G protein-coupled receptor 30 mediates meiosis resumption and gap junction communications downregulation in goat cumulus-oocyte complexes by 17β-estradiol
Zhang, Hui ; Wei, Qiang ; Gao, Zhen ; Ma, Chiyuan ; Yang, Zhenshan LU
; Zhao, Hui
; Liu, Chen
; Liu, Jie
; Zhao, Xiaoe
and Ma, Baohua
(2019)
In Journal of Steroid Biochemistry and Molecular Biology
187.
p.58-67
- Abstract
Estrogen plays a critical role in the regulation of gap junctions between oocytes and granulosa cells in mammalian ovaries. G protein-coupled receptor 30 (GPR30) was identified as a membrane estrogen receptor, mediating rapid, nongenomic signaling events that might be responsible for the regulation of oocyte meiosis resumption and gap junction intercellular communications (GJICs). The present study aimed to determine the expression and localization of GPR30 and its role in oocyte meiotic progression and GJICs in goat cumulus-oocyte complexes (COCs). Immunofluorescence experiments revealed that GPR30 was primarily located in the plasma membrane of cumulus cells and oocytes in goats. 17β-estradiol could promote oocyte meiotic progression,... (More)
Estrogen plays a critical role in the regulation of gap junctions between oocytes and granulosa cells in mammalian ovaries. G protein-coupled receptor 30 (GPR30) was identified as a membrane estrogen receptor, mediating rapid, nongenomic signaling events that might be responsible for the regulation of oocyte meiosis resumption and gap junction intercellular communications (GJICs). The present study aimed to determine the expression and localization of GPR30 and its role in oocyte meiotic progression and GJICs in goat cumulus-oocyte complexes (COCs). Immunofluorescence experiments revealed that GPR30 was primarily located in the plasma membrane of cumulus cells and oocytes in goats. 17β-estradiol could promote oocyte meiotic progression, which was blocked by G15 (a selective GPR30 antagonist) but not ICI182780 (a nuclear estrogen receptor inhibitor) in the early stage of in vitro culture. The effect of 17β-estradiol on the GJICs was quantified by lucifer yellow (LY) microinjection and calcein-AM fluorescent dye diffusion. 17β-estradiol treatment of goat COCs resulted in rapid downregulation of GJICs. The transfer of calcein from cumulus cells to oocytes could be significantly inhibited by carbenoxolone (a known gap junction blocker), 17β-estradiol or G1 (a GPR30 agonist), and this inhibition could be reversed by G15 but not ICI182780, indicating that GPR30 mediates the effect of 17β-estradiol on the rapid downregulation of GJICs. 17β-estradiol also stimulated the serine 368 phosphorylation of connexin 43 (Cx43) when COCs were in vitro cultured for 4 h, 6 h, and 8 h. More importantly, 17β-estradiol or G1 could separately promote the phosphorylation of extracellular signal-regulated kinase 1/2 (ERK 1/2) and Cx43 significantly when COCs were cultured for 4 h. Furthermore, both ERK1/2 and Cx43 phosphorylation could be inhibited by G15 and the epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor AG1478 or by the ERK1/2 inhibitor PD98059, indicating that EGFR-ERK1/2 signaling was involved in these events. These results supported the hypothesis that GPR30 mediated 17β-estradiol-stimulated meiotic resumption and GJIC reduction in goat COCs. Thus, the present study provides novel insights into elucidating the mechanisms for steroid hormone action in the regulation of oocyte maturation.
(Less)
- author
- Zhang, Hui
; Wei, Qiang
; Gao, Zhen
; Ma, Chiyuan
; Yang, Zhenshan
LU
; Zhao, Hui
; Liu, Chen
; Liu, Jie
; Zhao, Xiaoe
and Ma, Baohua
- publishing date
- 2019-03
- type
- Contribution to journal
- publication status
- published
- keywords
- 17β-estradiol, Cumulus-oocyte complexes, G protein-coupled receptor 30, Gap junction intercellular communications
- in
- Journal of Steroid Biochemistry and Molecular Biology
- volume
- 187
- pages
- 10 pages
- publisher
- Elsevier
- external identifiers
-
- pmid:30414946
- scopus:85056572463
- ISSN
- 0960-0760
- DOI
- 10.1016/j.jsbmb.2018.11.001
- language
- English
- LU publication?
