Mammalian meiosis is more conserved by sex than by species: conserved co-expression networks of meiotic prophase

Su, Yongchun; Li, Yunfei

doi:10.1530/rep-11-0260

Cited by 8 publications

(10 citation statements)

References 55 publications

(70 reference statements)

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“…Also refer to Supplementary (Su et al, 2011). In contrast, in mPGCs we detected expression of NODAL, which has been shown in the mouse to have an autocrine signaling role during the specification of male PGCs (Souquet et al, 2012).…”

Section: Distinct and Overlapping Expression Of Members Of The Olfactmentioning

confidence: 83%

Comparative molecular portraits of human unfertilized oocytes and primordial germ cells at 10 weeks of gestation

Diedrichs

Mlody

Matz³

et al. 2012

Int. J. Dev. Biol.

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Primordial germ cells (PGCs) are precursors of gametes and share several features in common with pluripotent stem cells, such as alkaline phosphatase activity and the expression of pluripotency-associated genes such as OCT4 and NANOG. PGCs are able to differentiate into oocytes and spermatogonia and establish totipotency after fertilization. However, our knowledge of human germ cell development is still fragmentary. In this study, we have carried out genomewide comparisons of the transcriptomes and molecular portraits of human male PGCs (mPGCs), female PGCs (fPGCs) and unfertilized oocytes. We detected 9210 genes showing elevated expression in fPGCs, 9184 in mPGCs and 9207 in oocytes, with 6342 of these expressed in common. As well as known germ cell-related genes such as BLIMP1/PRDM1, PIWIL2, VASA/DDX4, DAZL, STELLA/ DPPA3 and LIN28, we also identified 465 novel non-annotated genes with orthologs in the mouse. A plethora of olfactory receptor-encoding genes were detected in all samples, which would suggest their involvement not only in sperm chemotaxis, but also in the development of female germ cells and oocytes. We anticipate that our data might increase our meagre knowledge of the genes and associated signaling pathways operative during germ cell development. This in turn might aid in the development of strategies enabling better differentiation and molecular characterisation of germ cells derived from either embryonic or induced pluripotent stem cells. Ultimately, this would have a profound relevance for reproductive as well as regenerative medicine.

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Section: Distinct and Overlapping Expression Of Members Of The Olfactmentioning

confidence: 83%

Comparative molecular portraits of human unfertilized oocytes and primordial germ cells at 10 weeks of gestation

Diedrichs

Mlody

Matz³

et al. 2012

Int. J. Dev. Biol.

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“…The estimated incidence is 1:50,000 to 1:100,000 [34]. In addition, our previous co-expression study also identified Rps6ka3 as a candidate prophase gene [35]. …”

Section: Resultsmentioning

confidence: 99%

Identification of germ cell-specific genes in mammalian meiotic prophase

Ray

2013

BMC Bioinformatics

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BackgroundMammalian germ cells undergo meiosis to produce sperm or eggs, haploid cells that are primed to meet and propagate life. Meiosis is initiated by retinoic acid and meiotic prophase is the first and most complex stage of meiosis when homologous chromosomes pair to exchange genetic information. Errors in meiosis can lead to infertility and birth defects. However, despite the importance of this process, germ cell-specific gene expression patterns during meiosis remain undefined due to difficulty in obtaining pure germ cell samples, especially in females, where prophase occurs in the embryonic ovary. Indeed, mixed signals from both germ cells and somatic cells complicate gonadal transcriptome studies.ResultsWe developed a machine-learning method for identifying germ cell-specific patterns of gene expression in microarray data from mammalian gonads, specifically during meiotic initiation and prophase. At 10% recall, the method detected spermatocyte genes and oocyte genes with 90% and 94% precision, respectively. Our method outperformed gonadal expression levels and gonadal expression correlations in predicting germ cell-specific expression. Top-predicted spermatocyte and oocyte genes were both preferentially localized to the X chromosome and significantly enriched for essential genes. Also identified were transcription factors and microRNAs that might regulate germ cell-specific expression. Finally, we experimentally validated Rps6ka3, a top-predicted X-linked spermatocyte gene. Protein localization studies in the mouse testis revealed germ cell-specific expression of RPS6KA3, mainly detected in the cytoplasm of spermatogonia and prophase spermatocytes.ConclusionsWe have demonstrated that, through the use of machine-learning methods, it is possible to detect germ cell-specific expression from gonadal microarray data. Results from this study improve our understanding of the transition from germ cells to meiocytes in the mammalian gonad. Further, this approach is applicable to other tissues for which isolating cell populations remains difficult.

