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TEX14 is essential for intercellular bridges and fertility in male mice.

ABSTRACT: Cytokinesis in somatic cells concludes with the formation of a midbody, which is abscised to form individual daughter cells. In contrast, germ cell cytokinesis results in a permanent intercellular bridge connecting the daughter cells through a large cytoplasmic channel. During spermatogenesis, proposed roles for the intercellular bridge include germ cell communication, synchronization, and chromosome dosage compensation in haploid cells. Although several essential components of the midbody have recently been identified, essential components of the vertebrate germ cell intercellular bridge have until now not been described. Herein, we show that testis-expressed gene 14 (TEX14) is a novel protein that localizes to germ cell intercellular bridges. In the absence of TEX14, intercellular bridges are not observed by using electron microscopy and other markers. Spermatogenesis in Tex14(-/-) mice progresses through the transit amplification of diploid spermatogonia and the expression of early meiotic markers but halts before the completion of the first meiotic division. Thus, TEX14 is required for intercellular bridges in vertebrate germ cells, and these studies provide evidence that the intercellular bridge is essential for spermatogenesis and fertility.

SUBMITTER: Greenbaum MP

PROVIDER: S-EPMC1458781 | biostudies-literature | 2006 Mar

REPOSITORIES: biostudies-literature

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TEX14 is essential for intercellular bridges and fertility in male mice.

Greenbaum Michael P MP Yan Wei W Wu Meng-Hsieh MH Lin Yi-Nan YN Agno Julio E JE Sharma Manju M Braun Robert E RE Rajkovic Aleksandar A Matzuk Martin M MM

Proceedings of the National Academy of Sciences of the United States of America 20060320 13

Cytokinesis in somatic cells concludes with the formation of a midbody, which is abscised to form individual daughter cells. In contrast, germ cell cytokinesis results in a permanent intercellular bridge connecting the daughter cells through a large cytoplasmic channel. During spermatogenesis, proposed roles for the intercellular bridge include germ cell communication, synchronization, and chromosome dosage compensation in haploid cells. Although several essential components of the midbody have ...[more]

PMID: 16549803

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Project description:Germ cell connectivity via intercellular bridges is a widely conserved feature but its functional significance is poorly understood. Intercellular bridges are essential for fertility in male mice as genetic ablation of a critical bridge component, TEX14, causes loss of germ cell connectivity and meiotic failure, however the underlying reasons are unknown. A screen for meiosis-defective mouse mutants yielded a sterile mutant harboring a point mutation in Tex14 that leads to a partial loss of germ cell intercellular bridges. We utilized the Tex14 hypomorphs with reduced intercellular bridges, along with Tex14-null mice that completely lack bridges to examine the roles of germ cell connectivity during adult spermatogenesis. Complete or partial loss of intercellular bridges does not severely deplete spermatogonia, but spermatocytes are unable to undergo meiotic DNA replication and enter meiotic prophase. Phenotypic severity correlates with the extent of intercellular bridge depletion, with Tex14 hypomorphs containing a relatively larger number of spermatocytes undergoing meiosis, thus allowing us to assess impacts on meiotic progression. Tex14-deficient germ cells that enter prophase form meiotic breaks and initiate synapsis, but later exhibit synaptic failures and retain unrepaired breaks. Strikingly, Tex14-deficient germ cells derepress LINE1 retrotransposons and accumulate LINE1-encoded proteins during meiosis. Single-cell RNA-sequencing of testes from Tex14 hypomorphs show that intercellular bridge depletion modestly impacts the RNA landscape in early germ cell stages, while mutant cells that progress to late spermatocyte and post-meiotic spermatid stages broadly upregulate retrotransposons and dysregulate gene expression. RNA-sequencing confirms extensive sharing of transcripts between normal spermatids and demonstrates its partial attenuation in Tex14 hypomorphs, indicating that intercellular bridges enable exchange of cytoplasmic material between connected germ cells in testes. Tex14 hypomorphs display a progressive decline in germ cell numbers starting from the spermatocyte stage, with a complete lack of elongating spermatids, and are therefore sterile. Our findings reveal that the regulation of meiosis is non-cell-intrinsic and inform a model in which intercellular bridges orchestrate critical meiotic events and protect germline genome integrity during spermatogenesis, possibly by facilitating the exchange of regulatory factors.

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TEX14 is essential for intercellular bridges and fertility in male mice.

Publications

TEX14 is essential for intercellular bridges and fertility in male mice.

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