Changes in granulosa cells gene expression associated with growth, plateau and atretic phases in medium bovine follicles

Douville, Gabriel; Sirard, Marc‐André

doi:10.1186/1757-2215-7-50

Cited by 61 publications

(46 citation statements)

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“…APP has been associated with mitochondrial dysfunction, which may compromise oocyte quality, fertilization, and development into viable offspring (26). Overexpression of MYC, in addition to causing ovarian cancer (30), affects follicle growth, oocyte quality, and embryo development (7,9). Decreased expression of PGR (progesterone receptor), known for its role in oocyte competence acquisition and ovulation (6), likely decreases oocyte quality.…”

Section: Discussionmentioning

confidence: 99%

Transcriptome meta-analysis of three follicular compartments and its correlation with ovarian follicle maturity and oocyte developmental competence in cows

Khan

Landry

Fournier

et al. 2016

Physiological Genomics

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Sirard MA. Transcriptome meta-analysis of three follicular compartments and its correlation with ovarian follicle maturity and oocyte developmental competence in cows. Physiol Genomics 48: 633-643, 2016. First published July 8, 2016 doi:10.1152/physiolgenomics.00050.2016.-Oocyte developmental competence in superstimulated cows is dependent in part on the duration of the FSH coasting. FSH coasting refers to superstimulation with FSH (2 days of endogenous FSH following follicle ablation and 3 days of FSH injections) followed by no FSH for a specific duration. The optimal duration varies among individuals. FSH coasting appears to modulate the transcriptome of different follicular compartments, which cooperate as a single functional unit. However, the integrative effects of FSH coasting on different follicular compartments remain ambiguous. Meta-analysis of three independent transcriptome studies, each focused on a single cell type (granulosa, cumulus, and oocyte) during FSH coasting, allowed the identification of 12 gene clusters with similar time-course expression patterns in all three compartments. Network analysis identified HNF4A (involved in metabolic functions) and ELAVL1 (an RNA-binding protein) as hub genes regulated respectively upward and downward in the clusters enriched at the optimal coasting time, and APP (involved in mitochondrial functions) and COPS5 (a member of the COP9 signalosome) as hub genes regulated respectively upwards and downwards in the clusters enriched progressively throughout the coasting period. We confirmed the effects on HNF4A downstream targets (TTR, PPL) and other hub genes (ELAVL1, APP, MYC, and PGR) in 30 cows with RT-quantitative PCR. The correlation of hub gene expression levels with FSH coasting indicated that a combination of these genes could predict oocyte competence with 83% sensitivity, suggesting that they are potential biomarkers of follicle differentiation. These findings could be used to optimize FSH coasting on an individual basis. ovarian follicle; oocyte competence; transcriptomics; meta-analysis; FSH coasting ASSISTED REPRODUCTIVE TECHNOLOGIES have been used successfully in a wide range of research and clinical applications. However, the success rate remains low, despite increasing research efforts (19). Better understanding of ovarian physiology and of the acquisition of oocyte developmental competence in particular is needed to improve the efficiency of fertility treatments in the clinical setting and in livestock production.

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Section: Discussionmentioning

confidence: 99%

Transcriptome meta-analysis of three follicular compartments and its correlation with ovarian follicle maturity and oocyte developmental competence in cows

Khan

Landry

Fournier

et al. 2016

Physiological Genomics

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“…Previous study on the transcriptomic profiles of granulosa cells revealed several genes linked to follicular development before establishment of dominance, and provided tools to classify medium-sized (6-9 mm) follicles in different growing phases [19]. …”

Section: Introductionmentioning

confidence: 99%

Global gene expression in granulosa cells of growing, plateau and atretic dominant follicles in cattle

