Complete male-to-female sex reversal in XY mice lacking the miR-17∼92 cluster
Posted on: 7 May 2023 , updated on: 10 May 2023
Preprint posted on 23 March 2023
Small but mighty! miRNA cluster miR-17-92 knock out results in complete testis to ovary sex reversal
Selected by Martin EstermannCategories: bioinformatics, cell biology, developmental biology, genetics, molecular biology
Background:
During embryogenesis, the mammalian bipotential gonads differentiate into ovaries in XX females and testis in XY males. The supporting cell lineage is the first to sexually differentiate into their ovarian (pre-granulosa) or testicular (Sertoli) fates. Once these cells are committed, they regulate the differentiation of the rest of the gonadal cells. In XY males, the expression of the Y-linked gene Sry is required to activate the testicular differentiation program, including Sox9. Sox9 then will cooperate with Fgf9 to achieve Sertoli cell differentiation, while inhibiting the expression of pre-granulosa differentiation genes. In XX females, in the absence of Sry, the gonads upregulate Foxl2, initiating the differentiation towards the pre-granulosa fate and inhibiting Sertoli cell genes.
In mouse, the activation of Sry occurs in a precise and narrow time window (Embryonic day 11.0 to 11.25). A delay in Sry expression (6 hours) results in the improper activation of Sox9. As a result, these gonads will differentiate into ovaries as the pre-granulosa cell program is not repressed.
Most of the research in the field of gonadal sex determination has focused on the coding genome, whereas the non-coding regions remain unexplored. In this preprint, the researchers evaluated the role of the microRNA (miRNA) cluster miR-17-92 in gonadal sex determination. miRNAs are small non-coding RNA molecules (21-23 nucleotides) that bind to complementary regions of mRNAs, targeting them for degradation and inhibiting their expression. The miR-17-92 cluster contains six miRNA genes (miR-17, miR-18a, miR-19a, miR-20a, miR-19b-1 and miR-92a-1) and is known to be involved in several developmental processes. In this research, the authors knocked out (KO) this cluster in mice, resulting in a complete male to female sex reversal: ovarian differentiation in XY males.
Key findings:
1) miR-17-92 KO causes ovarian development and FOXL2 expression.
The authors evaluated gonadal development and supporting cell differentiation in knockout mice for the miR-17-92 cluster. As can be seen in Figure 1, control male gonads showed normal expression of SOX9 in the testicular cords, and specifically in the Sertoli cells. In female controls, FOXL2 expression was detected in the pre-granulosa cells, as expected. Surprisingly, XY gonads lacking the miRNA cluster developed ovaries, having FOXL2 positive pre-granulosa cells instead of SOX9 positive Sertoli cells. This indicates that by E17.5 there was a complete male to female sex reversal in the XY knockouts.
Figure 1. Immunofluorescence for Sertoli (SOX9, red) and pre-granulosa (FOXL2, green) cell markers in E17.5 XY and XX, wild type or miR-17-92 cluster KO gonads.
2) miR-17-92 KO results in delayed SRY expression and SOX9 activation.
To gain insight into the mechanism behind the sex reversal in the XY knockout gonads, SRY and SOX9 immunofluorescence was performed during the process of sex determination (E11.0 to E12.5). As shown in Figure 2A, there was a delay in SRY expression in the knockout compared with the control. This delay prevented the activation of SOX9 and therefore the commitment into the Sertoli fate (Figure 2B), resulting in pre-granulosa cell differentiation.
Figure 2. Immunofluorescence for SRY (A, red) and SOX9 (B, green) in control or miR-17-92 KO XY differentiating gonads, from E11.0 to E12.5.
3) Removal of miRNA binding site in Foxl2 UTR does not alter gonadal development.
As miRNAs have been reported to inhibit gene expression, the authors wanted to evaluate how these miRNAs regulate sex differentiation. Since Foxl2 carries a miR-17 binding site in its 3’ untranslated region (UTR) and FOXL2 was upregulated in the XY knockout gonads, the authors deleted this binding site to evaluate if the miRNAs are inhibiting FOXL2 activation in male gonads. Unfortunately, the loss of the binding site was not sufficient to induce FOXL2 expression in E12.5 XY gonads, suggesting an indirect effect or the involvement of other factors.
Why I chose this preprint:
This study is the first to report miRNAs associated with a complete sex reversal in mammals. This manuscript is a great example of the importance of the non-coding genome in the regulation of sex determination. In addition, complete male to female sex reversals is rare in the literature with ovotestis development or gonadal agenesis being the most prominent phenotypes. This makes the results described in this preprint even more fascinating.
Future directions / questions for the authors:
- What controls the expression of these mRNAs? Are they sexually dimorphic?
- Do you think that all the miRNAs in from clusters are important for sex determination? Or do you think that one miRNA is regulating this process?
- Are you planning to evaluate the effect of single miRNA knockout on the differentiation process?
doi: https://doi.org/10.1242/prelights.34595
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