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Meiotic failure in male mice lacking an X-linked factor

¹ Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA; ² Department of Cell and Molecular Biology, Karolinska Institutet, SE-171 77 Stockholm, Sweden; ³ Howard Hughes Medical Institute, Whitehead Institute, and Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02142, USA; ⁴ Center for Animal Transgenesis and Germ Cell Research, New Bolton Center, University of Pennsylvania, Kennett Square, Pennsylvania 19348, USA; ⁵ Department of Cell and Developmental Biology, Biocenter of the University of Würzburg, Am Hubland, Würzburg 97074, Germany; ⁶ School of Molecular Biosciences and Center for Reproductive Biology, Washington State University, Pullman, Washington 99164, USA

Meiotic silencing of sex chromosomes may cause their depletion of meiosis-specific genes during evolution. Here, we challenge this hypothesis by reporting the identification of TEX11 as the first X-encoded meiosis-specific factor in mice. TEX11 forms discrete foci on synapsed regions of meiotic chromosomes and appears to be a novel constituent of meiotic nodules involved in recombination. Loss of TEX11 function causes chromosomal asynapsis and reduced crossover formation, leading to elimination of spermatocytes, respectively, at the pachytene and anaphase I stages. Specifically, TEX11-deficient spermatocytes with asynapsed autosomes undergo apoptosis at the pachytene stage, while those with only asynapsed sex chromosomes progress. However, cells that survive the pachytene stage display chromosome nondisjunction at the first meiotic division, resulting in cell death and male infertility. TEX11 interacts with SYCP2, which is an integral component of the synaptonemal complex lateral elements. Thus, TEX11 promotes initiation and/or maintenance of synapsis and formation of crossovers, and may provide a physical link between these two meiotic processes.

[Keywords: TEX11; male infertility; meiosis; synapsis; meiotic recombination; X chromosome]]

Received September 7, 2007; revised version accepted January 2, 2008.

⁸ Corresponding author.

E-MAIL pwang{at}vet.upenn.edu; FAX (215) 573-5188.

Supplemental material is available at http://www.genesdev.org.

Article is online at http://www.genesdev.org/cgi/doi/10.1101/gad.1613608.

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