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Spatio-Temporal Gene Expression Profiling during In Vivo Early Ovarian Folliculogenesis: Integrated Transcriptomic Study and Molecular Signature of Early Follicular Growth.

Bonnet A, Servin B, Mulsant P, Mandon-Pepin B - PLoS ONE (2015)

Bottom Line: 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.To our knowledge, this is the first in vivo spatio-temporal exploration of transcriptomes derived from early follicles in sheep.

View Article: PubMed Central - PubMed

Affiliation: INRA, UMR 1388 GenPhySE (Génétique, Physiologie et Systèmes d'Elevage), F-31326 Castanet-Tolosan, France.

ABSTRACT

Background: 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. 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.

Results: We 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.

Conclusions: To our knowledge, this is the first in vivo spatio-temporal exploration of transcriptomes derived from early follicles in sheep.

No MeSH data available.


Related in: MedlinePlus

Dynamic representation of gene expression involved in steroid biosynthesis process.Significant differences in relative gene expression during early folliculogenesis of genes involved in steroid synthesis (S2 Table). *: FDR <0.05, pairwise comparison pval <0.01.
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pone.0141482.g007: Dynamic representation of gene expression involved in steroid biosynthesis process.Significant differences in relative gene expression during early folliculogenesis of genes involved in steroid synthesis (S2 Table). *: FDR <0.05, pairwise comparison pval <0.01.

Mentions: At the end of early follicular development, granulosa cells may be capable of producing steroids. Pig preantral follicles produced hormones such as estradiol and progesterone [41] that originate from cholesterol and are required for the development and maturation of follicles [42]. We demonstrated a gradual increase during follicular development in the expression of genes already known to participate in lipid and steroid biosynthesis (Fig 3). At the small antral stage granulosa cells over-expressed the stearoyl-CoA desaturase (SCD) gene that is involved in lipid metabolism which had previously been observed as being weakly expressed in rat primordial follicles and mainly expressed in granulosa cells of antral follicles [43]. Other differential genes concerned steroid synthesis such as steroid-5-alpha-reductase, alpha polypeptide 1 (SRD5A1), hydroxy-delta-5-steroid dehydrogenase, 3 beta- and steroid delta-isomerase 1 (HSD3β) and hydroxysteroid (17-beta) dehydrogenase (HSD17β) and steroid regulation such as the nuclear receptor subfamily 5, group A, member 2 (NR5A2) [44] and luteinizing hormone/choriogonadotropin receptor (LHCGR). In line with these changes, IPA predicted an increase in the steroid biosynthesis process (S5 Table). Gene expression profiles are summarized in Fig 7.


Spatio-Temporal Gene Expression Profiling during In Vivo Early Ovarian Folliculogenesis: Integrated Transcriptomic Study and Molecular Signature of Early Follicular Growth.

Bonnet A, Servin B, Mulsant P, Mandon-Pepin B - PLoS ONE (2015)

Dynamic representation of gene expression involved in steroid biosynthesis process.Significant differences in relative gene expression during early folliculogenesis of genes involved in steroid synthesis (S2 Table). *: FDR <0.05, pairwise comparison pval <0.01.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4634757&req=5

pone.0141482.g007: Dynamic representation of gene expression involved in steroid biosynthesis process.Significant differences in relative gene expression during early folliculogenesis of genes involved in steroid synthesis (S2 Table). *: FDR <0.05, pairwise comparison pval <0.01.
Mentions: At the end of early follicular development, granulosa cells may be capable of producing steroids. Pig preantral follicles produced hormones such as estradiol and progesterone [41] that originate from cholesterol and are required for the development and maturation of follicles [42]. We demonstrated a gradual increase during follicular development in the expression of genes already known to participate in lipid and steroid biosynthesis (Fig 3). At the small antral stage granulosa cells over-expressed the stearoyl-CoA desaturase (SCD) gene that is involved in lipid metabolism which had previously been observed as being weakly expressed in rat primordial follicles and mainly expressed in granulosa cells of antral follicles [43]. Other differential genes concerned steroid synthesis such as steroid-5-alpha-reductase, alpha polypeptide 1 (SRD5A1), hydroxy-delta-5-steroid dehydrogenase, 3 beta- and steroid delta-isomerase 1 (HSD3β) and hydroxysteroid (17-beta) dehydrogenase (HSD17β) and steroid regulation such as the nuclear receptor subfamily 5, group A, member 2 (NR5A2) [44] and luteinizing hormone/choriogonadotropin receptor (LHCGR). In line with these changes, IPA predicted an increase in the steroid biosynthesis process (S5 Table). Gene expression profiles are summarized in Fig 7.

Bottom Line: 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.To our knowledge, this is the first in vivo spatio-temporal exploration of transcriptomes derived from early follicles in sheep.

View Article: PubMed Central - PubMed

Affiliation: INRA, UMR 1388 GenPhySE (Génétique, Physiologie et Systèmes d'Elevage), F-31326 Castanet-Tolosan, France.

ABSTRACT

Background: 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. 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.

Results: We 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.

Conclusions: To our knowledge, this is the first in vivo spatio-temporal exploration of transcriptomes derived from early follicles in sheep.

No MeSH data available.


Related in: MedlinePlus