SYCP2 and SYCP3 are required for cohesin core integrity at diplotene but not for centromere cohesion at the first meiotic division

Anna Kouznetsova,Ivana Novak,Christer HöÖG,Rolf Jessberger

doi:10.1242/jcs.02362

Anna Kouznetsova, Ivana Novak + Show 2 more

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https://doi.org/10.1242/jcs.02362

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Abstract

Much of the organization of the meiotic prophase-I chromosome axis is attributed to two groups of proteins: the axial element proteins, SYCP2 and SYCP3; and the cohesin-complex proteins. Although the cohesin-complex proteins ensure that sister chromatids remain paired during meiosis, the role of SYCP2 and SYCP3 is not clear. Interestingly, it has been shown that SYCP3 and SYCP2 associate with the centromere regions of male, but not female, metaphase-I chromosomes, suggesting a sex-specific function for the two proteins. We have analysed the spatial distribution of cohesin-complex proteins associated with meiotic chromosomes in germ cells derived from Sycp3-deficient female and male mice. We show that, in the absence of SYCP3, the cohesin cores associated with the female meiotic chromosomes disassemble prematurely at the diplotene stage of meiosis. We also show that SYCP3 and SYCP2 are not required for centromere cohesion at the metaphase-I stage in male germ cells. We conclude that SYCP3 has a temporally restricted role in maintaining, but not establishing, cohesin-core organization during prophase I. This finding supports a model in which the removal of bulk cohesin from paired sister chromatids at late prophase in both meiotic and mitotic cells ensures proper chromosome compaction and segregation.

Highlights

The generation of haploid germ cells requires a distinct chromosomal segregation process termed meiosis
Studies of Sycp3-deficient spermatocytes show that SYCP3 is required for recruitment of SYCP2 to the centromere regions, but we find no evidence that SYCP3 or SYCP2 are required for cohesin protein distribution or centromere cohesion at the metaphase I (MI) stage
We initially analysed the organization of the diplotene-dictyate meiotic chromosome axis in female meiotic germ cells derived from wild-type animals

Summary

Introduction

The generation of haploid germ cells requires a distinct chromosomal segregation process termed meiosis (for a review, see Petronczki et al, 2003). The paired sister chromatids are organized into parallel linear arrays of chromatin loops, the bases of which define a protein-rich chromosomal axis (Kleckner et al, 2004; Moens and Spyropoulos, 1995). The most prominent structural feature of the synapsed homologous chromosomes is their trilaminar organization, which is generated through the formation of the synaptonemal complex (SC), a meiosisspecific proteinaceous structure (for reviews, see Page and Hawley, 2004; Zickler and Kleckner, 1999). Cohesin-complex proteins are of critical importance for sister-chromatid pairing and separation during mitosis and meiosis (for a review, see Petronczki et al, 2003) and are likely to be key organizers of the chromatin loop arrays along the meiotic chromosome axes (Revenkova et al, 2004; Zickler and Kleckner, 1999). Three meiosisspecific cohesin subunits – REC8 (Eijpe et al, 2003), STAG3 (Prieto et al, 2001) and SMC1β (Revenkova et al, 2001) – have been identified in addition to the cohesin subunits that are produced in mitotic cells, which include SMC1α, SMC3 and RAD21 (Eijpe et al, 2000; Xu et al, 2004)

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