雌激素及其受体调控卵母细胞成熟的研究进展

doi:10.16431/j.cnki.1671-7236.2018.07.024

摘要/Abstract

摘要：

目前很多女性受到不孕不育、自然流产和出生缺陷等诸多生殖相关疾病的困扰，其主要原因为生殖细胞减数分裂异常和卵母细胞质量下降。雌激素不仅参与调控哺乳动物的发情和性行为，也参与调控卵母细胞的生长发育。雌激素受体作为类固醇激素受体的一种，在介导雌激素发挥基因组效应和非基因组效应中有着重要的作用。目前关于雌激素受体调控卵母细胞成熟的报道多集中于硬骨鱼类，特别是新型膜受体GPR30，而在哺乳动物方面的研究鲜有报道。因此作者介绍了雌激素核受体ERα、ERβ与新型膜受体GPR30的结构与分布，简述了膜受体GPR30的不同类型配体的研究进展，综述了雌激素受体在调控卵母细胞发育中的相互作用，发现雌激素的核受体与膜受体在卵母细胞成熟的过程中可能发挥不同的调控作用，并进一步阐述了雌激素及其受体在卵母细胞成熟过程中的潜在调控机制。

关键词: 雌激素; 雌激素受体; 卵母细胞; 成熟调控

Abstract:

Nowadays many women suffer from many reproductive-related diseases such as infertility,spontaneous abortion and birth defects.The main internal factors are the germ cell abnormal meiosis and the decline of oocyte quality.It is well known that estrogen not only regulates the estrus and sexual behavior of mammals, but also involves in the regulation of the growth and development of oocytes.Estrogen receptor, as a kind of steroid receptors, plays a vital role in mediating the genomics and non-genome effects of estrogen.At present,the reports about estrogen receptors regulating oocyte maturation are mostly focused on the teleosts, especially the novel membrane receptor GPR30, but few reports on mammalian.So the structure and distribution of estrogen nuclear receptor ER α,ER β and new membrane receptor GPR30 are described in this review.Moreover,the research progress of different types of ligands for membrane receptor GPR30 and the interaction between estrogen receptors and oocyte development are introduced.The analysis have showed that estrogen's nuclear receptors and membrane receptor may play a different regulatory role in the process of oocyte maturation.Besides, this article further reveals the potential mechanism of estrogen and its receptors in the regulation of maturation of oocyte.

Key words: estrogen; estrogen receptors; oocyte; mature regulation

中图分类号:

S852.2

葛均邦, 赵慧, 马保华. 雌激素及其受体调控卵母细胞成熟的研究进展[J]. 《中国畜牧兽医》, 2018, 45(7): 1919-1925.

GE Junbang, ZHAO Hui, MA Baohua. Research Progress on Regulation of Oocyte Maturation by Estrogen and Its Receptors[J]. , 2018, 45(7): 1919-1925.