Girard

Dufort

Douville

et al. 2015

Reprod Biol Endocrinol

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BackgroundThe physiological state of the dominant follicle is important as it may be linked to the competence of the oocyte within. The objective of this study was to analyze, by transcriptomic analysis, the changes occurring in granulosa cells from dominant follicles at different phases of follicular growth.MethodsGranulosa cells were collected from slaughterhouse dairy cattle follicles with a diameter greater than 9 mm, and were classified at different phases of follicle growth based on flow cytometry profiles of DNA content after staining with propidium iodide. Three phases were identified based on the proportion of cells in -G1 (less than 2n DNA), G0-G1 (2n DNA) or S-M (more than 2n DNA) and follicles were thus allocated to the growing, plateau or atresia group. Between group analysis (BGA) showed clear segregation of the three groups, and the groups were contrasted against each other in a loop design to identify differently expressed genes. Ingenuity Pathway Analysis (IPA) was used to identify the functions and upstream regulators associated with the observed differently expressed genes.ResultsMajor differences were observed between the growth phases. Granulosa cells from follicles in the plateau phase had increased expression of TYRO3 and downregulation of JAM2 compared to growing follicles, supporting the idea of a shift from proliferation to differentiation. On the other hand, genes regulating the response to oxidative stress (VNN1) and angiogenesis (ANGPT2) were upregulated in granulosa cells from atretic follicles. While the predicted activated functions in cells at the plateau stage compared to cells at the growing stage included synthesis and transport of molecules, the predictions for atretic follicles relative to plateau ones included an increase in apoptosis and cell death.ConclusionConsistent with previous studies, these observations allowed us to match the presence of specific gene transcripts to a particular physiological status and consequently to classify follicles. The results also demonstrated that the plateau phase is not a simple ‘in between’ status between growth and atresia, as several characteristics are unique to this stage.Electronic supplementary materialThe online version of this article (doi:10.1186/s12958-015-0010-7) contains supplementary material, which is available to authorized users.

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“…The gene expression in bovine granulosa cells collected from three different phases of follicle development was examined previously, and TP53 and SP1 were shown to be the main upstream factors between the growth and plateau phases [12]. In the comparison of oocytes with expanded cumulus cells and those with compact cumulus cells, expression of STAT3 was detected in oocytes associated with high developmental competence [13].…”

Section: Discussionmentioning

confidence: 99%

Gene expression patterns in granulosa cells and oocytes at various stages of follicle development as well as in <i>in vitro</i> grown oocyte-and-granulosa cell complexes

Munakata

Kawahara-Miki

Shiratsuki

et al. 2016

Journal of Reproduction and Development

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Follicle development is accompanied by proliferation of granulosa cells and increasing oocyte size. To obtain high-quality oocytes in vitro, it is important to understand the processes that occur in oocytes and granulosa cells during follicle development and the differences between in vivo and in vitro follicle development. In the present study, oocytes and granulosa cells were collected from early antral follicles (EAFs, 0.5–0.7 mm in diameter), small antral follicles (SAFs, 1–3 mm in diameter), large antral follicles (LAFs, 3–7 mm in diameter), and in vitro grown oocyte-and-granulosa cell complexes (OGCs), which were cultured for 14 days after collection from EAFs. Gene expression was analyzed comprehensively using the next-generation sequencing technology. We found top upstream regulators during the in vivo follicle development and compared them with those in in vitro developed OGCs. The comparison revealed that HIF1 is among the top regulators during both in vivo and in vitro development of OGCs. In addition, we found that HIF1-mediated upregulation of glycolysis in granulosa cells is important for the growth of OGCs, but the cellular metabolism differs between in vitro and in vivo grown OGCs. Furthermore, on the basis of comparison of upstream regulators between in vivo and in vitro development of OGCs, we believe that low expression levels of FLT1 (VEGFA receptor), SPP1, and PCSK6 can be considered causal factors of the suboptimal development under in vitro culture conditions.

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Changes in granulosa cells gene expression associated with growth, plateau and atretic phases in medium bovine follicles

Cited by 61 publications

References 72 publications

Transcriptome meta-analysis of three follicular compartments and its correlation with ovarian follicle maturity and oocyte developmental competence in cows

Transcriptome meta-analysis of three follicular compartments and its correlation with ovarian follicle maturity and oocyte developmental competence in cows

Global gene expression in granulosa cells of growing, plateau and atretic dominant follicles in cattle

Gene expression patterns in granulosa cells and oocytes at various stages of follicle development as well as in <i>in vitro</i> grown oocyte-and-granulosa cell complexes

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