Phosphorylation of Cohesin Rec11/SA3 by Casein Kinase 1 Promotes Homologous Recombination by Assembling the Meiotic Chromosome Axis

Sakuno, Takeshi; Watanabe, Yoshinori

doi:10.1016/j.devcel.2014.11.033

Cited by 46 publications

(77 citation statements)

References 61 publications

(88 reference statements)

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“…In addition, Red1 interacts with and requires Rec8‐cohesin for its normal chromosomal association (Panizza et al, ; Sun et al, ). From these data, it seems likely that an interaction between cohesin and Red1 is central to driving Red1 chromosomal loading (possibly via Scc3, the homolog of Psc3/Rec11, in a manner analogous to fission yeast Rec11‐Rec10 axis (Phadnis et al, ; Sakuno & Watanabe, ), although this interaction might also involve Rec8 directly (Sun et al, ). Interestingly, within budding yeast pericentromeres, Red1 and cohesin chromosomal patterns diverge: Here, Red1 levels are lower than cohesin levels (Sun et al, ).…”

Section: Control Of Meiotic Recombination Within Pericentromeresmentioning

confidence: 99%

“…One protein required for this assembly is a structural protein called Red1 (in budding yeast; the homolog of Red1 in fission yeast is called Rec10; Panizza et al, 2011;Sun et al, 2015). Work in fission yeast demonstrated that an interaction between Rec11-containing cohesin and Rec10 is needed for the efficient recruitment of Rec10 to fission yeast chromosomes (Phadnis et al, 2015;Sakuno & Watanabe, 2015). Pericentromeric cohesin contains Psc3 instead of Rec11 (see above; Kitajima et al, 2003), leading to an absence of Rec10 within pericentromeres.…”

Section: Control Of Meiotic Recombination Within Pericentromeresmentioning

confidence: 99%

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Kinetochores, cohesin, and DNA breaks: Controlling meiotic recombination within pericentromeres

Kuhl

Vader

2019

Yeast

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In meiosis, DNA break formation and repair are essential for the formation of crossovers between homologous chromosomes. Without crossover formation, faithful meiotic chromosome segregation and sexual reproduction cannot occur. Crossover formation is initiated by the programmed, meiosis‐specific introduction of numerous DNA double‐strand breaks, after which specific repair pathways promote recombination between homologous chromosomes. Despite its crucial nature, meiotic recombination is fraud with danger: When positioned or repaired inappropriately, DNA breaks can have catastrophic consequences on genome stability of the resulting gametes. As such, DNA break formation and repair needs to be carefully controlled. Within centromeres and surrounding regions (i.e., pericentromeres), meiotic crossover recombination is repressed in organisms ranging from yeast to humans, and a failure to do so is implicated in chromosome missegregation and developmental aneuploidy. (Peri)centromere sequence identity and organization diverge considerably across eukaryotes, yet suppression of meiotic DNA break formation and repair appear universal. Here, we discuss emerging work that has used budding and fission yeast systems to study the mechanisms underlying pericentromeric suppression of DNA break formation and repair. We particularly highlight a role for the kinetochore, a universally conserved, centromere‐associated structure essential for chromosome segregation, in suppressing (peri)centromeric DNA break formation and repair. We discuss the current understanding of kinetochore‐associated and chromosomal factors involved in this regulation and suggest future avenues of research.

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Section: Control Of Meiotic Recombination Within Pericentromeresmentioning

confidence: 99%

Section: Control Of Meiotic Recombination Within Pericentromeresmentioning

confidence: 99%

Kinetochores, cohesin, and DNA breaks: Controlling meiotic recombination within pericentromeres

Kuhl

Vader

2019

Yeast

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“…Like the SC, LinE formation requires a meiosis-specific sister chromatid cohesin complex containing Rec8 and Rec11 subunits, and phosphorylation of one of them (Rec11) by a casein kinase 1 ortholog 5, 6 . Rec8 forms filamentous structures with the chromosomes aligned in parallel from one end to the other during the horsetail stage of meiosis as observed in live cells by super-resolution structured illumination microscopy (SIM) 7 .…”