- no
- additional info
- Funding Information: This work was supported by the National Nature Science Foundation of China ( 31772818 ); Natural Science Basic Research Plan in Shaanxi Province [ 2014JQ3101 ] and Basic Scientific Research Business Expenses of Northwest A&F University, Youth Cultivate Special Program [ 2452015319 ]. Funding Information: This work was supported by the National Nature Science Foundation of China (31772818); Natural Science Basic Research Plan in Shaanxi Province [2014JQ3101] and Basic Scientific Research Business Expenses of Northwest A&F University, Youth Cultivate Special Program [2452015319]. Publisher Copyright: © 2018 Elsevier Ltd
- id
- da214ce4-ff4d-47d7-8c51-af46decae6b9
- date added to LUP
- 2024-02-28 15:03:35
- date last changed
- 2024-03-30 09:34:42
@article{da214ce4-ff4d-47d7-8c51-af46decae6b9,
abstract = {{<p>Estrogen plays a critical role in the regulation of gap junctions between oocytes and granulosa cells in mammalian ovaries. G protein-coupled receptor 30 (GPR30) was identified as a membrane estrogen receptor, mediating rapid, nongenomic signaling events that might be responsible for the regulation of oocyte meiosis resumption and gap junction intercellular communications (GJICs). The present study aimed to determine the expression and localization of GPR30 and its role in oocyte meiotic progression and GJICs in goat cumulus-oocyte complexes (COCs). Immunofluorescence experiments revealed that GPR30 was primarily located in the plasma membrane of cumulus cells and oocytes in goats. 17β-estradiol could promote oocyte meiotic progression, which was blocked by G15 (a selective GPR30 antagonist) but not ICI182780 (a nuclear estrogen receptor inhibitor) in the early stage of in vitro culture. The effect of 17β-estradiol on the GJICs was quantified by lucifer yellow (LY) microinjection and calcein-AM fluorescent dye diffusion. 17β-estradiol treatment of goat COCs resulted in rapid downregulation of GJICs. The transfer of calcein from cumulus cells to oocytes could be significantly inhibited by carbenoxolone (a known gap junction blocker), 17β-estradiol or G1 (a GPR30 agonist), and this inhibition could be reversed by G15 but not ICI182780, indicating that GPR30 mediates the effect of 17β-estradiol on the rapid downregulation of GJICs. 17β-estradiol also stimulated the serine 368 phosphorylation of connexin 43 (Cx43) when COCs were in vitro cultured for 4 h, 6 h, and 8 h. More importantly, 17β-estradiol or G1 could separately promote the phosphorylation of extracellular signal-regulated kinase 1/2 (ERK 1/2) and Cx43 significantly when COCs were cultured for 4 h. Furthermore, both ERK1/2 and Cx43 phosphorylation could be inhibited by G15 and the epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor AG1478 or by the ERK1/2 inhibitor PD98059, indicating that EGFR-ERK1/2 signaling was involved in these events. These results supported the hypothesis that GPR30 mediated 17β-estradiol-stimulated meiotic resumption and GJIC reduction in goat COCs. Thus, the present study provides novel insights into elucidating the mechanisms for steroid hormone action in the regulation of oocyte maturation.</p>}},
author = {{Zhang, Hui and Wei, Qiang and Gao, Zhen and Ma, Chiyuan and Yang, Zhenshan and Zhao, Hui and Liu, Chen and Liu, Jie and Zhao, Xiaoe and Ma, Baohua}},
issn = {{0960-0760}},
keywords = {{17β-estradiol; Cumulus-oocyte complexes; G protein-coupled receptor 30; Gap junction intercellular communications}},
language = {{eng}},
pages = {{58--67}},
publisher = {{Elsevier}},
series = {{Journal of Steroid Biochemistry and Molecular Biology}},
title = {{G protein-coupled receptor 30 mediates meiosis resumption and gap junction communications downregulation in goat cumulus-oocyte complexes by 17β-estradiol}},
url = {{http://dx.doi.org/10.1016/j.jsbmb.2018.11.001}},
doi = {{10.1016/j.jsbmb.2018.11.001}},
volume = {{187}},
year = {{2019}},
}