spo5, we constructed a series of new spo5 truncated mutants and previously reported spo5 missense mutants. In addition, we isolated novel spo5 missense mutants. The phenotypic characteristics of these mutants indicated that the RRMs are essential for both the localization and function of the protein. Interestingly, Spo5 is exported from the nucleus to the cytoplasm via the Rae1-dependent mRNA export pathway, but is unlikely to be involved in global mRNA export. Furthermore, cytoplasmic localization of Spo5 is important for its function, which suggests the involvement of Spo5 in post-transcriptional regulation. We identified pcr1 + mRNA as one of the critical targets of Spo5. The pcr1 + gene encodes an activating transcription factor/cAMP response element binding (ATF/CREB) transcription factor family. Among the four family members, namely Pcr1, Atf1, Atf21, and Atf31, only the mRNA encoding Pcr1 binds to Spo5.ConclusionsSpo5 is exported from the nucleus with mRNAs via the Rae1-dependent pathway. RRMs are necessary for this process and also for the function of Spo5 after the nuclear export. Spo5 appears to influence the activity of pcr1 + mRNA, and the mechanism of how Spo5 stimulates the mRNA to promote the progression of meiosis II and spore formation remains an intriguing question for future research.

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Spo5 phosphorylation is essential for its own timely degradation and for successful meiosis inSchizosaccharomyces pombe

Cited by 8 publications

References 16 publications

The RNA‐binding protein Spo5 promotes meiosis II by regulating cyclin Cdc13 in fission yeast

The RNA‐binding protein Spo5 promotes meiosis II by regulating cyclin Cdc13 in fission yeast

Red5 and three nuclear pore components are essential for efficient suppression of specific mRNAs during vegetative growth of fission yeast

Functional significance of nuclear export and mRNA binding of meiotic regulator Spo5 in fission yeast

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