Direct Coupling Between Meiotic DNA Replication and Recombination Initiation

Borde, Valérie; Goldman, Alastair S. H.; Lichten, Michael

doi:10.1126/science.290.5492.806

Cited by 228 publications

(265 citation statements)

References 23 publications

Supporting

Mentioning

249

Contrasting

Unclassified

Order By: Relevance

“…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: 93%

Rec8 Guides Canonical Spo11 Distribution along Yeast Meiotic Chromosomes

Kugou

Fukuda

Yamada

et al. 2009

MBoC

109

143

View full text Add to dashboard Cite

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.

show abstract

Section: Dynamic Distributions Of Spo11 Along Meiotic Yeast Chromosomessupporting

confidence: 93%

Rec8 Guides Canonical Spo11 Distribution along Yeast Meiotic Chromosomes

Kugou

Fukuda

Yamada

et al. 2009

MBoC

109

143

View full text Add to dashboard Cite

show abstract

“…Borde et al (13) showed that delaying the replication of a chromosome segment specifically delays the formation of the break at that segment. Cha et al (14) showed that Spo11, which is required for interhomolog interaction, and Rec8, a meiosisspecific cohesin subunit, are negative and positive regulators for the progression of premeiotic S-phase, respectively.…”

mentioning

confidence: 99%

Perturbation of the Activity of Replication Origin by Meiosis-specific Transcription

Mori

Shirahige

2007

Journal of Biological Chemistry

View full text Add to dashboard Cite

We have determined the activity of all ARSs on the Saccharomyces cerevisiae chromosome VI as chromosomal replication origins in premeiotic S-phase by neutral/neutral two-dimensional gel electrophoresis. The comparison of origin activity of each origin in mitotic and premeiotic S-phase showed that one of the most efficient origins in mitotic S-phase, ARS605, was completely inhibited in premeiotic S-phase. ARS605 is located within the open reading frame of MSH4 gene that is transcribed specifically during an early stage of meiosis. Systematic analysis of relationships between MSH4 transcription and ARS605 origin activity revealed that transcription of MSH4 inhibited the ARS605 origin activity by removing origin recognition complex from ARS605. Deletion of UME6, a transcription factor responsible for repressing MSH4 during mitotic S-phase, resulted in inactivation of ARS605 in mitosis. Our finding is the first demonstration that the transcriptional regulation on the replication origin activity is related to changes in cell physiology. These results may provide insights into changes in replication origin activity in embryonic cell cycle during early developmental stages.Eukaryotic chromosomes consist of multiple replication units. Each origin of DNA replication is strictly controlled to fire only once in the cell cycle in the fixed sequential order (1, 2). This temporal program for origin firing is utilized for the maintenance of genome integrity through DNA replication checkpoint mechanism (3, 4). It was shown that a checkpoint effector kinase Rad53 repressed firing of late origins when replication was perturbed by hydroxy urea or methyl methane sulfonate. Furthermore, recent genome-wide studies of eukaryotic chromosomal DNA replication using Saccharomyces cerevisiae have provided us with a kinetic map of progression of DNA replication along the chromosome (5, 6). However, these studies were restricted to DNA replication during mitotic cell cycle and little is known about how these multiple replication origins behave under different cell cycle, i.e. meiotic cell cycle.The decision to enter the meiotic cell cycle is made in G 1 phase and this affects the way in which the G 1 /S transition is controlled. In budding yeast (S. cerevisiae), poor nutrient conditions are the cue to embark on the meiotic cell cycle, which culminates in the production of spores (7). The replication of chromosome is the first detectable cytological event in meiosis. The coordinated synthesis of genomic DNA requires multiple levels of regulation and a large number of gene products. Genetic analysis in S. cerevisiae indicates that the replicative machinery used to synthesize DNA in vegetative cells is also required for the duplication of chromosome in meiosis (8 -10).In S. cerevisiae, mitotic S-phase and premeiotic S-phase appear to be differently regulated. For example, premeiotic S-phase is 1.5-2 times longer than mitotic S-phase (11). However, replication kinetics as measured by neutral/neutral twodimensional gel electrophoresis of 100-kb s...

show abstract

“…A high level of homologous recombination occurs after meiotic DNA replication but before the first meiotic nuclear division (1,(3)(4)(5)(6)(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.…”

mentioning

confidence: 99%

“…In addition, it has been reported that the removal of active replication origin delays both replication and DSB appearance in budding yeast (5). However, in fission yeast, DSB formation occurs when completion of DNA replication is prevented by the inactivation of initiators of DNA replication (15).…”

mentioning

confidence: 99%

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.

View full text Add to dashboard Cite

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 ...

show abstract

Direct Coupling Between Meiotic DNA Replication and Recombination Initiation

Cited by 228 publications

References 23 publications

Rec8 Guides Canonical Spo11 Distribution along Yeast Meiotic Chromosomes

Rec8 Guides Canonical Spo11 Distribution along Yeast Meiotic Chromosomes

Perturbation of the Activity of Replication Origin by Meiosis-specific Transcription

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

Contact Info

Product

Resources

About