Dissecting chicken germ cell dynamics by combining a germ cell tracing transgenic chicken model with single-cell RNA sequencing

Rengaraj, Deivendran; Gon, Dong; Lee, Hong Jo; Lee, Kyung Youn; Choi, Yoon Ha; Jung, Kyung Min; Kim, Young Min; Choi, Hojun; Yoo, Eunhui; Woo, Seung Je; Park, Jin Se; Park, Kyung Je; Kim, Jong; Han, Jae Yong

doi:10.1016/j.csbj.2022.03.040

Cited by 16 publications

(27 citation statements)

References 101 publications

(134 reference statements)

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“…Although our result showed female-specific potential pathways and processes, Rengaraj et al reported many male-biased genes via transcriptome analysis using PGCs collected from early embryos (E2.5-E8) in a very recent study 25 . These differences may be caused by molecular markers used in purifying the PGCs.…”

Section: Discussioncontrasting

confidence: 67%

“…However, this study provided no data suggesting the relationship between DMRT1 and the sex determination of PGCs. In a previous study, sex-biased expression of DMRT1 was observed in the germ cells of female chick embryos at E16, which corresponds to the meiotic stage 25 . Therefore, DMRT1 may play an essential role in germ cell development even later than the embryonic stages we evaluated in this study.…”

Section: Discussionmentioning

confidence: 81%

“…It was observed that sex determination may occur earlier in females than in males and involve cell-autonomous and RA regulation aspects. A very recent study demonstrated the sex-differences between early embryonic PGCs (mix of E2.5 to E8.0) using transcriptome analysis 25 . However, this study did not demonstrate the timing and factors underlying sex determination.…”

Section: Discussionmentioning

confidence: 99%

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Prediction of sex-determination mechanisms in avian primordial germ cells using RNA-seq analysis

Ichikawa

Nakamura

Bono

et al. 2022

Sci Rep

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In birds, sex is determined through cell-autonomous mechanisms and various factors, such as the dosage of DMRT1. While the sex-determination mechanism in gonads is well known, the mechanism in germ cells remains unclear. In this study, we explored the gene expression profiles of male and female primordial germ cells (PGCs) during embryogenesis in chickens to predict the mechanism underlying sex determination. Male and female PGCs were isolated from blood and gonads with a purity > 96% using flow cytometry and analyzed using RNA-seq. Prior to settlement in the gonads, female circulating PGCs (cPGCs) obtained from blood displayed sex-biased expression. Gonadal PGCs (gPGCs) also exhibited sex-biased expression, and the number of female-biased genes detected was higher than that of male-biased genes. The female-biased genes in gPGCs were enriched in some metabolic processes. To reveal the mechanisms underlying the transcriptional regulation of female-biased genes in gPGCs, we performed stimulation tests. Retinoic acid stimulation of cultured gPGCs derived from male embryos resulted in the upregulation of several female-biased genes. Overall, our results suggest that sex determination in avian PGCs involves aspects of both cell-autonomous and somatic-cell regulation. Moreover, it appears that sex determination occurs earlier in females than in males.

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Section: Discussioncontrasting

confidence: 67%

Section: Discussionmentioning

confidence: 81%

Section: Discussionmentioning

confidence: 99%

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Prediction of sex-determination mechanisms in avian primordial germ cells using RNA-seq analysis

Ichikawa

Nakamura

Bono

et al. 2022

Sci Rep

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“…It was reported in chickens that the retinoic acid (RA) produced by the mesonephros promotes meiosis initiation in oocytes by triggering the expression of the pre-meiotic marker that is stimulated by retinoic acid 8 ( STRA8 ), as well as the subsequent expression of synaptonemal complex proteins (SYCPs), such as SYCP1 , SYCP2 , and SYCP3 [ 20 , 24 ]. The cells that entered into meiosis are arrested in meiotic prophase I as oocytes (termed primary oocytes) from E15.5, with the subsequent upregulation of meiotic prophase I markers, such as SPO11, initiator of meiotic double-stranded breaks ( SPO11 ); RAD21 cohesin complex component like 1 ( RAD21L1 ); and piwi like RNA-mediated gene silencing 1 ( PIWIL1 ) [ 20 , 21 , 25 ]. From E17, the chicken ovaries show a composite population of oocytes at different stages of meiotic prophase I, and the maximum amount of pachytene stage oocytes was, in a previous work, found around the time of hatching [ 26 ].…”