参考文献

[1] LIU W,XIN Q,WANG X,et al.Estrogen receptors in granulosa cells govern meiotic resumption of pre-ovulatory oocytes in mammals[J].Cell Death & Disease,2017,8:e2662.
[2] HEWITT S C,KORACH K S.Estrogen receptors:Structure,mechanisms and function[J].Reviews in Endocrine and Metabolic Disorders,2002,3(3):193-200.
[3] KUIPER G G,ENMARK E,PELTO-HUIKKO M,et al.Cloning of a novel receptor expressed in rat prostate and ovary[J]. Proceedings of the National Academy of Sciences of the United States of America,1996,93(12):5925-5930.
[4] HEWITT S C,WINUTHAYANON W,KORACH K S.What's new in estrogen receptor action in the female reproductive tract[J]. Journal of Molecular Endocrinology,2016,56(2):55-71.
[5] PROSSNITZ E R,BARTON M.Estrogen biology:New insights into GPER function and clinical opportunities[J].Molecular and Cellular Endocrinology,2014,389(1):71-83.
[6] GUSTAFSSON J A.Historical overview of nuclear receptors[J].The Journal of Steroid Biochemistry and Molecular Biology,2016,157:3-6.
[7] PARAMANIK V,KRISHNAN H,KUMAR T M.Estrogen receptor α-and β-interacting proteins contain consensus secondary structures:An in silico study[J].Annals of Neurosciences,2018,25(1):1-10.
[8] LUBAHN D B,MOYER J S,GOLDING T S,et al.Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene[J].Proceedings of the National Academy of Sciences of the United States of America,1993,90(23):11162-11166.
[9] KREGE J H, HODGIN J B,COUSE J F,et al.Generation and reproductive phenotypes of mice lacking estrogen receptor β[J].Proceedings of the National Academy of Sciences of the United States of America,1998, 95(26):15677-15682.
[10] ADASHI E Y,HSUEH A J.Estrogens augment the stimulation of ovarian aromatase activity by follicle-stimulating hormone in cultured rat granulosa cells[J].Journal of Biological Chemistry,1982, 257(11):6077-6083.
[11] ZHANG M,SU Y,SUGIURA K,et al.Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes[J].Science,2010,330(6002):366.
[12] 蔡姣.雌激素对C型钠肽诱导的山羊卵母细胞减数分裂阻滞的影响[D].杨凌:西北农林科技大学,2016. CAI J.Estrogen on the c-type natriuretic peptide-induced meiotic arrest of goat oocytes[D].Yangling:Northwest A & F University,2016.(in Chinese)
[13] CHAO H,ZHANG X,CHEN B,et al.Bisphenol a exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway[J].Histochemistry and Cell Biology,2012,137(2):249-259.
[14] CARMECI C,THOMPSON D A,RING H Z,et al.Identification of a gene (GPR30) with homology to the G-protein-coupled receptor superfamily associated with estrogen receptor expression in breast cancer[J].Genomics,1997,45(3):607-617.
[15] THOMAS P,PANG Y,FILARDO E J,et al.Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells[J].Endocrinology,2005,146(2):624-632.
[16] ARONICA S M, KRAUS W L,KATZENELLENBOGEN B S.Estrogen action via the cAMP signaling pathway:Stimulation of adenylate cyclase and cAMP-regulated gene transcription[J].Proceedings of the National Academy of Sciences of the United States of America,1994,91(18):8517-8521.
[17] IMPROTA-BREARS T,WHORTON A R,CODAZZI F,et al.Estrogen-induced activation of mitogen-activated protein kinase requires mobilization of intracellular calcium[J].Proceedings of the National Academy of Sciences of the United States of America,1999,96(8):4686-4691.
[18] FILARDO E J,QUINN J A,BLAND K I,et al.Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog,GPR30,and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF[J].Molecular Endocrinology,2000,14(10):1649-1660.