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“…Although these divisions have many similarities between males and females, meiosis is also sexdimorphic. This particularly concerns timing, synchronization, the number of haploid gametes This has been demonstrated over the last 25 years by the use of a large number of mutant mouse models, mainly gene knockout mice [30][31][32].…”

Section: Topaz1 Ablation Leads To Chromosome Misalignments At Pro-metmentioning

confidence: 99%

“…It was hypothesized that the mechanisms regulating and controlling prophase I during mammalian meiosis, frequently named "checkpoints", are more stringent in males than in females. This has been demonstrated over the last 25 years by the use of a large number of mutant mouse models, mainly gene knockout mice [30][31][32].…”

Section: Topaz1 Ablation Leads To Chromosome Misalignments At Pro-metaphase Imentioning

confidence: 99%

Topaz1, an essential gene for murine spermatogenesis, down-regulates the expression of numerous testis-specific long non-coding RNAs

Chadourne

Poumerol

Jouneau

et al. 2021

Preprint

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Spermatogenesis comprises a coordinated process, including meiosis, to produce fertile male gametes. Previous study reported that Topaz1 is a germ cell specific gene highly conserved in vertebrates. Topaz1 knockout male mice are sterile. The mutant testes lack haploid germ cells and meiosis arrests at the first-division prophase-metaphase transition. Here, in order to better characterize the testicular phenotype of Topaz1-/- mice, we used RNA-seq analyses at two different developmental stages. At postnatal days 16 (P16), 205 genes were differentially expressed genes (DEGs) in Topaz1-/- testes. They suggest stress conditions in mutant testes. At P18, the number of DEGs was increased 10-fold and 90% were down-regulated. The absence of Topaz1 seems to disturb the expression of genes involved in microtubule and/or cilium mobility, spermatogenesis and first meiotic division during the transition from prophase to metaphase. This is consistent with the Topaz1?/- testis phenotype where microtubule networks and centrosomes are disrupted. Moreover, a quarter of P18-DEGs are long non-coding RNAs (lncRNAs). Three of them, down-regulated at P16 and P18, were studied. They are testis-specific, located in spermatocytes and their expression starts between P11 and P15. We report here the effects of the suppression of one of these lncRNAs, 4939463O16Rik. The mouse fertility is not affected although the sperm parameters are disturbed. Transcriptome of P18-4939463O16Rik-/- testes is altered and the affected molecular pathways include microtubule-based process, regulation of cilium movement, spermatogenesis, male gamete differentiation. The absence of TOPAZ1 protein or of 4930463O16Rik lncRNA showed the same enrichment clusters in mutant testes despite a contrasted phenotype on the male fertility. In conclusion, Topaz1 is an essential gene for male fertility in mice and seems to stabilize the expression of many lncRNAs. Its absence leads to meiotic arrest. Suppression of one lncRNA is dispensable for mouse fertility but is necessary during terminal differentiation of male gametes.

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Mammalian meiosis is more conserved by sex than by species: conserved co-expression networks of meiotic prophase

Cited by 8 publications

References 55 publications

Comparative molecular portraits of human unfertilized oocytes and primordial germ cells at 10 weeks of gestation

Comparative molecular portraits of human unfertilized oocytes and primordial germ cells at 10 weeks of gestation

Identification of germ cell-specific genes in mammalian meiotic prophase

Topaz1, an essential gene for murine spermatogenesis, down-regulates the expression of numerous testis-specific long non-coding RNAs

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