Section: Development Of Germ Cells Oocytes and Ovarian Follicles In C...mentioning

confidence: 99%

“…Studies elucidating the conservation of germ cell development between humans and chickens, which are a lower vertebrate, are very rare and disconnected [ 62 ]. In a recent paper, chicken germ cell dynamics were determined using single-cell RNA sequencing (scRNA-seq), and the development of chicken and human germ cells during embryogenesis was compared [ 25 ]. As a result of analyzing the chicken female germ cells from E2.5 to 1 week post-hatch, five stages (female stage 1 (fS1)—female stage 5 (fS5)) were defined for the chicken female germ cells on the basis of cluster-specific signature scores for the Kyoto encyclopedia of genes and genomes (KEGG) pathways [ 25 ].…”

Section: Transcriptome-based Conservation Of Female Germ Cell Develop...mentioning

confidence: 99%

Female Germ Cell Development in Chickens and Humans: The Chicken Oocyte Enriched Genes Convergent and Divergent with the Human Oocyte

Rengaraj

Han

2022

IJMS

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The development of germ cells and other physiological events in the differentiated ovary of humans are highly conserved with several mammalian species, except for the differences in timing. However, comparative knowledge on this topic is very scarce with respect to humans and lower vertebrates, such as chickens. In chickens, female germ cells enter into meiosis around embryonic day (E) 15.5 and are arrested in meiotic prophase I as primary oocytes. The oocytes arrested in meiosis I are accumulated in germ-cell cysts; shortly after hatching, they are enclosed by flattened granulosa cells in order to form primordial follicles. In humans, the process of meiotic recombination in female germ cells begins in the 10–11th week of gestation, and primordial follicles are formed at around week 20. In this review, we comprehensively elucidate both the conservation and the species-specific differences between chickens and humans with respect to germ cell, oocyte, and follicle development. Importantly, we provide functional insights into a set of chicken oocyte enriched genes (from E16 to 1 week post-hatch) that show convergent and divergent expression patterns with respect to the human oocyte (from week 11 to 26).

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Single‐cell transcriptome analysis of male chicken germ cells reveals changes in signaling pathway‐related gene expression profiles during mitotic arrest

et al. 2023

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Mitotic arrest is necessary for the embryonic development of germ cells, and thus, it is important to understand the signaling pathways that regulate mitotic arrest. Here, we investigated the signaling pathway dynamics of male embryonic chicken germ cells during mitotic arrest by single‐cell transcriptome analysis using germ‐cell tracing models. We identified signaling pathways that change at the transcriptional level during chicken male germ‐cell development after sex determination. We found that several components of the BMP, Notch, and JAK–STAT signaling pathways were downregulated at the mitotic‐arrest stage and were reactivated 1 week after hatching when all germ cells are quiescent after entering mitotic arrest. In addition, the transcriptional levels of components of the MAPK, Hedgehog, and thyroid‐hormone signaling pathways were steadily upregulated after mitotic arrest. This suggests the cooperation of multiple signaling pathways during entry into mitotic arrest and subsequent quiescence of chicken male germ cells.

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Dissecting chicken germ cell dynamics by combining a germ cell tracing transgenic chicken model with single-cell RNA sequencing

Cited by 16 publications

References 101 publications

Prediction of sex-determination mechanisms in avian primordial germ cells using RNA-seq analysis

Prediction of sex-determination mechanisms in avian primordial germ cells using RNA-seq analysis

Female Germ Cell Development in Chickens and Humans: The Chicken Oocyte Enriched Genes Convergent and Divergent with the Human Oocyte

Single‐cell transcriptome analysis of male chicken germ cells reveals changes in signaling pathway‐related gene expression profiles during mitotic arrest

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