Involvement of Epidermal Growth Factor Receptor Signaling in Estrogen Inhibition of Oocyte Maturation Mediated Through the G Protein-Coupled Estrogen Receptor (Gper) in Zebrafish (Danio rerio)1

Peyton, Candace; Thomas, Peter

doi:10.1095/biolreprod.110.088765

Cited by 88 publications

(87 citation statements)

References 45 publications

(88 reference statements)

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“…Ovarian follicles were collected and incubated according to procedures described previously , Peyton & Thomas 2011 for the zebrafish germinal vesicle breakdown (GVBD) assay. Briefly, ovarian follicles were separated and only those O560 mm in diameter were selected for subsequent enzymatic treatments with collagenase (50 mg/ml) to remove the follicle layers and obtain denuded oocytes for the GVBD bioassay.…”

Section: Germinal Vesicle Breakdown Assaymentioning

confidence: 99%

“…To confirm that the oocytes were maturationally competent, the zebrafish maturation-inducing steroid, DHP, was used as a positive control in all the GVBD assays. The effects of E 2 (100 nM), G-1 (100 nM), and EGFR (ErbB1) inhibitors AG1478 (50 mM) and AG825 (50 mM) on GVBD were tested as described previously (Peyton & Thomas 2011) with or without co-treatment with the PGRMC1 inhibitor, AG205 (20 mM). All treatments were replicated three times in each experiment and all the GVBD experiments were repeated three times.…”

Section: Germinal Vesicle Breakdown Assaymentioning

confidence: 99%

“…Thus, AG205 is a useful PGRMC1 antagonist for exploring its adaptor protein functions. G protein-coupled estrogen receptor 1 (GPER1), formerly known as GPR30, is a novel, specific seventransmembrane-domain estrogen receptor coupled to a stimulatory G protein (G s ) that mediates rapid, nongenomic estrogen actions through activation of adenylyl cyclase and EGFR transactivation in various cell types, including breast cancer cells and fish oocytes (Filardo et al 2000, Filardo 2002, Peyton & Thomas 2011. Activation of Gper on Atlantic croaker and zebrafish oocytes by estradiol-17b (E 2 ) or the specific GPER agonist, G-1, blocks spontaneous meiotic maturation of denuded oocytes and attenuates induction of oocyte maturation (OM) by the maturationinducing steroid (Pang et al 2008, Pang & Thomas 2009.…”

Section: Introductionmentioning

confidence: 99%

“…These inhibitory actions of estrogens on OM are partially mediated through activation of membrane adenylyl cyclase to sustain high cAMP concentrations in the oocyte, which are essential for maintaining meiotic arrest (DeManno & Goetz 1987, Pang et al 2008. They may also involve Egfr and Mapk3/1 because these inhibitory effects were blocked by co-treatment with several specific inhibitors of the EGFR pathway and MAPK (Peyton & Thomas 2011). Moreover, initial evidence was obtained from western blot analyses for the presence of Egfr on the plasma membranes of denuded oocytes (Peyton & Thomas 2011).…”

Section: Introductionmentioning

confidence: 99%

“…They may also involve Egfr and Mapk3/1 because these inhibitory effects were blocked by co-treatment with several specific inhibitors of the EGFR pathway and MAPK (Peyton & Thomas 2011). Moreover, initial evidence was obtained from western blot analyses for the presence of Egfr on the plasma membranes of denuded oocytes (Peyton & Thomas 2011). However, additional research is required to clarify the roles of Egfr in OM, because EGF has been shown to exert an opposite action in teleost ovarian follicle cells to stimulate OM and the resumption of meiosis by increasing expression of activin (Wang & Ge 2004, Van Der Kraak & Lister 2011.…”

Section: Introductionmentioning

confidence: 99%

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Role of Pgrmc1 in estrogen maintenance of meiotic arrest in zebrafish oocytes through Gper/Egfr

Aizen¹,

Thomas²

2015

Journal of Endocrinology

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The regulation of receptor trafficking to the cell surface and its effect on responses of target cells to growth factors and hormones remain poorly understood. Initial evidence has been recently obtained using cancer cells that surface expression of the epidermal growth factor receptor (EGFR) is dependent on its association with progesterone receptor membrane component 1 (PGRMC1). Estrogen inhibition of oocyte maturation (OM) in zebrafish is mediated through G-protein-coupled estrogen membrane receptor 1 (Gper1) and involves activation of Egfr. Therefore, in this study, the potential roles of Pgrmc1 in the cell surface expression and functions of Egfr in normal cells were investigated in this in vitro OM model of Egfr action using an inhibitor of PGMRC1 signaling, AG205. A single w60 kDa protein band, which corresponds to the size of the Pgrmc1 dimer, was detected on plasma membranes of fully grown oocytes by western blotting. Co-treatment with the PGRMC1 inhibitor AG205 (20 mM) blocked the inhibitory effects of 100 nM estradiol-17b and the GPER agonist, G-1, on spontaneous maturation of denuded zebrafish oocytes. Moreover, reversal of these estrogen effects on OM by the EGFR inhibitors AG1478 and AG825 (50 mM) was prevented by co-incubation with the PGRMC1 inhibitor. Inhibition of Pgrmc1 signaling with AG205 also caused a decrease in Egfr-dependent signaling and Egfr expression on oocyte cell membranes. These results indicate that maintenance of Pgrmc1 signaling is required for Egfr expression on zebrafish oocyte cell membranes and for conserving the functions of Egfr in maintaining meiotic arrest through estrogen activation of Gper.

