A Role for GPRx, a Novel GPR3/6/12-related G-protein Coupled Receptor, in the Maintenance of Meiotic Arrest in Xenopus Laevis Oocytes

Overview

Journal Dev Biol

Publisher Elsevier

Specialties Biology
Reproductive Medicine

Date 2008 Apr 3

PMID 18381211

Citations 15

Authors

Diana Rios-Cardona

Roberto R Ricardo-Gonzalez

Ajay Chawla

James E Ferrell Jr

Affiliations

Soon will be listed here.

Abstract

Progesterone-induced Xenopus laevis oocyte maturation is mediated via a plasma membrane-bound receptor and does not require gene transcription. Evidence from several species suggests that the relevant progesterone receptor is a G-protein coupled receptor (GPCR) and that a second receptor-GPR3 and/or GPR12 in mammals-tonically opposes the progesterone receptor. We have cloned a novel X. laevis GPCR, GPRx, which may play a similar role to GPR3/GPR12 in amphibians and fishes. GPRx is related to but distinct from GPR3, GPR6, and GPR12; GPRx orthologs are present in Xenopus tropicalis and Danio rerio, but apparently not in birds or mammals. X. laevis GPRx is mainly expressed in brain, ovary, and testis. The GPRx mRNA increases during oogenesis, persists during oocyte maturation and early embryogenesis, and then falls after the midblastula transition. Microinjection of GPRx mRNA increases the concentration of cAMP in oocytes and causes the oocytes to fail to respond to progesterone, and this block is reversed by co-injecting GPRx with morpholino oligonucleotides. Morpholino injections did not cause spontaneous maturation of oocytes, but did accelerate progesterone-induced maturation. Thus, GPRx contributes to the maintenance of G2-arrest in immature X. laevis oocytes.

Citing Articles

Progesterone induces meiosis through two obligate co-receptors with PLA2 activity.

Nader N, Assaf L, Zarif L, Halama A, Yadav S, Dib M Elife. 2025; 13.

PMID: 39873665 PMC: 11774516. DOI: 10.7554/eLife.92635.

Progesterone induces meiosis through two obligate co-receptors with PLA2 activity.

Nader N, Assaf L, Zarif L, Halama A, Yadav S, Dib M bioRxiv. 2023; .

PMID: 37905030 PMC: 10614741. DOI: 10.1101/2023.09.09.556646.

Dissection of the Ovulatory Process Using Approaches.

Tokmakov A, Stefanov V, Sato K Front Cell Dev Biol. 2020; 8:605379.

PMID: 33363163 PMC: 7755606. DOI: 10.3389/fcell.2020.605379.

Translational Control of Oocyte Meiosis: Toward the Genomic Era.

Meneau F, Dupre A, Jessus C, Daldello E Cells. 2020; 9(6).

PMID: 32575604 PMC: 7348711. DOI: 10.3390/cells9061502.

Advances in Neurobiology and Pharmacology of GPR12.

Allende G, Chavez-Reyes J, Guerrero-Alba R, Vazquez-Leon P, Marichal-Cancino B Front Pharmacol. 2020; 11:628.

PMID: 32457622 PMC: 7226366. DOI: 10.3389/fphar.2020.00628.

References

Filardo E, Thomas P . GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol Metab. 2005; 16(8):362-7. DOI: 10.1016/j.tem.2005.08.005. View

Smythe C, Newport J . Systems for the study of nuclear assembly, DNA replication, and nuclear breakdown in Xenopus laevis egg extracts. Methods Cell Biol. 1991; 35:449-68. DOI: 10.1016/s0091-679x(08)60583-x. View

Kalinowski R, Berlot C, Jones T, Ross L, Jaffe L, Mehlmann L . Maintenance of meiotic prophase arrest in vertebrate oocytes by a Gs protein-mediated pathway. Dev Biol. 2004; 267(1):1-13. DOI: 10.1016/j.ydbio.2003.11.011. View

Sadler S, Maller J . Inhibition of Xenopus oocyte adenylate cyclase by progesterone: a novel mechanism of action. Adv Cyclic Nucleotide Protein Phosphorylation Res. 1985; 19:179-94. View

Cork R, Taylor M, Varnold R, Smith L, Robinson K . Microinjected GTP-gamma-S inhibits progesterone-induced maturation of Xenopus oocytes. Dev Biol. 1990; 141(2):447-50. DOI: 10.1016/0012-1606(90)90399-4. View

