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Oocyte heterogeneity with respect to the meiotic silencing of unsynapsed X chromosomes in the XY female mouse

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Abstract

In the XY pachytene spermatocyte, the sex chromosomes do not synapse except for the pseudoautosomal region and become transcriptionally silenced. It has been suggested that the meiotic silencing of unsynapsed chromatin (MSUC) also occurs in oocytes. In the XY sex-reversed female mouse, the sex chromosomes fail to pair in the majority of oocytes and a greater number of oocytes are eliminated during the meiotic prophase compared to the XX female. Yet, many XY oocytes survive to reach the second meiotic metaphase. The goal of our current study was to determine whether the single X chromosome shows the characteristics of asynapsis and meiotic silencing in a proportion of XY oocytes, which can explain the survival of the remaining oocytes. We first examined the accumulation of markers associated with asynapsis or transcriptional silencing, i.e., BRCA1, γH2AX, H3K9me3, and H3K27me3, at the single X chromosome in the XY oocyte. We found that γH2AX and BRCA1 were enriched on the single X chromosome whereas H3K9me3 was not, and H3K27me3 was enriched at all chromosomes in the majority of XY oocytes. We next examined the meiotic silencing of the single X chromosome using enrichment of the X-encoded ATRX protein. On average, ATRX enrichment was lower in XY oocytes than in XX oocytes as expected from its half gene dosage. However, the intensity of ATRX staining in XY oocytes harboring γH2AX domains showed a remarkable heterogeneity. We conclude that MSUC occurs with varying consequences, resulting in a heterogeneous population of oocytes with respect to protein enrichment in the XY female mouse.

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Acknowledgments

We are grateful for the gift of antibodies to Drs. P. Moens (deceased) and S. Namekawa. This work was supported by funds from the Natural Sciences and Engineering Research Council of Canada Discovery Grants program (to AN and TT).

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Authors and Affiliations

  1. Department of Surgery, McGill University, Montreal, QC, Canada

    Teruko Taketo

  2. Department of Biology, McGill University, Montreal, QC, Canada

    Teruko Taketo

  3. Department of Obstetrics and Gynecology, McGill University, Montreal, QC, Canada

    Teruko Taketo & Anna K. Naumova

  4. Department of Human Genetics, McGill University, Montreal, QC, Canada

    Anna K. Naumova

  5. The Research Institute of McGill University Health Centre, Montreal, QC, Canada

    Teruko Taketo & Anna K. Naumova

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  1. Teruko Taketo
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  2. Anna K. Naumova
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Correspondence to Teruko Taketo.

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Taketo, T., Naumova, A.K. Oocyte heterogeneity with respect to the meiotic silencing of unsynapsed X chromosomes in the XY female mouse. Chromosoma 122, 337–349 (2013). https://doi.org/10.1007/s00412-013-0415-z

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  • DOI: https://doi.org/10.1007/s00412-013-0415-z

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