Section: Introductionmentioning

confidence: 99%

Functional organization of protein determinants of meiotic DNA break hotspots

Fowler

Martı́n-Castellanos

et al. 2017

Sci Rep

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During Schizosaccharomyces pombe meiotic prophase, homologous chromosomes are co-aligned by linear elements (LinEs) analogous to the axial elements of the synaptonemal complex (SC) in other organisms. LinE proteins also promote the formation of meiotic DNA double-strand breaks (DSBs), the precursors of cross-overs. Rec10 is required for essentially all DSBs and recombination, and three others (Rec25, Rec27, and Mug20) are protein determinants of DSB hotspots – they bind DSB hotspots with high specificity and are required for DSB formation there. These four LinE proteins co-localize in the nucleus in an interdependent way, suggesting they form a complex. We used random mutagenesis to uncover recombination-deficient missense mutants with novel properties. Some missense mutations changed essential residues conserved among Schizosaccharomyces species. DSB formation, gene conversion, and crossing-over were coordinately reduced in the mutants tested. Based on our mutant analysis, we revised the rec27 open reading frame: the new start codon is in the previously annotated first intron. Genetic and fluorescence-microscopy assays indicated that the Rec10 N- and C-terminal regions have complex interactions with Rec25. These mutants are a valuable resource to elucidate further how LinE proteins and the related SCs of other species regulate meiotic DSB formation to form crossovers crucial for meiosis.

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“…Several studies have shown how LinE subunits interact with each other and other meiotic proteins using yeast two-hybrid analysis or immunoprecipitation analysis (Loidl, 2006;Spirek et al, 2010;Miyoshi et al, 2012;Estreicher et al, 2012;Sakuno and Watanabe, 2015). We and others have shown that all LinE subunits are needed for intact LinE complex formation ( Figures 1C and S3) (Davis et al, 2008;Fowler et al, 2013).…”

Section: Line Missense Mutants Have Defective Line Structuresmentioning

confidence: 74%

Dynamic configurations of meiotic hotspot determinants

Chuang

Smith

2020

Preprint

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During meiosis, appropriate DNA double-strand break (DSB) and crossover distributions are required for proper homologous chromosome segregation in most species. Linear element proteins (LinEs) of Schizosaccharomyces pombe are DSB hotspot determinants. Clusters of LinE-bound hotspots form within ∼200 kb chromosomal regions independent of DSB formation. Previous reports showed that LinEs form chromatin-bound, dot-like nuclear foci in nuclear spreads and in fixed cells. Here, we investigated the regulation of LinE configuration and distribution in live cells using super-resolution fluorescence microscopy. In live cells at optimal meiotic temperature (∼25°C), LinEs made long linear forms, not previously reported, in both zygotic and azygotic meiosis and shared other characteristics with the synaptonemal complex in other species. LinE structures appeared around the time of replication, underwent a dotty-to-linear-to-dotty configurational transition, and disassembled before the first meiotic division. DSB formation and repair did not detectably influence LinE structure formation, but failure of DSB formation delayed LinE structure disassembly. Several LinE missense mutations formed dotty but not linear LinE configurations. Our study reveals a second, important configuration of LinEs, which suggests that LinE complexes are involved in regulating meiotic events, such as DSB repair, in addition to their established role in DSB formation.

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Phosphorylation of Cohesin Rec11/SA3 by Casein Kinase 1 Promotes Homologous Recombination by Assembling the Meiotic Chromosome Axis

Cited by 46 publications

References 61 publications

Kinetochores, cohesin, and DNA breaks: Controlling meiotic recombination within pericentromeres

Kinetochores, cohesin, and DNA breaks: Controlling meiotic recombination within pericentromeres

Functional organization of protein determinants of meiotic DNA break hotspots

Dynamic configurations of meiotic hotspot determinants

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