Sadler S, Maller J, Cooper D . Progesterone inhibition of Xenopus oocyte adenylate cyclase is not mediated via the Bordetella pertussis toxin substrate. Mol Pharmacol. 1984; 26(3):526-31. View

Campioni N, Beccari E, Bozzoni I, Amaldi F . Expression of ribosomal-protein genes in Xenopus laevis development. Cell. 1982; 30(1):163-71. DOI: 10.1016/0092-8674(82)90022-8. View

Mehlmann L . Oocyte-specific expression of Gpr3 is required for the maintenance of meiotic arrest in mouse oocytes. Dev Biol. 2005; 288(2):397-404. PMC: 1868506. DOI: 10.1016/j.ydbio.2005.09.030. View

Tang Y, Hu T, Arterburn M, Boyle B, Bright J, Emtage P . PAQR proteins: a novel membrane receptor family defined by an ancient 7-transmembrane pass motif. J Mol Evol. 2005; 61(3):372-80. DOI: 10.1007/s00239-004-0375-2. View

10.

Fredriksson R, Lagerstrom M, Lundin L, Schioth H . The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol. 2003; 63(6):1256-72. DOI: 10.1124/mol.63.6.1256. View

11.

Lutz L, Cole L, Gupta M, Kwist K, Auchus R, Hammes S . Evidence that androgens are the primary steroids produced by Xenopus laevis ovaries and may signal through the classical androgen receptor to promote oocyte maturation. Proc Natl Acad Sci U S A. 2001; 98(24):13728-33. PMC: 61109. DOI: 10.1073/pnas.241471598. View

12.

Tanaka S, Ishii K, Kasai K, Yoon S, Saeki Y . Neural expression of G protein-coupled receptors GPR3, GPR6, and GPR12 up-regulates cyclic AMP levels and promotes neurite outgrowth. J Biol Chem. 2007; 282(14):10506-15. DOI: 10.1074/jbc.M700911200. View

13.

Karaiskou A, Perez L, Ferby I, Ozon R, Jessus C, Nebreda A . Differential regulation of Cdc2 and Cdk2 by RINGO and cyclins. J Biol Chem. 2001; 276(38):36028-34. DOI: 10.1074/jbc.M104722200. View

14.

Romo X, Hinrichs M, Guzman L, Olate J . G(alpha)s levels regulate Xenopus laevis oocyte maturation. Mol Reprod Dev. 2002; 63(1):104-9. DOI: 10.1002/mrd.10150. View

15.

Lutz L, Kim B, Jahani D, Hammes S . G protein beta gamma subunits inhibit nongenomic progesterone-induced signaling and maturation in Xenopus laevis oocytes. Evidence for a release of inhibition mechanism for cell cycle progression. J Biol Chem. 2000; 275(52):41512-20. DOI: 10.1074/jbc.M006757200. View

16.

Tusnady G, Simon I . Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J Mol Biol. 1998; 283(2):489-506. DOI: 10.1006/jmbi.1998.2107. View

17.

Bagowski C, MYERS J, Ferrell Jr J . The classical progesterone receptor associates with p42 MAPK and is involved in phosphatidylinositol 3-kinase signaling in Xenopus oocytes. J Biol Chem. 2001; 276(40):37708-14. DOI: 10.1074/jbc.M104582200. View

18.

Gallo C, Hand A, Jones T, Jaffe L . Stimulation of Xenopus oocyte maturation by inhibition of the G-protein alpha S subunit, a component of the plasma membrane and yolk platelet membranes. J Cell Biol. 1995; 130(2):275-84. PMC: 2199928. DOI: 10.1083/jcb.130.2.275. View

19.

Norris R, Freudzon L, Freudzon M, Hand A, Mehlmann L, Jaffe L . A G(s)-linked receptor maintains meiotic arrest in mouse oocytes, but luteinizing hormone does not cause meiotic resumption by terminating receptor-G(s) signaling. Dev Biol. 2007; 310(2):240-9. PMC: 2311505. DOI: 10.1016/j.ydbio.2007.07.017. View

20.

Prossnitz E, Arterburn J, Sklar L . GPR30: A G protein-coupled receptor for estrogen. Mol Cell Endocrinol. 2007; 265-266:138-42. PMC: 1847610. DOI: 10.1016/j.mce.2006.12.010. View