Role of G protein-coupled estrogen receptor 1, GPER, in inhibition of oocyte maturation by endogenous estrogens in zebrafish.
Estrogen inhibition of oocyte maturation (OM) and the role of GPER (formerly known as GPR30) were investigated in zebrafish. Estradiol-17beta (E2) and G-1, a GPER-selective agonist, bound to zebrafish oocyte membranes suggesting the presence of GPER which was confirmed by immunocytochemistry using a specific GPER antibody. Incubation of follicle-enclosed oocytes with an aromatase inhibitor, ATD, and enzymatic and manual removal of the ovarian follicle cell layers significantly increased spontaneous OM which was partially reversed by co-treatment with either 100 nM E2 or G-1. Incubation of denuded oocytes with the GPER antibody blocked the inhibitory effects of estrogens on OM, whereas microinjection of estrogen receptor alpha (ERalpha) antisense oligonucleotides into the oocytes was ineffective. The results suggest that endogenous estrogens produced by the follicle cells inhibit or delay spontaneous maturation of zebrafish oocytes and that this estrogen action is mediated through GPER. Treatment with E2 and G-1 also attenuated the stimulatory effect of the teleost maturation-inducing steroid, 17,20beta-dihyroxy-4-pregnen-3-one (DHP), on OM. Moreover, E2 and G-1 down-regulated the expression of membrane progestin receptor alpha (mPRalpha), the intermediary in DHP induction of OM. Conversely DHP treatment caused a >50% decline in GPER mRNA levels. The results suggest that estrogens and GPER are critical components of the endocrine system controlling the onset of OM in zebrafish. A model is proposed for the dual control of the onset of oocyte maturation in teleosts by estrogens and progestins acting through GPER and mPRalpha, respectively, at different stages of oocyte development.
Pang
Yefei
Y
University of Texas at Austin, Marine Science Institute, Port Aransas, TX 78373, USA.
Thomas
Peter
P
D000818:Animals; D004967:Estrogens / Q000378:metabolism*; D005260:Female; D036341:Intercellular Signaling Peptides and Proteins / Q000378:metabolism; D008297:Male; D009865:Oocytes / Q000378:metabolism; D006080:Ovarian Follicle / Q000378:metabolism; D010053:Ovary / Q000378:metabolism; D011372:Progestins / Q000378:metabolism; D043562:Receptors, G-Protein-Coupled / Q000378:metabolism*; D015027:Zebrafish / Q000196:embryology* / Q000378:metabolism; D029961:Zebrafish Proteins / Q000378:metabolism*
D004967:Estrogens; D036341:Intercellular Signaling Peptides and Proteins; D011372:Progestins; D043562:Receptors, G-Protein-Coupled; D029961:Zebrafish Proteins; C549840:gper1 protein, zebrafish; C018355:intraovarian peptides
C R Acad Hebd Seances Acad Sci D. 1975 Sep 22;281(12):811-4
813851
Am J Pathol. 2007 Apr;170(4):1210-8
17392161
Biol Reprod. 2001 Jan;64(1):21-9
11133654
Biol Reprod. 2005 Nov;73(5):988-96
16014813
J Soc Gynecol Investig. 2000 Jan-Feb;7(1 Suppl):S33-7
10732327
Gen Comp Endocrinol. 1989 Sep;75(3):405-12
2792726
Dev Growth Differ. 1987 Feb;29(1):1-12
37282157
Dev Biol. 1994 Dec;166(2):615-22
7813780
Mol Cell Endocrinol. 2009 Nov 27;312(1-2):72-9
19773085
Dev Biol. 2005 Nov 15;287(2):249-61
16229830
Reprod Biol Endocrinol. 2007 Jun 05;5:21
17550604
Annu Rev Biochem. 1994;63:451-86
7979245
Nat Rev Drug Discov. 2004 Jan;3(1):27-41
14708019
Mol Endocrinol. 2000 Oct;14(10):1649-60
11043579
Steroids. 2010 Aug-Sep;75(8-9):595-602
19931550
Trends Endocrinol Metab. 2005 Oct;16(8):362-7
16125968
Dev Biol. 2005 Sep 1;285(1):70-9
16099448
J Immunol. 2009 Mar 1;182(5):3294-303
19234228
Biol Reprod. 1990 Nov;43(5):818-27
2291916
Steroids. 2010 Apr;75(4-5):314-22
20096719
Gen Comp Endocrinol. 1987 May;66(2):233-43
3034715
C R Acad Hebd Seances Acad Sci D. 1976 Oct 27;283(10):1205-8
827357
Dev Biol. 2004 Mar 1;267(1):1-13
14975713
Endocrinology. 2007 Oct;148(10):4853-64
17640985
Gen Comp Endocrinol. 2006 Jan 1;145(1):101-8
16139281
Fish Physiol Biochem. 1986 Oct;2(1-4):65-74
24233168
Endocrinology. 1992 Jun;130(6):3223-30
1375896
Biol Reprod. 2000 Apr;62(4):995-1004
10727269
Mol Endocrinol. 2010 Apr;24(4):709-21
20197310
Endocrinology. 2006 May;147(5):2280-6
16439460
Dev Biol (N Y 1985). 1985;1:127-77
3917200
Endocrinology. 2007 Sep;148(9):4458-65
17525120
Gen Comp Endocrinol. 1994 Aug;95(2):178-91
7958748
Rev Endocr Metab Disord. 2002 Sep;3(3):193-200
12215714
Steroids. 2002 May;67(6):511-7
11960629
Gen Comp Endocrinol. 1990 Jun;78(3):361-73
2347486
Gen Comp Endocrinol. 1988 Sep;71(3):516-23
3192072
Biol Cell. 1998 Oct;90(6-7):453-60
9923070
Biochem Biophys Res Commun. 1996 Nov 12;228(2):285-92
8920907
Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2231-6
12574519
Gen Comp Endocrinol. 1987 Jun;66(3):333-42
3609704
Endocrinology. 2008 Jul;149(7):3410-26
18420744
J Biol Chem. 1981 Jun 25;256(12):6368-73
7240211
Endocrinology. 2005 Feb;146(2):624-32
15539556
Gen Comp Endocrinol. 2010 Jan 1;165(1):144-54
19539624
Fish Physiol Biochem. 1995 Dec;14(6):489-500
24197645
Curr Top Dev Biol. 1995;30:103-45
7555044
J Endocrinol. 2006 Aug;190(2):247-60
16899559
Gen Comp Endocrinol. 2009 Mar;161(1):58-61
18952087
Gen Comp Endocrinol. 1988 Dec;72(3):443-52
3240853
J Steroid Biochem Mol Biol. 2006 Dec;102(1-5):175-9
17088055
Biol Reprod. 1987 Jun;36(5):1321-32
3040136
Endocr Rev. 1998 Feb;19(1):3-17
9494778
Environ Toxicol. 2006 Aug;21(4):332-7
16841311
Mol Endocrinol. 2002 Jan;16(1):70-84
11773440
Science. 2005 Mar 11;307(5715):1625-30
15705806