The WNT/β-catenin signaling pathway and expression of survival promoting genes in luteinized granulosa cells: endometriosis as a paradigm for a dysregulated apoptosis pathway

Sánchez, Ana M.; Viganò, Paola; Quattrone, Federica; Pagliardini, Luca; Papaleo, Enrico; Candiani, Massimo; Panina-Bordignon, Paola

doi:10.1016/j.fertnstert.2014.02.040

Cited by 50 publications

(32 citation statements)

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“…On the other hand, the activation of the same molecule was proposed as an upstream regulator of the transition from plateau to atretic follicles. This view is supported by data from Sanchez et al who suggested that beta-catenin, which is closely related to alpha catenin, is involved in granulosa cell atresia [53]. The shift observed in the action of genes regulated by alpha catenin as follicles go from growing to plateau and from plateau to atresia (Figure 4C and D) suggests that this molecule acts as an initiator of some of the changes occurring during folliculogenesis.…”

Section: Discussionsupporting

confidence: 61%

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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Section: Discussionsupporting

confidence: 61%

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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“…Our PCR survey failed to detect WNT4 mRNA in bovine granulosa cells, which is in agreement with a study in human cumulus cells (Wang et al, 2009) but in contrast to studies with human luteinized granulosa cells and rodent ovaries (Hsieh et al, 2002;Sanchez et al, 2014). We also failed to detect significant quantities of WNT2 mRNA, unlike previous studies in bovine and rodent granulosa cells (Castañon et al, 2012;Ricken et al, 2002).…”

Section: Discussionsupporting

confidence: 88%

“…Messenger RNA encoding WNT5A has previously been detected in human granulosa cells (Sanchez et al, 2014), and we could readily detect mRNA and protein in bovine granulosa cells. Abundance of WNT5A mRNA was regulated by FSH, whereas WNT2B and WNT5B mRNA levels were not, which points to a specific regulation of WNT5A in the ovary.…”

Section: Discussionmentioning

confidence: 81%

“…Previous reports have demonstrated that treatment with WNT5A decreases total CTNNB protein levels and/or CTNNB1 signaling in luteinized human granulosa cells as well as other cell types (Pourreyron et al, 2012;Sanchez et al, 2014;Sato et al, 2009;Topol et al, 2003). Several mechanisms have been proposed to explain how non-canonical WNTs may antagonize the canonical pathway, including direct competition with canonical WNTs for binding to FZD receptor complexes (Bryja et al, 2009), increasing the expression of SIAH ubiquitin ligase and accelerating ubiquitination and degradation of CTNNB1 (Topol et al, 2003), and inhibiting coactivator recruitment to the promoters of target genes via a protein kinase C pathway (Lee et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

“…In humans, WNT2 but not WNT4 mRNA was detected in cumulus cells (Wang et al, 2009), whereas WNT4 and WNT5A transcripts have recently been reported in luteinized granulosa cells (Sanchez et al, 2014). In luteinized bovine granulosa cells, WNT2 mRNA was detected and upregulated by FSH (Castañon et al, 2012), and CTNNB1 has been shown to act downstream of LH to regulate STAR expression and progesterone synthesis (Roy et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Non-canonical WNT5A is a potential regulator of granulosa cell function in cattle

Abedini

Zamberlam

Boerboom

et al. 2015

Molecular and Cellular Endocrinology

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Clinical correlation of apoptosis in human granulosa cells—A review

Almeida

Ferreira

Silveira

et al. 2018

Cell Biology International

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The quality of oocytes depends on interactions with surrounding granulosa cells. Granulosa cells are essential in normal follicular maturation process since they produce steroidal hormones and growth factors, and they play a crucial role in follicular atresia. The success in reproductive biology and medicine depends on reliable assessment of oocyte and embryo viability which presently mainly bases on oocyte and embryo morphology. Recent investigations have tried to establish an evaluation system for oocyte quality and to predict outcome of in vitro fertilization (IVF) based on the incidence of granulosa cells and cumulus cells apoptosis. Apoptosis of granulosa cells seems to have a negative effect on conception and pregnancy rates in IFV programs. Thus, in this review we present a brief outline of clinical correlation of apoptosis in human granulosa cells and cumulus cells, and its influence upon oocyte quality and IFV outcome. Taken together, understanding the influence of granulosa cell apoptosis on oocyte quality and maturity as well as on embryo health may ultimately allow scientists and clinicians to harness better protocols of ovarian stimulation for infertility treatments.

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The WNT/β-catenin signaling pathway and expression of survival promoting genes in luteinized granulosa cells: endometriosis as a paradigm for a dysregulated apoptosis pathway

Cited by 50 publications

References 33 publications

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

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

Non-canonical WNT5A is a potential regulator of granulosa cell function in cattle

Clinical correlation of apoptosis in human granulosa cells—A review

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