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The Fetal and Infant Human Testis Cell Atlas via Single-cell RNA-seq

ABSTRACT: Human testis development in prenatal life involves complex changes in germline and somatic cell identity. To better understand, we profiled and analyzed ~32,500 single-cell transcriptomes of testicular cells from embryonic, fetal and infant stages. Our data shows that at 6-7 weeks post-fertilization as the testicular cords are established, the Sertoli and interstitial cells originate from a common heterogeneous progenitor pool, which then resolves into fetal Sertoli cells (expressing tube-forming genes) or interstitial cells (including Leydig-lineage cells expressing steroidogenesis genes). Almost ten weeks later, beginning at 15-16 weeks post-fertilization, the male primordial germ cells exit mitosis, downregulate pluripotent transcription factors and transition into cells that strongly resemble the ‘State 0’ spermatogonia originally defined in the infant and adult testes. Therefore, we termed these fetal spermatogonia ‘State f0’. Taken together, we reveal multiple insights into the coordinated and temporal development of the embryonic, fetal and postnatal male germline together with the somatic niche.

ORGANISM(S): Homo sapiens

PROVIDER: GSE161617 | GEO | 2021/01/18

REPOSITORIES: GEO

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Project description:The piRNA pathway is studied in great detail in Drosophila female germline. In this study we show that unlike the female germline where all Piwi proteins are expressed throughout oogenesis, Ago3 - a Piwi family protein shows a spatial expression male germline. To understand dynamics of piRNA pathway during spermatogonia and primary spermatocyte stages of male germline development, we used arrest mutants. The bag of marbles (bam) and benign gonial cell neoplasm (bgcn) mutants have only early mitotic dividing germline cells in the testes due to failure to progress to primary spermatocyte stage, the cannonball (can) and spermatocyte arrest (sa) mutant germline cells cannot progress beyond primary spermatocyte stage. To investigate the dynamics of the piRNA pathway during spermatogenesis in spermatogonia and primary spermatocyte stages, we used testicular tissues from these stage-specific arrested mutants. While we used entire bam and bgcn mutant testes for spermatogonia purification, we while we manually removed the apical regions of can and sa mutant testes to exclude mitotically dividing undifferentiated germline cells for primary spermatocytes purification. Our results show that piRNAs mapping to transposons are more abundant in spermatogonia, whereas those mapping to Suppressor of Stellate [Su(Ste)] and AT-chX are mostly expressed in primary spermatocytes. Furthermore we observed that transposon-mapping piRNAs with ping-pong signature are more abundant in spermatogonia albeit still detectable in primary spermatocytes where Ago3 is not expressed. These results suggest that robust piRNA production via ping-pong cycle takes place in spermatogonia, and to a lesser extent in primary spermatocytes even in the absence of Ago3. Consistently, piRNAs from ago3 mutant testes also exhibit the ping-pong signature, confirming that a non-canonical ping-pong cycle is acting during spermatogenesis. Our study provides a developmental dimension to the piRNA pathway and uncovers a new mechanism used in the male germline to silence transposons. The difference in piRNA from spermatogonia and primary spermatocyte stages was studied by comparing small RNAs from bam and bgcn mutant testis, which represent spermatogonia stages with the small RNAs from apex removed can and sa testis, representing primary spermatocyte stages. In the study we also studied effect of loss of Piwi family proteins Aub and Ago3, which have different spatial expression during male germline development.

Dataset Information

The Fetal and Infant Human Testis Cell Atlas via Single-cell RNA-seq

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