Temporal Transcriptional Profiling of Somatic and Germ Cells Reveals Biased Lineage Priming of Sexual Fate in the Fetal Mouse Gonad

Samantha A. Jameson, Anirudh Natarajan, Jonah Cool, Tony DeFalco, Danielle M. Maatouk, Lindsey Mork, Steven C. Munger, Blanche Capel

PLoS Genetics · 2012 · 296 citations · 154 references

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TL;DR

The divergence of distinct cell populations from multipotent progenitors is poorly understood in vivo, and the gonad serves as an ideal model because it originates as a bipotential primordium that differentiates into testis or ovary. The study aimed to dissect gonadal differentiation by profiling sorted XX and XY gonadal cells at three developmental stages using microarrays. Microarray analysis was performed on sorted supporting, interstitial/stromal, germ, and endothelial cells from XX and XY gonads at three time points. The analysis revealed lineage‑specific gene expression changes, demonstrated that undifferentiated germ and supporting cell progenitors are primed toward male and female fates respectively, and provided a molecular framework reconciling female‑default and balanced sex‑determination models while offering new insights into organ‑wide fate adoption.

Abstract

The divergence of distinct cell populations from multipotent progenitors is poorly understood, particularly in vivo. The gonad is an ideal place to study this process, because it originates as a bipotential primordium where multiple distinct lineages acquire sex-specific fates as the organ differentiates as a testis or an ovary. To gain a more detailed understanding of the process of gonadal differentiation at the level of the individual cell populations, we conducted microarrays on sorted cells from XX and XY mouse gonads at three time points spanning the period when the gonadal cells transition from sexually undifferentiated progenitors to their respective sex-specific fates. We analyzed supporting cells, interstitial/stromal cells, germ cells, and endothelial cells. This work identified genes specifically depleted and enriched in each lineage as it underwent sex-specific differentiation. We determined that the sexually undifferentiated germ cell and supporting cell progenitors showed lineage priming. We found that germ cell progenitors were primed with a bias toward the male fate. In contrast, supporting cells were primed with a female bias, indicative of the robust repression program involved in the commitment to XY supporting cell fate. This study provides a molecular explanation reconciling the female default and balanced models of sex determination and represents a rich resource for the field. More importantly, it yields new insights into the mechanisms by which different cell types in a single organ adopt their respective fates.

References

154