[19] CHENG S,DONG J,PANG Y,et al.Anatomical location and redistribution of G protein-coupled estrogen receptor-1 during the estrus cycle in mouse kidney and specific binding to estrogens but not aldosterone[J].Molecular and Cellular Endocrinology,2014,382(2):950-959.
[20] PROSSNITZ E R,ARTERBURN J B,OHLSTEIN E H.International union of basic and clinical pharmacology.XCⅦ.G protein-coupled estrogen receptor and its pharmacologic modulators[J].Pharmacological Reviews, 2015,67(3):505.
[21] ROMANO S N,GORELICK D A.Crosstalk between nuclear and G protein-coupled estrogen receptors[J].General and Comparative Endocrinology,2017,6480(16):30496-30498.
[22] LI Y,REN C,ZHANG Q,et al.Expression of G protein estrogen receptor (GPER) on membrane of mouse oocytes during maturation[J].Journal of Assisted Reproduction and Genetics,2013,30(2):227-232.
[23] PANG Y,THOMAS P.Role of G protein-coupled estrogen receptor 1,GPER,in inhibition of oocyte maturation by endogenous estrogens in zebrafish[J].Developmental Biology,2010,342(2):194-206.
[24] FELDMAN R D,LIMBIRD L E.Copernicus revisited:Overturning ptolemy's view of the GPER universe[J].Trends in Endocrinology & Metabolism,2015,26(11):592-594.
[25] BARTON M,FILARDO E J,LOLAIT S J,et al.Twenty years of the G protein-coupled estrogen receptor GPER:Historical and personal perspec-tives[J].The Journal of Steroid Biochemistry and Molecular Biology,2018,176:4-15.
[26] RIGIRACCIOLO D C,SCARPELLI A,LAPPANO R,et al.GPER is involved in the stimulatory effects of aldosterone in breast cancer cells and breast tumor-derived endothelial cells[J].Oncotarget,2016, 7(1):94-111.
[27] MOTULSKY H J,INSEL P A.Adrenergic receptors in man:Direct identification,physiologic regulation, and clinical alterations[J].The New England Journal of Medicine,1982,307(1):18-29.
[28] PROSSNITZ E R,MAGGIOLINI M.Mechanisms of estrogen signaling and gene expression via GPR30[J].Molecular and Cellular Endocrinology,2009,308(1):32-38.
[29] DENNIS M K,BURAI R,RAMESH C,et al.In vivo effects of a GPR30 antagonist[J].Nature Chemical Biology, 2009,5:421-427.
[30] TSKITISHVILI E,PEQUEUX C,MUNAUT C,et al.Estrogen receptors and estetrol-dependent neuroprotective actions:A pilot study[J].The Journal of Endocrinology,2017,232(1):85-95.
[31] DENNIS M K,FIELD A S,BURAI R,et al.Identification of a GPER/GPR30 antagonist with improved estrogen receptor counter selectivity[J].The Journal of Steroid Biochemistry and Molecular Biology,2011,127(3):358-366.
[32] OWMAN C,NILSSON C,LOLAIT S J.Cloning of cDNA encoding a putative chemoattractant receptor[J].Genomics, 1996,37(2):187-194.
[33] 杨光伦,涂刚.雌激素受体GPR30研究进展[J].中国癌症杂志,2009,11:881-886. YANG G L,TU G.Advances on novel estrogen receptor GPR30[J].China Oncology,2009,11:881-886.(in Chinese)
[34] WANG C,PROSSNITZ E R,ROY S K.Expression of G protein-coupled receptor 30 in the hamster ovary:Differential regulation by gonadotropins and steroid hormones[J].Endocrinology,2007,148:4853-4864.
[35] FELDMAN R D,LIMBIRD L E.GPER (GPR30):A nongenomic receptor (GPCR) for steroid hormones with implications for cardiovascular disease and cancer[J].Annual Review of Pharmacology and Toxicology,2017,57:567-584.
[36] PANG Y,DONG J,THOMAS P.Estrogen signaling characteristics of atlantic croaker G protein-coupled receptor 30(GPR30) and evidence it is involved in maintenance of oocyte meiotic arrest[J].Endocrinology,2008, 149(7):3410-3426.
[37] SAKAMOTO H,MATSUDA K,HOSOKAWA K,et al.Expression of G protein-coupled receptor-30,a G protein-coupled membrane estrogen receptor,in oxytocin neurons of the rat paraventricular and supraoptic nuclei[J].Endocrinology,2007,148(12):5842-5850.
