Abstract
BackgroundThe successful achievement of early ovarian folliculogenesis is important for fertility and reproductive life span. This complex biological process requires the appropriate expression of numerous genes at each developmental stage, in each follicular compartment. Relatively little is known at present about the molecular mechanisms that drive this process, and most gene expression studies have been performed in rodents and without considering the different follicular compartments.ResultsWe used RNA-seq technology to explore the sheep transcriptome during early ovarian follicular development in the two main compartments: oocytes and granulosa cells. We documented the differential expression of 3,015 genes during this phase and described the gene expression dynamic specific to these compartments. We showed that important steps occurred during primary/secondary transition in sheep. We also described the in vivo molecular course of a number of pathways. In oocytes, these pathways documented the chronology of the acquisition of meiotic competence, migration and cellular organization, while in granulosa cells they concerned adhesion, the formation of cytoplasmic projections and steroid synthesis. This study proposes the involvement in this process of several members of the integrin and BMP families. The expression of genes such as Kruppel-like factor 9 (KLF9) and BMP binding endothelial regulator (BMPER) was highlighted for the first time during early follicular development, and their proteins were also predicted to be involved in gene regulation. Finally, we selected a data set of 24 biomarkers that enabled the discrimination of early follicular stages and thus offer a molecular signature of early follicular growth. This set of biomarkers includes known genes such as SPO11 meiotic protein covalently bound to DSB (SPO11), bone morphogenetic protein 15 (BMP15) and WEE1 homolog 2 (S. pombe)(WEE2) which play critical roles in follicular development but other biomarkers are also likely to play significant roles in this process.ConclusionsTo our knowledge, this is the first in vivo spatio-temporal exploration of transcriptomes derived from early follicles in sheep.
Highlights
In large mammalian species at birth, the ovaries contain a large and fixed reserve of non-growing primordial follicles
The expression of genes such as Kruppel-like factor 9 (KLF9) and BMP binding endothelial regulator (BMPER) was highlighted for the first time during early follicular development, and their proteins were predicted to be involved in gene regulation
We investigated the 3,015 differential expression genes (DEG) (S2 Table) in order to clarify the dynamics of transcription during early development and we observed more marked changes in gene expression in oocytes than in granulosa cells (2173/1192)
Summary
In large mammalian species at birth, the ovaries contain a large and fixed reserve of non-growing primordial follicles (oocytes surrounded by flattened pre-granulosa cells). The gradual exit of primordial follicles starts shortly after formation of the primordial follicle pool and continues throughout the reproductive years [1] This early follicular development is important as it regulates the size of the remaining stock of primordial follicles and their fate, which in turn affects fertility and the reproductive life span. Follicular development requires the appropriate expression of numerous genes at different developmental stages and orchestrated communication between the two main compartments (oocytes and granulosa cells) [3, 4]. The successful achievement of early ovarian folliculogenesis is important for fertility and reproductive life span This complex biological process requires the appropriate expression of numerous genes at each developmental stage, in each follicular compartment. Little is known at present about the molecular mechanisms that drive this process, and most gene expression studies have been performed in rodents and without considering the different follicular compartments
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