Mutations that affect meiosis in male mice influence the dynamics of the mid-preleptotene and bouquet stages

Liebe, Bodo; Petukhova, Galina V.; Barchi, Marco; Bellani, Marina A.; Braselmann, Herbert; Nakano, Toru; Pandita, Tej K.; Jasin, Maria; Fornace, Albert J.; Meistrich, M. L.; Baarends, Willy M.; Schimenti, John C.; Lange, Titia de; Keeney, Scott; Camerini‐Otero, R. Daniel; Scherthan, Harry

doi:10.1016/j.yexcr.2006.07.019

Cited by 57 publications

(50 citation statements)

References 101 publications

(177 reference statements)

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“…However, there may be another example of this meiotic paradigm, namely Bombyx mori females, which form telomere bouquets and elaborate SCs but do not exhibit meiotic recombination (41)(42)(43). In S. mediterranea, bouquet formation persists in spo11(RNAi) and sycp1(RNAi) mutants, indicating that telomere clustering in these mutants occurs independently of DSB or SC formation, being reminiscent of the mode of bouquet formation in yeast and mammals (3,44). We also show that meiotic DSBs preferentially occur near the base of the telomere bouquet in zygotene and that the SC is required for DSB maturation and repair.…”

Section: Discussionmentioning

confidence: 99%

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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Section: Discussionmentioning

confidence: 99%

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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“…7I). We presumed that these cells were abnormal spermatocytes blocked in leptotene-zygotene (Liebe et al, 2006;Mahadevaiah et al, 2001). In other tubules, the cells in the luminal region showed filamentous SYCP3 and XY bodies typical of pachytene spermatocytes (Fig.…”

Section: Bnc2 Is Required For Meiotic Progression Of Spermatocytesmentioning

confidence: 91%

The zinc-finger protein basonuclin 2 is required for proper mitotic arrest, prevention of premature meiotic initiation and meiotic progression in mouse male germ cells

et al. 2014

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Absence of mitosis and meiosis are distinguishing properties of male germ cells during late fetal and early neonatal periods. Repressors of male germ cell meiosis have been identified, but mitotic repressors are largely unknown, and no protein repressing both meiosis and mitosis is known. We demonstrate here that the zinc-finger protein BNC2 is present in male but not in female germ cells. In testis, BNC2 exists as several spliced isoforms and presumably binds to DNA. Within the male germ cell lineage, BNC2 is restricted to prospermatogonia and undifferentiated spermatogonia. Fetal prospermatogonia that lack BNC2 multiply excessively on embryonic day (E)14.5 and reenter the cell cycle prematurely. Mutant prospermatogonia also engage in abnormal meiosis; on E17.5, Bnc2−/− prospermatogonia start synthesizing the synaptonemal protein SYCP3, and by the time of birth, many Bnc2 −/− prospermatogonia have accumulated large amounts of nonfilamentous SYCP3, thus appearing to be blocked at leptonema. Bnc2 −/− prospermatogonia do not undergo proper male differentiation, as they lack almost all the mRNA for the malespecific methylation protein DNMT3L and have increased levels of mRNAs that encode meiotic proteins, including STRA8. Bnc2 −/− prospermatogonia can produce spermatogonia, but these enter meiosis prematurely and undergo massive apoptotic death during meiotic prophase. This study identifies BNC2 as a major regulator of male germ stem cells, which is required for repression of meiosis and mitosis in prospermatogonia, and for meiosis progression during spermatogenesis. In view of the extreme evolutionary conservation of BNC2, the findings described here are likely to apply to many species.

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“…formation, was found to be normal by cH2AX and SYCP3 (Liebe et al, 2006) staining of spreads of wild-type and Spoc1 2/2 spermatocytes (Fig. 6D).…”

Section: Spoc1 a New Factor Essential For Spermatogenesis 3143mentioning

confidence: 93%

SPOC1 (PHF13) is required for spermatogonial stem cell differentiation and sustained spermatogenesis

Bördlein

Scherthan

Nelkenbrecher

et al. 2011

Journal of Cell Science

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Summary SPOC1 (PHF13) is a recently identified protein that has been shown to dynamically associate with somatic chromatin, to modulate chromatin compaction and to be important for proper cell division. Here, we report on the expression of SPOC1 in promyelocytic leukaemia zinc finger (PLZF)-positive undifferentiated spermatogonial stem cells (SSCs) of the mouse testis. To investigate further the biological function of SPOC1 in germ cells we generated Spoc1 mutant mice from a gene-trap embryonic stem cell clone. Postpubertal homozygous Spoc1 2/2 animals displayed a pronounced progressive loss of germ cells from an initially normal germ epithelium of the testis tubules leading to testis hypoplasia. This loss first affected non-SSC stages of germ cells and then, at a later time point, the undifferentiated spermatogonia. Remarkably, successive loss of all germ cells (at .20 weeks of age) was preceded by a transient increase in the number of undifferentiated A aligned (A al ) spermatogonia in younger mice (at .10 weeks of age). The number of primary Spoc1 2/2 gonocytes, the proliferation of germ cells, and the initiation and progression of meiosis was normal, but we noted a significantly elevated level of apoptosis in the Spoc1 2/2 testis. Taken together, the data argue that SPOC1 is indispensable for stem cell differentiation in the testis and for sustained spermatogenesis.

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Mutations that affect meiosis in male mice influence the dynamics of the mid-preleptotene and bouquet stages

Cited by 57 publications

References 101 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

The zinc-finger protein basonuclin 2 is required for proper mitotic arrest, prevention of premature meiotic initiation and meiotic progression in mouse male germ cells

SPOC1 (PHF13) is required for spermatogonial stem cell differentiation and sustained spermatogenesis

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