The Mouse Spo11 Gene Is Required for Meiotic Chromosome Synapsis

Romanienko, Peter; Camerini‐Otero, R. Daniel

doi:10.1016/s1097-2765(00)00097-6

Cited by 741 publications

(732 citation statements)

References 49 publications

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“…Furthermore, activation of DNA damage repair is a normal event in meiosis. During meiosis induction of DSBs by Spo11‐endonuclease occurs in the leptotene spermatocytes as the chromosomes begin to pair, in the same cell type with a high E2f1 expression level (Baudat et al ., 2000; Romanienko & Camerini‐Otero, 2000). In zygotene spermatocytes the pairing is completed and DSB repair and meiotic crossing‐over commence in the pachytene phase.…”

Section: Discussionmentioning

confidence: 99%

E2F1 controls germ cell apoptosis during the first wave of spermatogenesis

et al. 2015

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SummaryCell cycle control during spermatogenesis is a highly complex process owing to the control of the mitotic expansion of the spermatogonial cell population and following meiosis, induction of DNA breaks during meiosis and the high levels of physiological germ‐cell apoptosis. We set out to study how E2F1, a key controller of cell cycle, apoptosis, and DNA damage responses, functions in the developing and adult testis. We first analyzed the expression pattern of E2f1 during post‐natal testis development using RNA in situ hybridization, which showed a differential expression pattern of E2f1 in the adult and juvenile mouse testes. To study the function of E2f1, we took advantage of the E2F1−/− mouse line, which was back‐crossed to C57Bl/6J genetic background. E2f1 loss led to a severe progressive testicular atrophy beginning at the age of 20 days. Spermatogonial apoptosis during the first wave of spermatogenesis was decreased. However, already in the first wave of spermatogenesis an extensive apoptosis of spermatocytes was observed. In the adult E2F1−/− testes, the atrophy due to loss of spermatocytes was further exacerbated by loss of spermatogonial stem cells. Surprisingly, only subtle changes in global gene expression array profiling were observed in E2F1−/− testis at PND20. To dissect the changes in each testicular cell type, an additional comparative analysis of the array data was performed making use of previously published data on transcriptomes of the individual testicular cell types. Taken together, our data indicate that E2F1 has a differential role during first wave of spermatogenesis and in the adult testis, which emphasizes the complex nature of cell cycle control in the developing testis.

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Section: Discussionmentioning

confidence: 99%

E2F1 controls germ cell apoptosis during the first wave of spermatogenesis

et al. 2015

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“…In contrast to its relation to meiotic cohesins, the AE formation occurs independently on recombination initiation (Romanienko and Camerini-Otero 2000) and vice versa (Yuan et al 2000) in the mouse although this takes place during leptotene as well. The induction of DSBs occurs prior/or simultaneously to the formation of the chromosome axes and is catalyzed by the evolutionarily highly conserved topoisomerase Spo11 in mouse as in the other organisms (Cole et al 2010).…”

Section: First Step: the Assembly Of The Chromosomal Axes And The Aximentioning

confidence: 96%

“…Only 5-10% of meiotic nuclei showed some degree of synapsis as indicated by the presence of SYCP1, SYCE1 and SYCE2 in this study. The synapsis, however, occurred mainly between non-homologous chromosomes (Baudat et al 2000;Romanienko and Camerini-Otero 2000;Bolcun-Filas et al 2009). Besides, different studies have reported about interactions between early proteins of the recombination machinery and SC components.…”

Section: Second Step: the Assembly Of The Central Regionmentioning

confidence: 99%

Evolutionary history of the mammalian synaptonemal complex

et al. 2016

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“…Here we show that mouse spermatogenesis genes are relatively underrepresented on the X chromosome and female-biased genes are enriched on it. We used Spo11 -/-mice blocked in spermatogenesis early in meiosis 12 to evaluate the temporal pattern of gene expression in sperm development. Genes expressed before the Spo11 block are enriched on the X chromosome, whereas those expressed later in spermatogenesis are depleted.…”

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confidence: 99%

“…The disruption of Spo11 in mice blocks meiosis before pachytene and interrupts normal testis development (Fig. 3a,b) 12,22 . In agreement with the marked changes in testis morphology in Spo11 -/-mice (Fig.…”

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confidence: 99%

The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation

et al. 2004

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Sex chromosomes are subject to sex-specific selective evolutionary forces 1,2 . One model predicts that genes with sexbiased expression should be enriched on the X chromosome 2-5 . In agreement with Rice's hypothesis 3 , spermatogonial genes are over-represented on the X chromosome of mice 6 and sex-and reproduction-related genes are over-represented on the human X chromosome 7,8 . Male-biased genes are under-represented on the X chromosome in worms and flies 9-11 , however. Here we show that mouse spermatogenesis genes are relatively underrepresented on the X chromosome and female-biased genes are enriched on it. We used Spo11 -/-mice blocked in spermatogenesis early in meiosis 12 to evaluate the temporal pattern of gene expression in sperm development. Genes expressed before the Spo11 block are enriched on the X chromosome, whereas those expressed later in spermatogenesis are depleted. Inactivation of the X chromosome in male meiosis may be a universal driving force for X-chromosome demasculinization.To investigate the genomic distribution of mouse genes with patterns of sex-biased expression, we analyzed the chromosomal distribution of genes expressed in sexually dimorphic tissues. We consider genes that are preferentially expressed in such tissues as testis, ovary and placenta to be sex-biased genes. We used two approaches to define the tissue specificity of genes expressed in mice: analysis of large-scale microarray-based gene expression data and analysis of the distribution of expressed-sequence tags (ESTs) in different cDNA libraries. Instead of focusing on transcripts restricted to a single tissue, our analysis targeted the identification of tissue-enriched transcripts using a 'preferential expression measure' (PEM) 13 . As an uniform source of expression data, we used publicly available data sets of mouse RNA samples representing 49 tissues hybridized to Affymetrix mouse U74A microarrays (GNF data set) 14 and 20 tissues analyzed with RIKEN cDNA microarrays (RIKEN data set) 15 .In the GNF data set 14 , expression of 624 genes (∼7% of all analyzed) in testis was three times greater than the median expression in other tissues, and expression of 361 genes in testis was five times greater (PEM values >1.58 and >2.32, respectively). These genes are considered testis-enriched genes. The chromosomal distribution of testisenriched genes was significantly different from uniform (χ 2 = 30.8, P = 0.05; Fig. 1a and Supplementary Table 1 online). The most significant deviation from the average gene density was on the X chromosome, where testis-enriched genes were 2.5 times less dense (the ratio of the density of testis-enriched genes on the X chromosome to the average density on all chromosomes, ρ X , was 0.40; χ 2 = 7.7, P = 0.006). The depletion of testis-enriched genes on the X chromosome was independent of the cut-off (three or five times greater expression) used in the selection process (Table 1). In addition, genes that were expressed most highly in testis and all the genes detected in testis were underrepresen...

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The Mouse Spo11 Gene Is Required for Meiotic Chromosome Synapsis

Cited by 741 publications

References 49 publications

E2F1 controls germ cell apoptosis during the first wave of spermatogenesis

E2F1 controls germ cell apoptosis during the first wave of spermatogenesis

Evolutionary history of the mammalian synaptonemal complex

The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation

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