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

Tonami, Yuko; Murakami, Hiroshi; Shirahige, Katsuhiko; Nakanishi, Makoto

doi:10.1073/pnas.0407236102

Cited by 42 publications

(43 citation statements)

References 27 publications

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“…Furthermore, they were not restored even in the presence of cds1⌬ mek1⌬ double or cds1⌬ mek1⌬ chk1⌬ triple mutations. The inability of checkpoint mutations to rescue the defects of hsk1-89 is in a sharp contrast to hydroxyurea-induced inhibition of DSB formation, which is restored by mutations in the Rad3-Cds1 checkpoint pathway (31,32).…”

Section: Known Checkpoint Kinases Are Not Involved In Suppression Of Dsbmentioning

confidence: 93%

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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Section: Known Checkpoint Kinases Are Not Involved In Suppression Of Dsbmentioning

confidence: 93%

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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“…Works in S. cerevisiae and S. pombe suggest that meiotic cells monitor the progression of the replication forks and permit DSB formation only once the replication fork has passed. [57][58][59] Although Mec1 does not appear to be required for the meiotic DSB block in response to stalled replication forks, 57 it is tempting to speculate that a checkpoint, possibly dependent on the redundant activities of both Mec1 and Tel1, might be activated during premeiotic S phase to couple DNA replication and DSB formation.…”

Section: Discussionmentioning

confidence: 99%

Budding Yeast Sae2 is an In Vivo Target of the Mec1 and Tel1 Checkpoint Kinases During Meiosis

Cartagena‐Lirola

Guerini²,

Viscardi³

et al. 2006

Cell Cycle

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“…Synchronous meiosis was induced in liquid culture with haploid or diploid temperature-sensitive pat1 mutants as described in ref. 34. Cells were stained with 4Ј,6-diamidino-2-phenylindole for monitoring of meiotic progression as described in ref.…”

Section: Methodsmentioning

confidence: 99%

Mei4p coordinates the onset of meiosis I by regulating cdc25 ⁺ in fission yeast

Murakami-Tonami

Yamada‐Namikawa

Tochigi

et al. 2007

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

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The kinase Cdc2p is a central regulator of entry into and progression through nuclear division during mitosis and meiosis in eukaryotes. Cdc2p is activated at the onset of mitosis by dephosphorylation on tyrosine-15, the phosphorylation status of which is determined mainly by the kinase Wee1p and the phosphatase Cdc25p. In fission yeast, the forkhead-type transcription factor Mei4p is required for expression of many genes during meiosis, with mei4 mutant cells arresting before meiosis I. The mechanism of cell cycle arrest in mei4 cells has remained unknown, however. We now show that cdc25 ؉ is an important target of Mei4p in control of entry into meiosis I. Forced dephosphorylation of Cdc2p on tyrosine-15 thus induced meiosis I in mei4 mutant cells without a delay, although no spores were formed. We propose that Mei4p acts as a rate-limiting regulator of meiosis I by activating cdc25 ؉ transcription in coordination with other meiotic events.cell cycle ͉ transcription

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

Cited by 42 publications

References 27 publications

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

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

Budding Yeast Sae2 is an In Vivo Target of the Mec1 and Tel1 Checkpoint Kinases During Meiosis

Mei4p coordinates the onset of meiosis I by regulating cdc25 ⁺ in fission yeast

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

Cited by 42 publications

References 27 publications

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

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

Budding Yeast Sae2 is an In Vivo Target of the Mec1 and Tel1 Checkpoint Kinases During Meiosis

Mei4p coordinates the onset of meiosis I by regulating cdc25 + in fission yeast

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Mei4p coordinates the onset of meiosis I by regulating cdc25 ⁺ in fission yeast