Correlation between premeiotic DNA replication and chromatin transition at yeast recombination initiation sites

Murakami, Hajime

doi:10.1093/nar/gkg441

Cited by 50 publications

(42 citation statements)

References 26 publications

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“…These results indicate that the distribution of Spo11 to later replicating regions would be coupled to DNA replication-related processes. This is consistent with previous observations that the Spo11-dependent chromatin alterations, DSB formation and DNA replicationrelated processes are tightly coupled (Borde et al, 2000;Murakami et al, 2003;Sasanuma et al, 2008;Wan et al, 2008). One possible mechanism for such coupling is that the Spo11-containing DSB machineries may migrate with the active DNA replication forks.…”

Section: Dynamic Distributions Of Spo11 Along Meiotic Yeast Chromosomessupporting

confidence: 92%

Rec8 Guides Canonical Spo11 Distribution along Yeast Meiotic Chromosomes

Kugou

Fukuda

Yamada

et al. 2009

MBoC

109

143

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Spo11-mediated DNA double-strand breaks (DSBs) that initiate meiotic recombination are temporally and spatially controlled. The meiotic cohesin Rec8 has been implicated in regulating DSB formation, but little is known about the features of their interplay. To elucidate this point, we investigated the genome-wide localization of Spo11 in budding yeast during early meiosis by chromatin immunoprecipitation using high-density tiling arrays. We found that Spo11 is dynamically localized to meiotic chromosomes. Spo11 initially accumulated around centromeres and thereafter localized to arm regions as premeiotic S phase proceeded. During this stage, a substantial proportion of Spo11 bound to Rec8 binding sites. Eventually, some of Spo11 further bound to both DSB and Rec8 sites. We also showed that such a change in a distribution of Spo11 is affected by hydroxyurea treatment. Interestingly, deletion of REC8 influences the localization of Spo11 to centromeres and in some of the intervals of the chromosomal arms. Thus, we observed a lack of DSB formation in a region-specific manner. These observations suggest that Rec8 would prearrange the distribution of Spo11 along chromosomes and will provide clues to understanding temporal and spatial regulation of DSB formation.

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Section: Dynamic Distributions Of Spo11 Along Meiotic Yeast Chromosomessupporting

confidence: 92%

Rec8 Guides Canonical Spo11 Distribution along Yeast Meiotic Chromosomes

Kugou

Fukuda

Yamada

et al. 2009

MBoC

109

143

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“…Strong coupling between premiotic DNA replication and meiotic recombination has been reported in budding yeast (6)(7)(8)(9). Although premeiotic DNA replication is slightly delayed in hsk1-89 cells, evidence indicates that recombination and meiotic defects may not be consequences of incomplete DNA replication.…”

Section: Discussionmentioning

confidence: 87%

“…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)(7)(8)(9).…”

mentioning

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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“…Sequences that serve as hotspots for DSB formation become more accessible (as evidenced by an increase in nuclease sensitivity) just prior to recombination initiation (Ohta et al 1994). Spo11 cannot cleave DNA that has not undergone premeiotic DNA replication and the associated transition in chromatin structure (Borde et al 2000;Cha et al 2000;Smith et al 2001;Murakami et al 2003). Sister-chromatid cohesion is regulated in a meiosis-specific manner and cohesion depends on proteins produced specifically in meiotic cells (Petronczki et al 2003).…”

Section: Discussionmentioning

confidence: 99%

Saccharomyces cerevisiae Mer2, Mei4 and Rec114 Form a Complex Required for Meiotic Double-Strand Break Formation

2006

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In budding yeast, at least 10 proteins are required for formation of the double-strand breaks (DSBs) that initiate meiotic recombination. Spo11 is the enzyme responsible for cleaving DNA and is found in a complex that also contains Ski8, Rec102, and Rec104. The Mre11/Rad50/Xrs2 complex is required for both DSB formation and DSB processing. In this article we investigate the functions of the remaining three proteins-Mer2, Mei4, and Rec114-with particular emphasis on Mer2. The Mer2 protein is present in vegetative cells, but it increases in abundance and becomes phosphorylated specifically during meiotic prophase. Mer2 localizes to distinct foci on meiotic chromosomes, with foci maximally abundant prior to the formation of synaptonemal complex. If DSB formation is blocked (e.g., by a spo11 mutation), dephosphorylation of Mer2 and its dissociation from chromosomes are delayed. We have also found that the Mei4 and Rec114 proteins localize to foci on chromosomes and these foci partially colocalize with each other and with Mer2. Furthermore, the three proteins co-immunoprecipitate. Mer2 does not show significant colocalization with Mre11 or Rec102 and Mer2 does not co-immunoprecipitate with Rec102. We propose that Mer2, Mei4, and Rec114 form a distinct complex required for DSB formation.

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Correlation between premeiotic DNA replication and chromatin transition at yeast recombination initiation sites

Cited by 50 publications

References 26 publications

Rec8 Guides Canonical Spo11 Distribution along Yeast Meiotic Chromosomes

Rec8 Guides Canonical Spo11 Distribution along Yeast Meiotic Chromosomes

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

Saccharomyces cerevisiae Mer2, Mei4 and Rec114 Form a Complex Required for Meiotic Double-Strand Break Formation

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