Response of follicle cells to ovulatory stimuli within the follicle and in primary culture

Motola, S.; Popliker, Malka; Tsafriri, A.

doi:10.1016/j.mce.2007.11.002

Cited by 9 publications

(8 citation statements)

References 21 publications

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“…This study also examined the effect of amphiregulin and epiregulin supplementation during IVM on oocyte developmental competence, and our results have shown that epiregulin increases blastocyst formation and quality and thereby improves oocyte developmental competence. LH-induced EGF-like peptide signalling in mural granulosa and cumulus cells is a critical event that occurs in the pre-ovulatory follicles of mammalian species, thus far confirmed in rodent, pig, cow, horse, macaque, and human (Ashkenazi et al 2005;Ben-Ami et al 2006;Freimann et al 2004;Motola et al 2008;Park et al 2004;Sekiguchi et al 2004;Shimada et al 2006;Zamah et al 2010). The autocrine and paracrine expression of EGF-like peptides in both these somatic cell types plays a fundamental role in oocyte maturation, cumulus matrix expansion and ovulation (Conti et al 2012).…”

Section: Discussionmentioning

confidence: 90%

“…Studies have demonstrated that epidermal growth factor (EGF)-like peptides are important propagators of the LH signal. LH induces fast and transient upregulation in expression of three members of the EGF growth factor family: amphiregulin (AREG); epiregulin (EREG); and betacellulin (BTC) in the mural granulosa cells and cumulus cells (CCs) of several animal species as well as human (Ashkenazi et al 2005;Ben-Ami et al 2006;Freimann et al 2004;Motola et al 2008;Park et al 2004;Sekiguchi et al 2004;Shimada et al 2006;Zamah et al 2010). The importance of EGF-like peptides in the propagation of the LH signal in vivo was revealed when mice null for Areg or Ereg exhibited compromised oocyte meiotic resumption, cumulus matrix expansion and ovulation; mice null for one EGF-like peptide generally only exhibit a mild phenotype, which is believed to be due to a compensatory mechanism by the other EGF-like peptides (Hsieh et al 2007).…”

Section: Introductionmentioning

confidence: 99%

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Mode of oocyte maturation affects EGF-like peptide function and oocyte competence

Richani

Ritter

Thompson

et al. 2013

Molecular Human Reproduction

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The function and impact of epidermal growth factor (EGF)-like peptide signalling during ovulation and in vivo oocyte maturation (IVV) has been recently characterized, however, little is currently known about the effect of oocyte in vitro maturation (IVM) on this pathway. The aim of this study was to examine expression and functional aspects of three EGF-like peptides (amphiregulin, epiregulin and betacellulin) and their common receptor (EGFR) in cumulus cells during mouse oocyte IVM compared with IVV. Cumulus-oocyte complexes (COCs) were collected from prepubertal mice either 46 h post-eCG (IVM) or 46 h post-eCG plus 0.5-12 h post-hCG (IVV). Time course experiments showed mRNA expression of all three EGF-like peptides and amphiregulin protein in IVM media were significantly lower for the majority of FSH-supplemented IVM compared with IVV. The supplementation of EGF during IVM yielded EGF-like peptide expression levels comparable with IVV and amphiregulin/epiregulin supplemented IVM. However, despite this, EGF activation of the COC EGFR remained significantly lower at 3 and 6 h of IVM than in vivo, and levels were similar to those observed during FSH-supplemented IVM. The addition of exogenous epiregulin during IVM significantly increased blastocyst rates, and epiregulin and amphiregulin improved blastocyst quality, compared with FSH or EGF. In conclusion, findings from this study suggest that the widely used IVM additives, FSH and EGF, are inadequate propagators of the essential EGF-like peptide signalling cascade. In contrast, the use of epiregulin and/or amphiregulin during IVM leads to improved oocyte developmental competence and therefore may be preferable IVM additives than FSH or EGF.

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Section: Discussionmentioning

confidence: 90%

Section: Introductionmentioning

confidence: 99%

Mode of oocyte maturation affects EGF-like peptide function and oocyte competence

Richani

Ritter

Thompson

et al. 2013

Molecular Human Reproduction

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“…The EGF-like factors AREG , EREG and NRG1 are well known target genes of hLH/hCG action [66], [81], [82]. These molecules may play a role in the ovulatory process and oocyte maturation [66], [83] exerted via both ERK- and AKT-pathways activation [22],[71].…”

