<i>CLB5</i> and <i>CLB6</i> are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint

Stuart, David A.; Wittenberg, Curt

doi:10.1101/gad.12.17.2698

Cited by 152 publications

(240 citation statements)

References 69 publications

(109 reference statements)

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“…DSBs were detected in fission yeast cells deficient in the B-type cyclins Cig2p (data not shown) or Cdc13p (this study) but not in budding yeast clb5 and clb6 mutants (4). However, B-type cyclins are required for meiotic S phase in both yeasts (23,25,26). These observations suggest that the roles of B-type cyclins and this cyclin-dependent kinase during meiosis differ between the two yeast species (4, 15, 18, 23, 26).…”

Section: Resultsmentioning

confidence: 95%

“…Mec1 (a homolog of fission yeast Rad3p) is not required for coupling of meiotic DNA replication to recombination initiation in budding yeast (5), although Mec1 is required for the linkage between meiotic DNA replication and the first meiotic nuclear division (23). This discrepancy might be due to the different roles of the checkpoint proteins in the two yeasts.…”

Section: Resultsmentioning

confidence: 99%

“…Budding yeast Mec1 is essential for viability, whereas fission yeast Rad3p is not (11,24). The hypomorphic mutant mec1-1 is deficient only in coupling of DNA replication and meiotic nuclear division, the link between DNA replication and DSB formation being intact (23). It is also possible that these two yeasts rely on completely different systems for the coordination between meiotic S phase and recombination initiation.…”

Section: Resultsmentioning

confidence: 99%

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A checkpoint control linking meiotic S phase and recombination initiation in fission yeast

Tonami

Murakami²,

Shirahige³

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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During meiosis, high levels of recombination initiated by DNA double-strand breaks (DSBs) occur only after DNA replication. However, how DSB formation is coupled to DNA replication is unknown. We examined several DNA replication proteins for a role in this coupling in Schizosaccharomyces pombe, and we show that ribonucleotide reductase, the rate-limiting enzyme of deoxyribonucleotide synthesis and the target of the DNA synthesis inhibitor hydroxyurea (HU) is indirectly required for DSB formation linked to DNA replication. However, in cells in which the function of the DNA-replication-checkpoint proteins Rad1p, Rad3p, Rad9p, Rad17p, Rad26p, Hus1p, or Cds1p was compromised, DSB formation occurred at similar frequencies in the absence or presence of HU. The DSBs in the HU-treated mutant cells occurred at normal sites and were associated with recombination. In addition, Cdc2p is apparently not involved in this process. We propose that the sequence of meiotic S phase and initiation of recombination is coordinated by DNA-replication-checkpoint proteins.cell cycle ͉ DNA replication ͉ meiosis ͉ double-strand break formation D uring meiosis, DNA replication occurs, followed by two rounds of chromosome segregation (1, 2). A high level of homologous recombination occurs after meiotic DNA replication but before the first meiotic nuclear division (1, 3-7). Meiotic recombination is required for the proper segregation of homologs at meiosis I, because a chromatid of one homolog recombines with a chromatid of the other homolog, thereby joining homologous chromosomes.It is well established that meiotic recombination in both budding and fission yeasts is initiated by DNA double-strand breaks (DSBs), catalyzed by the DNA topoisomerase type-2-related enzyme Spo11 in budding yeast (8) and Rec12p in fission yeast (6). Both Spo11 in budding yeast and Rec12p in fission yeast are also essential for meiotic recombination. In addition to Rec12p, meiotic DSB requires multiple gene products that are also essential for meiotic recombination in two yeasts (1, 2).The DNA-replication checkpoint operates during both the mitotic cell cycle and meiosis to ensure that chromosome segregation is blocked if DNA replication is incomplete (9-12). The proteins Rad1p, Rad3p, Rad9p, Rad17p, Rad26p, Hus1p, and Cds1p are required for operation of the DNA-replication checkpoint in fission yeast (9-11, 13). The DNA-replicationcheckpoint proteins send a signal to block mitosis via the cyclin-dependent kinase Cdc2p complexed with the B-type cyclin Cdc13p (9). The Cdc2p-Cdc13p protein kinase is fully activated at the onset of mitosis by dephosphorylation of Cdc2p Tyr-15 (9). Phosphorylation of Cdc2p on Tyr-15 is catalyzed by both the Wee1p and Mik1p Tyr kinases, and dephosphorylation is carried out mainly by the Cdc25p Tyr phosphatase (14).It has been proposed that DNA replication is directly coupled to initiation of DSB formation in budding yeast, because inhibition of the completion of DNA replication either by hydroxyurea (HU) treatment or by mutation of both ...