[38] REVANKAR C M, MITCHELL H D, FIELD A S,et al.Synthetic estrogen derivatives demonstrate the functionality of intracellular GPR30[J].ACS Chemical Biology,2007,2(8):536-544.
[39] MIZUKAMI Y.In vivo functions of GPR30/GPER-1,a membrane receptor for estrogen:From discovery to functions in vivo[J].Endocrine Journal,2010,57(2):101-107.
[40] ZHU C X,XIONG W,WANG M L,et al.Nuclear G protein-coupled oestrogen receptor (GPR30) predicts poor survival in patients with ovarian cancer[J].Journal of International Medical Research,2017,46(2):723-731.
[41] 高学军.雌激素及其受体对动物乳腺上皮细胞泌乳性能的影响[J].中国畜牧兽医,2011,38(4):151-153. GAO X J.Effects of estrogen and its receptor on lactation fuction of mammary gland epithelial cell in mammal[J].China Animal Husbandry & Veterinary Medicine,2011,38(4):151-153.(in Chinese)
[42] BARTON M.Position paper:The membrane estrogen receptor GPER-clues and questions[J].Steroids,2012, 77(10):935-942.
[43] ALBANITO L,MADEO A,LAPPANO R,et al.G protein-coupled receptor 30(GPR30) mediates gene expression changes and growth response to 17beta-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells[J].Cancer Research,2007,67(4):1859-1866.
[44] GAO F,MA X,OSTMANN A B,et al.GPR30 activation opposes estrogen-dependent uterine growth via inhibition of stromal ERK1/2 and estrogen receptor alpha (ERα) phosphorylation signals[J].Endocrinology,2011, 152(4):1434-1447.
[45] VIVACQUA A,BONOFIGLIO D,RECCHIA A G,et al.The G protein-coupled receptor GPR30 mediates the proliferative effects induced by 17beta-estradiol and hydroxytamoxifen in endometrial cancer cells[J].Molecular Endocrinology,2006,20(3):631-646.
[46] HUANG G S,GUNTER M J,AREND R C,et al.Co-expression of GPR30 and ERbeta and their association with disease progression in uterine carcinosarcoma[J].American Journal of Obstetrics and Gynecology,2010,203(3):241-242.
[47] WANG Z,YIN L.Estrogen receptor alpha-36(ER-α36):A new player in human breast cancer[J].Molecular and Cellular Endocrinology,2015,418:193-206.
[48] TAYLOR S E,MARTIN-HIRSCH P L,MARTIN F L.Oestrogen receptor splice variants in the pathogenesis of disease[J].Cancer Letters,2010,288(2):133-148.
[49] WALLACIDES A,CHESNEL A,AJJ H,et al.Estrogens promote proliferation of the seminoma-like TCam-2 cell line through a GPER-dependent ERα36 induction[J].Molecular and Cellular Endocrinology,2012,350(1):61-71.
[50] KANG L,ZHANG X,XIE Y,et al.Involvement of estrogen receptor variant ER-alpha36, not GPR30, in nongenomic estrogen signaling[J].Molecular Endocrinology,2010,24(4):709-721.
[51] LINDSEY S H,YAMALEYEVA L M,BROSNIHAN K B,et al.Estrogen receptor GPR30 reduces oxidative stress and proteinuria in the salt-sensitive female mRen2.Lewis rat[J].Hypertension,2011,58(4):665-671.
[52] CLELLAND E,PENG C.Endocrine/paracrine control of zebrafish ovarian development[J].Molecular and Cellular Endocrinology,2009,312(1):42-52.
[53] PEYTON C,THOMAS P.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)[J].Biology of Reproduction,2011,85(1):42-50.
[54] PANG Y,GE W.Gonadotropin and activing enhance maturational competence of oocytes in the zebrafish (Danio rerio)[J].Biology of Reproduction,2002,66(2):259-265.
[55] 张骏鸿.C型钠肽对山羊卵母细胞体外成熟及孤雌胚胎发育的影响[D].杨凌:西北农林科技大学, 2014. ZHANG J H.Effect of C type natriuretic peptide on in vitro maturation of goat oocytes and development of parthenogenetic embryos[D].Yangling:Northwest A & F University,2014.(in Chinese)
[56] 李伊然.雌激素及其受体与卵母细胞成熟的相关性[D].银川:宁夏医科大学, 2013. LI Y R.The relationship between estrogen and its receptor and oocyte maturation[D].Yinchuan:Ningxia Medical University,2013.(in Chinese)