Section: Discussionmentioning

confidence: 99%

LH and hCG Action on the Same Receptor Results in Quantitatively and Qualitatively Different Intracellular Signalling

et al. 2012

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Human luteinizing hormone (hLH) and chorionic gonadotropin (hCG) act on the same receptor (LHCGR) but it is not known whether they elicit the same cellular and molecular response. This study compares for the first time the activation of cell-signalling pathways and gene expression in response to hLH and hCG. Using recombinant hLH and recombinant hCG we evaluated the kinetics of cAMP production in COS-7 and hGL5 cells permanently expressing LHCGR (COS-7/LHCGR, hGL5/LHCGR), as well as cAMP, ERK1/2, AKT activation and progesterone production in primary human granulosa cells (hGLC). The expression of selected target genes was measured in the presence or absence of ERK- or AKT-pathways inhibitors. In COS-7/LHCGR cells, hCG is 5-fold more potent than hLH (cAMP ED50: 107.1±14.3 pM and 530.0±51.2 pM, respectively). hLH maximal effect was significantly faster (10 minutes by hLH; 1 hour by hCG). In hGLC continuous exposure to equipotent doses of gonadotropins up to 36 hours revealed that intracellular cAMP production is oscillating and significantly higher by hCG versus hLH. Conversely, phospho-ERK1/2 and -AKT activation was more potent and sustained by hLH versus hCG. ERK1/2 and AKT inhibition removed the inhibitory effect on NRG1 (neuregulin) expression by hLH but not by hCG; ERK1/2 inhibition significantly increased hLH- but not hCG-stimulated CYP19A1 (aromatase) expression. We conclude that: i) hCG is more potent on cAMP production, while hLH is more potent on ERK and AKT activation; ii) hGLC respond to equipotent, constant hLH or hCG stimulation with a fluctuating cAMP production and progressive progesterone secretion; and iii) the expression of hLH and hCG target genes partly involves the activation of different pathways depending on the ligand. Therefore, the LHCGR is able to differentiate the activity of hLH and hCG.

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“…Although expression of these EGF-like factors is initially localized in the mural granulosa cells, they are subsequently induced within the cumulus cells as a result of autocrine and paracrine regulation by the factors themselves and by additional signaling pathways, including the action of prostaglandin E2 (PGE2) (11). Moreover, the cumulus celloocyte complex (COC) seems to be capable of responding to and coordinating signals not only from mural granulosa cells but also from thecal cells and the oocyte itself (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23).…”

mentioning

confidence: 99%

The Nuclear Receptor Cofactor Receptor-Interacting Protein 140 Is a Positive Regulator of Amphiregulin Expression and Cumulus Cell-Oocyte Complex Expansion in the Mouse Ovary

et al. 2010

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The nuclear receptor cofactor receptor-interacting protein 140 (RIP140) is essential for cumulus cell-oocyte complex (COC) expansion, follicular rupture, and oocyte release during ovulation. The expression of many genes necessary for COC expansion is impaired in the absence of RIP140, but the studies herein document that their expression can be restored and COC expansion rescued by treatment with the epidermal growth factor (EGF)-like factor amphiregulin (AREG) both in vitro and in vivo. We demonstrate by several approaches that RIP140 is required for the expression of the EGF-like factors in granulosa cells, but the dependence of genes involved in cumulus expansion, including Ptgs2 Has2, Tnfaip6, and Ptx3, is indirect because they are induced by AREG. Treatment of granulosa cells with forskolin to mimic the effects of LH increases AREG promoter activity in a RIP140-dependent manner that 1) requires an intact cAMP response element in the proximal promoter region of the Areg gene and 2) involves its actions as a coactivator for cAMP response element-binding protein/c-Jun transcription factors. Although human chorionic gonadotropin and AREG coadministration is sufficient to restore ovulation fully in RIP140 heterozygous mice in vivo, both follicular rupture and ovulation remain impaired in the RIP140 null mice. Thus, we conclude that although the level of RIP140 expression in the ovary is a crucial factor required for the transient expression of EGF-like factors necessary for cumulus expansion, it also plays a role in other signaling pathways that induce follicular rupture.

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Response of follicle cells to ovulatory stimuli within the follicle and in primary culture

Cited by 9 publications

References 21 publications

Mode of oocyte maturation affects EGF-like peptide function and oocyte competence

Mode of oocyte maturation affects EGF-like peptide function and oocyte competence

LH and hCG Action on the Same Receptor Results in Quantitatively and Qualitatively Different Intracellular Signalling

The Nuclear Receptor Cofactor Receptor-Interacting Protein 140 Is a Positive Regulator of Amphiregulin Expression and Cumulus Cell-Oocyte Complex Expansion in the Mouse Ovary

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