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Section: Resultsmentioning

confidence: 95%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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A checkpoint control linking meiotic S phase and recombination initiation in fission yeast

Tonami

Murakami²,

Shirahige³

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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“…Cells, grown at 25°C in MM (1% glucose) supplemented with 100 g͞ml of leucine and 100 g͞ml of adenine per liter Ϫ1 to 5 ϫ 10 6 cells͞ml, were washed with MM-NH 4 Cl (1% glucose) four times and resuspended in MM-NH 4 Cl (1% glucose) supplemented with 25 g͞ml of leucine, followed by incubation for 16 h at 25°C. After addition of an equal volume of prewarmed MM (containing 1 g͞liter of NH 4 Cl and 1% glucose) supplemented with 50 g͞ml of leucine and 70 g͞ml of adenine, meiosis was induced by shifting the temperature to 32°C or 34°C. Equal volumes of samples were withdrawn at each time point from each culture for FACS analyses and DNA analyses on pulsed-field gel electrophoresis.…”

Section: Methodsmentioning

confidence: 99%

Hsk1 kinase is required for induction of meiotic dsDNA breaks without involving checkpoint kinases in fission yeast

Ogino¹,

Hirota

Matsumoto³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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Cdc7 kinase, conserved through evolution, is known to be essential for mitotic DNA replication. The role of Cdc7 in meiotic recombination was suggested in Saccharomyces cerevisiae, but its precise role has not been addressed. Here, we report that Hsk1, the Cdc7-related kinase in Schizosaccharomyces pombe, plays a crucial role during meiosis. In a hsk1 temperature-sensitive strain (hsk1-89), meiosis is arrested with one nucleus state before meiosis I in most of the cells and meiotic recombination frequency is reduced by one order of magnitude, whereas premeiotic DNA replication is delayed but is apparently completed. Strikingly, formation of meiotic dsDNA breaks (DSBs) are largely impaired in the mutant, and Hsk1 kinase activity is essential for these processes. Deletion of all three checkpoint kinases, namely Cds1, Chk1, and Mek1, does not restore DSB formation, meiosis, or Cdc2 activation, which is suppressed in hsk1-89, suggesting that these aberrations are not caused by known checkpoint pathways but that Hsk1 may regulate DSB formation and meiosis. Whereas transcriptional induction of some rec genes and horsetail movement are normal, chromatin remodeling at ade6-M26, a recombination hotspot, which is prerequisite for subsequent DSB formation at this locus, is not observed in hsk1-89. These results indicate unique and essential roles of Hsk1 kinase in the initiation of meiotic recombination and meiosis.Cdc7-related kinase ͉ checkpoint control ͉ chromatin remodeling ͉ meiosis ͉ meiotic recombination A lthough recent studies revealed the presence of a number of conserved factors involved in mitotic DNA replication (1), it is largely unknown whether they play roles in meiotic replication and recombination (2, 3). Studies in fission and budding yeasts indicated essential roles of Cdc2 kinase (1) and Clb5-and Clb6-dependent Cdc28 kinase (4), respectively, in premeiotic DNA replication. Orc, Cdc18, and MCM are also required for premeiotic DNA synthesis (3, 5), although their requirement may not be identical to that during mitotic replication (2). It is not known whether initiation is regulated by a common mechanism or the same set of replication origins is used during premeiotic S phase. In budding yeast, strong coupling of DNA replication and meiotic recombination has been shown (6-9).Cdc7 kinase plays an essential role in firing replication origins during mitotic growth (10, 11). It was reported previously that meiotic recombination frequency is reduced, whereas premeiotic DNA replication proceeds, in the budding yeast cdc7 ts mutants and that Cdc7 may play a role in synaptonemal complex formation during meiosis, a step stabilizing homologous pairing during meiotic recombination (12,13), but the precise meiotic roles of Cdc7 have remained elusive. We report here that Hsk1, the fission yeast homologue of Cdc7 kinase, is required for efficient meiotic recombination and meiotic nuclear division. During meiosis, Hsk1 is required specifically for formation of dsDNA breaks (DSBs), an early event for meiotic recombinatio...

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“…In conjunction with the cyclins Clb5 and Clb6, Cdk28 then triggers the initiation of pre-meiotic S phase. 6,7 In Schizosaccharomyces pombe, the meiosis initiation pathway consists of Ste11 (a transcription factor), Mei2 (an RNA-binding protein), Pat1 (a kinase), Mmi1 (another RNA-binding protein) and Cdc2 (a Cdk) bound to Cig2 (a cyclin). Here, responding to nutritional cues, Mei2 promotes exit from the mitotic cell cycle by antagonizing the elimination of meiotic mRNAs.…”

Section: Introductionmentioning

confidence: 99%

Cdk3, a conjugation-specific cyclin-dependent kinase, is essential for the initiation of meiosis in Tetrahymena thermophila

et al. 2016

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Meiosis is an important process in sexual reproduction. Meiosis initiation has been found to be highly diverse among species. In yeast, it has been established that cyclin-dependent kinases (Cdks) and cyclins are essential components in the meiosis initiation pathway. In this study, we identified 4 Cdks in the model ciliate, Tetrahymena thermophila, and we found one of them, Cdk3, which is specifically expressed during early conjugation, to be essential for meiosis initiation. Cdk3 deletion led to arrest at the pair formation stage of conjugation. We then confirmed that Cdk3 acts upstream of double-strand break (DSB) formation. Moreover, we detected that Cdk3 is necessary for the expression of many genes involved in early meiotic events. Through proteomic quantification of phosphorylation, co-expression analysis and RNA-Seq analyses, we identified a conjugation-specific cyclin, Cyc2, which most likely partners with Cdk3 to initiate meiosis.

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CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint

Cited by 152 publications

References 69 publications

A checkpoint control linking meiotic S phase and recombination initiation in fission yeast

A checkpoint control linking meiotic S phase and recombination initiation in fission yeast

Hsk1 kinase is required for induction of meiotic dsDNA breaks without involving checkpoint kinases in fission yeast

Cdk3, a conjugation-specific cyclin-dependent kinase, is essential for the initiation of meiosis in Tetrahymena thermophila

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