Abstract
Movement and expansion of mesonephric-derived stroma appears to be very important in the development of the ovary. Here, we examined the expression of 24 genes associated with stroma in fetal ovaries during gestation (n = 17; days 58–274) from Bos taurus cattle. RNA was isolated from ovaries for quantitative RT-PCR. Expression of the majority of genes in TGFβ signalling, stromal transcription factors (NR2F2, AR), and some stromal matrix genes (COL1A1, COL3A1 and FBN1, but not FBN3) showed a positive linear increase with gestational age. Expression of genes associated with follicles (INSL3, CYP17A1, CYP11A1 and HSD3B1), was low until mid-gestation and then increased with gestational age. LHCGR showed an unusual bimodal pattern; high levels in the first and last trimesters. RARRES1 and IGFBP3 also increased with gestational age. To relate changes in gene expression in stromal cells with that in non stromal cells during development of the ovary we combined the data on the stromal genes with another 20 genes from non stromal cells published previously and then performed hierarchical clustering analysis. Three major clusters were identified. Cluster 1 genes (GATA4, FBN3, LHCGR, CYP19A1, ESR2, OCT4, DSG2, TGFB1, CCND2, LGR5, NR5A1) were characterised by high expression only in the first trimester. Cluster 2 genes (FSHR, INSL3, HSD3B1, CYP11A1, CYP17A1, AMH, IGFBP3, INHBA) were highly expressed in the third trimester and largely associated with follicle function. Cluster 3 (COL1A1, COL3A1, FBN1, TGFB2 TGFB3, TGFBR2, TGFBR3, LTBP2, LTBP3, LTBP4, TGFB1I1, ALDH1A1, AR, ESR1, NR2F2) had much low expression in the first trimester rising in the second trimester and remaining at that level during the third trimester. Cluster 3 contained members of two pathways, androgen and TGFβ signalling, including a common member of both pathways namely the androgen receptor cofactor TGFβ1 induced transcript 1 protein (TGFB1I1; hic5). GATA4, FBN3 and LHCGR, were highly correlated with each other and were expressed highly in the first trimester during stromal expansion before follicle formation, suggesting that this could be a critical phase in the development of the ovarian stroma.
Highlights
The mammalian ovary undergoes many different cell processes during its development [1]
The oogonia and oocytes arise from primordial germ cells (PGC) that migrate from as far away as the yolk sac into the mesonephros from where they are incorporated into the gonadal ridge [2]
The majority of genes involved in TGFβ signalling (Fig 1 and S1 Fig) increased throughout fetal ovarian development and showed a positive linear responses with gestational age, apart from TGFB1 (Fig 1A and S1A Fig), TGFBR1 (Fig 1D and S1D Fig) and LTBP1 (Fig 1G and S1G Fig)
Summary
The mammalian ovary undergoes many different cell processes during its development [1]. The somatic granulosa cells of follicles and the surface epithelial cells, except at the base of the ovary, are derived from a common precursor, the gonadal ridge-epithelial-like (GREL) cell. This precursor cell very likely originates from the surface epithelial cells of the mesonephros and replicates to form the gonadal ridge. The oogonia and oocytes arise from primordial germ cells (PGC) that migrate from as far away as the yolk sac into the mesonephros from where they are incorporated into the gonadal ridge [2] During their migration, the PGCs start to proliferate—a process which is continued after colonising the gonad. The germ cells firstly replicate (oogonia), subsequently enter meiosis and arrest in the dictyate stage of prophase I (oocytes) until ovulation
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