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Section: Germinal Vesicle Breakdown Assaymentioning

confidence: 99%

Section: Germinal Vesicle Breakdown Assaymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Role of Pgrmc1 in estrogen maintenance of meiotic arrest in zebrafish oocytes through Gper/Egfr

Aizen¹,

Thomas²

2015

Journal of Endocrinology

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Role of ataxia‐telangiectasia mutated (ATM) in porcine oocyte in vitro maturation

Lin

Kim

2015

Cell Biology International

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Ataxia-telangiectasia mutated (ATM) is critical for the DNA damage response, cell cycle checkpoints, and apoptosis. Significant effort has focused on elucidating the relationship between ATM and other nuclear signal transducers; however, little is known about the connection between ATM and oocyte meiotic maturation. We investigated the function of ATM in porcine oocytes. ATM was expressed at all stages of oocyte maturation and localized predominantly in the nucleus. Furthermore, the ATM-specific inhibitor KU-55933 blocked porcine oocyte maturation, reducing the percentages of oocytes that underwent germinal vesicle breakdown (GVBD) and first polar body extrusion. KU-55933 also decreased the expression of DNA damage-related genes (breast cancer 1, budding uninhibited by benzimidazoles 1, and P53) and reduced the mRNA and protein levels of AKT and other cell cycle-regulated genes that are predominantly expressed during G2/M phase, including bone morphogenetic protein 15, growth differentiation factor 9, cell division cycle protein 2, cyclinB1, and AKT. KU-55933 treatment decreased the developmental potential of blastocysts following parthenogenetic activation and increased the level of apoptosis. Together, these data suggested that ATM influenced the meiotic and cytoplasmic maturation of porcine oocytes, potentially by decreasing their sensitivity to DNA strand breaks, stimulating the AKT pathway, and/or altering the expression of other maternal genes.

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Characterization of G protein‐coupled estrogen receptors in Japanese medaka, Oryzias latipes

Miyaoku

Ogino

Lange

et al. 2020

J of Applied Toxicology

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The G protein‐coupled estrogen receptor 1 (Gper1) is a membrane‐bound estrogen receptor that mediates non‐genomic action of estrogens. A Gper1‐mediating pathway has been implicated in reproductive activities in fish, including oocyte growth, but Gper1 has been characterized in only a very limited number of fish species. In this study, we cloned and characterized two genes encoding medaka (Oryzias latipes) Gper1s, namely, Gper1a and Gper1b, and phylogenic and synteny analyses suggest that these genes originate through a teleost‐specific whole genome duplication event. We found that Gper1a induced phosphorylation of mitogen‐activated protein kinase (MAPK) in 293T cells transfected with medaka Gper1s on exposure to the natural estrogen, 17β‐estradiol (E2) and a synthetic Gper1 agonist (G‐1), and treatment with both E2 and G‐1 also decreased the rate of spontaneous maturation in medaka oocytes. These findings show that the processes for oocyte growth and maturation are sensitive to estrogens and are possibly mediated through Gper1a in medaka. We also show that 17α‐ethinylestradiol (EE2), one of the most potent estrogenic endocrine‐disrupting chemicals, and bisphenol A (BPA, a weak environmental estrogen) augmented phosphorylation of MAPK through medaka Gper1s in 293T cells. Interestingly, however, treatment with EE2 or BPA did not attenuate maturation of medaka oocytes. Our findings support that Gper1‐mediated effects on oocytes are conserved among fish species, but effects of estrogenic endocrine‐disrupting chemicals on oocytes acting through Gper1 may be divergent among fish species.

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Involvement of Epidermal Growth Factor Receptor Signaling in Estrogen Inhibition of Oocyte Maturation Mediated Through the G Protein-Coupled Estrogen Receptor (Gper) in Zebrafish (Danio rerio)1

Cited by 88 publications

References 45 publications

Role of Pgrmc1 in estrogen maintenance of meiotic arrest in zebrafish oocytes through Gper/Egfr

Role of Pgrmc1 in estrogen maintenance of meiotic arrest in zebrafish oocytes through Gper/Egfr

Role of ataxia‐telangiectasia mutated (ATM) in porcine oocyte in vitro maturation

Characterization of G protein‐coupled estrogen receptors in Japanese medaka, Oryzias latipes

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