Clustering of meiotic double-strand breaks on yeast chromosome III

Baudat, Frédéric; Nicolas, Alain

doi:10.1073/pnas.94.10.5213

Cited by 307 publications

(315 citation statements)

References 49 publications

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“…Alternatively, a delay in the onset of premeiotic S phase in the mutant might affect DSB formation. It is shown that premeiotic S phase is tightly coupled with the formation of meiotic DSBs (16,27). However, we think these indirect effects are unlikely.…”

Section: Discussionmentioning

confidence: 98%

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Rad6-Bre1-mediated histone H2B ubiquitylation modulates the formation of double-strand breaks during meiosis

Yamashita

Shinohara

2004

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

104

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An E2 ubiquitin-conjugating enzyme, Rad6, working with an E3 ubiquitin ligase Bre1, catalyzes monoubiquitylation of histone H2B on a C-terminal lysine residue. The rad6 mutant of Saccharomyces cerevisiae shows a meiotic prophase arrest. Here, we analyzed meiotic defects of a rad6 null mutant of budding yeast. The rad6 mutant exhibits pleiotropic phenotypes during meiosis. RAD6 is required for efficient formation of double-strand breaks (DSBs) at meiotic recombination hotspots, which is catalyzed by Spo11. The mutation decreases overall frequencies of DSBs in a cell. The effect of the rad6 mutation is local along chromosomes; levels of DSBs at stronger hotspots are particularly reduced in the mutant. The absence of RAD6 has little effect on the formation of ectopic DSBs targeted by Spo11 fusion protein with a Gal4 DNA-binding domain. Furthermore, the disruption of the BRE1 as well as substitution of the ubiquitylation site of histone H2B also reduces some DSB formation similar to the rad6. These results suggest that Rad6-Bre1, through ubiquitylation of histone H2B, is necessary for efficient recruitment and͞or stabilization of a DSB-forming machinery containing Spo11. Histone tail modifications might play a role in DSB formation during meiosis.

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Section: Discussionmentioning

confidence: 98%

“…3K). Along the chromosome, DSBs are clustered around the middle part of both arms (16,21). rad6 reduced overall amounts of DSBs along the chromosome but did not change the distribution of DSBs.…”

Section: Gat1 (mentioning

confidence: 99%

Rad6-Bre1-mediated histone H2B ubiquitylation modulates the formation of double-strand breaks during meiosis

Yamashita

Shinohara

2004

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

104

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“…For example, chromatin remodeling factors and histone modifications such as acetylation, methylation, and ubiquitination are involved in the meiotic alteration of the local chromatin structure at DSB sites (Sollier et al, 2004;Yamada et al, 2004;Yamashita et al, 2004;Mieczkowski et al, 2007). In addition, genome-wide studies have shown that DSB regions are distributed nonrandomly in DSB hot and cold domains (Baudat and Nicolas, 1997;Gerton et al, 2000;Borde et al, 2004;Blitzblau et al, 2007;Buhler et al, 2007) and that DSBs are formed preferentially in regions of chromatin loops (Blat et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

“…To uncover the regional regulation of Spo11, it is necessary to determine the chromosome-wide dynamic distribution of Spo11 in wild-type cells. Previous genome-wide studies of the Spo11 distribution along yeast chromosomes were performed in the rad50S-like mutant background, in which DSB ends are left unprocessed with covalently bound Spo11 (Alani et al, 1990), providing the map that does not taken into account the dynamic features of the process (Baudat and Nicolas, 1997;Mieczkowski et al, 2006Mieczkowski et al, , 2007Robine et al, 2007). The binding sites of Spo11 in rad50S-like mutants have been considered as DSB formation sites.…”

Section: Introductionmentioning

confidence: 99%

Rec8 Guides Canonical Spo11 Distribution along Yeast Meiotic Chromosomes

Kugou

Fukuda

Yamada

et al. 2009

MBoC

108

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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“…Recombination in budding yeast is initiated by the formation of DSBs, a process which may be highly conserved among other organisms [13,14]. Depending on the size of genome, one meiotic nucleus may contain numerous DSBs [15] and recombinational repair of the DSBs occurs at the sites of initiation of synapsis, providing a way for pairing between homologous chromosomes [2,16,17].…”

Section: Genes Involved In Dsb Formation: Spo11 and Othersmentioning

confidence: 99%

Double-stranded DNA breaks and gene functions in recombination and meiosis

Mā

2006

Cell Res

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Gene functions in recombination and meiosis 402 npg REVIEW Meiotic prophase I is a long and complex phase. Homologous recombination is an important process that occurs between homologous chromosomes during meiotic prophase I. Formation of chiasmata, which hold homologous chromosomes together until the metaphase I to anaphase I transition, is critical for proper chromosome segregation. Recent studies have suggested that the SPO11 proteins have conserved functions in a number of organisms in generating sites of double-stranded DNA breaks (DSBs) that are thought to be the starting points of homologous recombination. Processing of these sites of DSBs requires the function of RecA homologs, such as RAD51, DMC1, and others, as suggested by mutant studies; thus the failure to repair these meiotic DSBs results in abnormal chromosomal alternations, leading to disrupted meiosis. Recent discoveries on the functions of these RecA homologs have improved the understanding of the mechanisms underlying meiotic homologous recombination.Cell Research (2006) Meiosis is a highly coordinated cell division, which generates four haploid reproductive cells required for sexual reproduction. Meiosis involves one round of DNA replication and two nuclear divisions, meiosis I and meiosis II. The first nuclear division leads to the segregation of homologous chromosomes (homologs), and is unique to meiosis. During the second division, sister chromatids are separated, resulting in the formation of four haploid nuclei and followed by the meiotic cytokinesis that forms four haploid cells. Similar to mitosis, both meiosis I and meiosis II can be divided into four stages: prophase, metaphase, anaphase, and telophase.However, meiosis I differs from meiosis II as meiosis I involves homology search, pairing, interhomolog recombination, and synapsis of homologs, processes that are required for correct association and segregation of homologs. The prophase stage of meiosis I, or prophase I, has been the target of interest because of the occurrence of these major processes of chromosome interactions. During early prophase I, arms of sister chromosomes are closely associated by protein complexes called cohesins, which are removed during the metaphase I/anaphase I transition. However, the centromere regions remained associated until the segregation of sister chromatids during meiosis II. Homologous pairing is the result of interaction between homologous chromosomes relying on the homology of DNA sequences [1,2], and is considered to be a transient and non-stable association between homologous chromosomes. Pairing between homologous chromosomes facilitates the process of recombination. The recombination process confers the interexchange of genetic information between non-sister chromatids, and generates chiasmata, which ensure proper association between homologous chromosomes prior to chromosome segregation at anaphase I. Synapsis, however, is a stable association by forming synaptonemal complexes between chromosomes. Synaptonemal complexes are threeparti...

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Clustering of meiotic double-strand breaks on yeast chromosome III

Cited by 307 publications

References 49 publications

Rad6-Bre1-mediated histone H2B ubiquitylation modulates the formation of double-strand breaks during meiosis

Rad6-Bre1-mediated histone H2B ubiquitylation modulates the formation of double-strand breaks during meiosis

Rec8 Guides Canonical Spo11 Distribution along Yeast Meiotic Chromosomes

Double-stranded DNA breaks and gene functions in recombination and meiosis

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