Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes

Ishiguro, Kei‐ichiro; Kim, Jihye; Shibuya, Hiroki; Hernández‐Hernández, Abrahan; Suzuki, Aussie; Fukagawa, Tatsuo; Shioi, Go; Kanazawa, Hiroshi; Li, Xin C.; Schimenti, John C.; Höög, Christer; Watanabe, Yoshinori

doi:10.1101/gad.237313.113

Cited by 140 publications

(222 citation statements)

References 54 publications

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“…3 B and D). These results were surprising, because substantial homolog pairing precedes synapsis in budding yeast (30)(31)(32) and mammals (33,34).…”

Section: Full-length Homologous Pairing In S Mediterranea Occurs Promentioning

confidence: 70%

Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea

Xiang

Miller

Ross

et al. 2014

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

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In the 1920s, József Gelei proposed that chromosome pairing in flatworms resulted from the formation of a telomere bouquet followed by the extension of synapsis from telomeres at the base of the bouquet, thus facilitating homolog pairing in a processive manner. A modern interpretation of Gelei's model postulates that the synaptonemal complex (SC) is nucleated close to the telomeres and then extends progressively along the full length of chromosome arms. We used the easily visible meiotic chromosomes, a well-characterized genome, and RNAi in the sexual biotype of the planarian Schmidtea mediterranea to test that hypothesis. By identifying and characterizing S. mediterranea homologs of genes encoding synaptonemal complex protein 1 (SYCP1), the topoisomerase-like protein SPO11, and RAD51, a key player in homologous recombination, we confirmed that SC formation begins near the telomeres and progresses along chromosome arms during zygotene. Although distal regions pair at the time of bouquet formation, pairing of a unique interstitial locus is not observed until the formation of full-length SC at pachytene. Moreover, neither full extension of the SC nor homologous pairing is dependent on the formation of double-strand breaks. These findings validate Gelei's speculation that full-length pairing of homologous chromosomes is mediated by the extension of the SC formed near the telomeres. S. mediterranea thus becomes the first organism described (to our knowledge) that forms a canonical telomere bouquet but does not require double-strand breaks for synapsis between homologous chromosomes. However, the initiation of SC formation at the base of the telomere bouquet, which then is followed by full-length homologous pairing in planarian spermatocytes, is not observed in other species and may not be conserved.

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“…3 B and D). These results were surprising, because substantial homolog pairing precedes synapsis in budding yeast (30)(31)(32) and mammals (33,34).…”

Section: Full-length Homologous Pairing In S Mediterranea Occurs Promentioning

confidence: 70%

Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea

Xiang

Miller

Ross

et al. 2014

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

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“…The number of MEI4 foci further decreased from leptotene to zygotene in both mutant spermatocytes in which DSB repair and homologous synapsis are partially deficient (Bannister et al, 2004;Herrán et al, 2011). In the double Rad21L 2/2 Rec8 2/2 mutant, which has a greater reduction of the number of DSB repair foci and in which leptotene cells show a strong defect in axis formation (Ishiguro et al, 2014;Llano et al, 2012), the number of MEI4 foci was reduced to 3265% of wild-type levels (Fig. 5D,E).…”

Section: Research Articlementioning

confidence: 95%

“…n, number of nuclei. The number of DMC1 foci detected and quantified in wild-type and mutant mice in a previous study (Ishiguro et al, 2014) is plotted on the right y-axis.…”

Section: Discussion Association Of Mei4 With Chromosome Axesmentioning

confidence: 99%

“…2/2 and Stra8 2/2 ) are as described previously (Bannister et al, 2004;Baudat et al, 2000;Bolcun-Filas et al, 2007;Daniel et al, 2011;Ishiguro et al, 2014;Li and Schimenti, 2007;Mark et al, 2008;Pittman et al, 1998;Revenkova et al, 2004;Roig et al, 2010;Yuan et al, 2000). All experiments were carried out according to the CNRS guidelines and approved by the Ethics Committee of LanguedocRoussillon (CEEA-LR-11028).…”

Section: Micementioning

confidence: 99%

“…We have shown that mouse MEI4 is required for meiotic DSB formation, and that MEI4 is located at discrete foci on meiotic chromosome axes . The axis-associated protein HORMAD1, the yeast Hop1 ortholog and components of the cohesin complexes are required for wild-type DSB levels (Biswas et al, 2013;Daniel et al, 2011;Ishiguro et al, 2014;Llano et al, 2012). However, the nature and control of the interplay between DSB factors and chromosome axis components remain to be analyzed in the mouse.…”

Section: Introductionmentioning

confidence: 99%

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MEI4: a central player in the regulation of meiotic DNA double strand break formation in the mouse

Kumar

Ghyselinck

Ishiguro

et al. 2015

Journal of Cell Science

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The formation of programmed DNA double-strand breaks (DSBs) at the beginning of meiotic prophase marks the initiation of meiotic recombination. Meiotic DSB formation is catalyzed by SPO11 and their repair takes place on meiotic chromosome axes. The evolutionarily conserved MEI4 protein is required for meiotic DSB formation and is localized on chromosome axes. Here, we show that HORMAD1, one of the meiotic chromosome axis components, is required for MEI4 localization. Importantly, the quantitative correlation between the level of axis-associated MEI4 and DSB formation suggests that axis-associated MEI4 could be a limiting factor for DSB formation. We also show that MEI1, REC8 and RAD21L are important for proper MEI4 localization. These findings on MEI4 dynamics during meiotic prophase suggest that the association of MEI4 to chromosome axes is required for DSB formation, and that the loss of this association upon DSB repair could contribute to turning off meiotic DSB formation.

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STAG3‐mediated stabilization of REC8 cohesin complexes promotes chromosome synapsis during meiosis

et al. 2014

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Cohesion between sister chromatids in mitotic and meiotic cells is promoted by a ring-shaped protein structure, the cohesin complex. The cohesin core complex is composed of four subunits, including two structural maintenance of chromosome (SMC) proteins, one a-kleisin protein, and one SA protein. Meiotic cells express both mitotic and meiosis-specific cohesin core subunits, generating cohesin complexes with different subunit composition and possibly separate meiotic functions. Here, we have analyzed the in vivo function of STAG3, a vertebrate meiosis-specific SA protein. Mice with a hypomorphic allele of Stag3, which display a severely reduced level of STAG3, are viable but infertile. We show that meiocytes in homozygous mutant Stag3 mice display chromosome axis compaction, aberrant synapsis, impaired recombination and developmental arrest. We find that the three different a-kleisins present in meiotic cells show different dosage-dependent requirements for STAG3 and that STAG3-REC8 cohesin complexes have a critical role in supporting meiotic chromosome structure and functions.

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Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes

Cited by 140 publications

References 54 publications

Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea

Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea

MEI4: a central player in the regulation of meiotic DNA double strand break formation in the mouse

STAG3‐mediated stabilization of REC8 cohesin complexes promotes chromosome synapsis during meiosis

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