Regulation of Meiotic Prophase Arrest in Mouse Oocytes by GPR3, a Constitutive Activator of the Gs G Protein

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2005 Oct 26

PMID 16247026

Citations 50

Authors

Leon Freudzon

Rachael P Norris

Arthur R Hand

Shigeru Tanaka

Yoshinaga Saeki

Teresa L Z Jones

Mark M Rasenick

Catherine H Berlot

Lisa M Mehlmann

Laurinda A Jaffe

Affiliations

Soon will be listed here.

Abstract

The arrest of meiotic prophase in mouse oocytes within antral follicles requires the G protein G(s) and an orphan member of the G protein-coupled receptor family, GPR3. To determine whether GPR3 activates G(s), the localization of Galpha(s) in follicle-enclosed oocytes from Gpr3(+/+) and Gpr3(-/-) mice was compared by using immunofluorescence and Galpha(s)GFP. GPR3 decreased the ratio of Galpha(s) in the oocyte plasma membrane versus the cytoplasm and also decreased the amount of Galpha(s) in the oocyte. Both of these properties indicate that GPR3 activates G(s). The follicle cells around the oocyte are also necessary to keep the oocyte in prophase, suggesting that they might activate GPR3. However, GPR3-dependent G(s) activity was similar in follicle-enclosed and follicle-free oocytes. Thus, the maintenance of prophase arrest depends on the constitutive activity of GPR3 in the oocyte, and the follicle cell signal acts by a means other than increasing GPR3 activity.

Citing Articles

Exploring orphan GPCRs in neurodegenerative diseases.

Oz-Arslan D, Yavuz M, Kan B Front Pharmacol. 2024; 15:1394516.

PMID: 38895631 PMC: 11183337. DOI: 10.3389/fphar.2024.1394516.

Rare variants in GPR3 in POI patients: a case series with review of literature.

Ren S, Zhang F, Shang L, Yang X, Pan Y, Zhang X J Ovarian Res. 2023; 16(1):210.

PMID: 37919810 PMC: 10623876. DOI: 10.1186/s13048-023-01282-3.

Unraveling the Puzzle: Oocyte Maturation Abnormalities (OMAS).

Hatirnaz S, Hatirnaz E, Celik S, Soyer Caliskan C, Tinelli A, Malvasi A Diagnostics (Basel). 2022; 12(10).

PMID: 36292190 PMC: 9601227. DOI: 10.3390/diagnostics12102501.

Neurotransmitters, neuropeptides and calcium in oocyte maturation and early development.

Alhajeri M, Alkhanjari R, Hodeify R, Khraibi A, Hamdan H Front Cell Dev Biol. 2022; 10:980219.

PMID: 36211465 PMC: 9537470. DOI: 10.3389/fcell.2022.980219.

G protein-biased GPR3 signaling ameliorates amyloid pathology in a preclinical Alzheimer's disease mouse model.

Huang Y, Guimaraes T, Todd N, Ferguson C, Weiss K, Stauffer F Proc Natl Acad Sci U S A. 2022; 119(40):e2204828119.

PMID: 36161942 PMC: 9546571. DOI: 10.1073/pnas.2204828119.

References

Conti M, Andersen C, Richard F, Mehats C, Chun S, Horner K . Role of cyclic nucleotide signaling in oocyte maturation. Mol Cell Endocrinol. 2002; 187(1-2):153-9. DOI: 10.1016/s0303-7207(01)00686-4. View

Wedegaertner P, Bourne H, von Zastrow M . Activation-induced subcellular redistribution of Gs alpha. Mol Biol Cell. 1996; 7(8):1225-33. PMC: 275974. DOI: 10.1091/mbc.7.8.1225. View

Masciarelli S, Horner K, Liu C, Park S, Hinckley M, Hockman S . Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J Clin Invest. 2004; 114(2):196-205. PMC: 449752. DOI: 10.1172/JCI21804. View

Schultz R, Montgomery R, Belanoff J . Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev Biol. 1983; 97(2):264-73. DOI: 10.1016/0012-1606(83)90085-4. View

Duckworth B, Weaver J, Ruderman J . G2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A. Proc Natl Acad Sci U S A. 2002; 99(26):16794-9. PMC: 139223. DOI: 10.1073/pnas.222661299. View

Thiyagarajan M, Bigras E, Van Tol H, Hebert T, Evanko D, Wedegaertner P . Activation-induced subcellular redistribution of G alpha(s) is dependent upon its unique N-terminus. Biochemistry. 2002; 41(30):9470-84. DOI: 10.1021/bi025533u. View

Tsafriri A, Channing C . An inhibitory influence of granulosa cells and follicular fluid upon porcine oocyte meiosis in vitro. Endocrinology. 1975; 96(4):922-7. DOI: 10.1210/endo-96-4-922. View

Wedegaertner P, Bourne H . Activation and depalmitoylation of Gs alpha. Cell. 1994; 77(7):1063-70. DOI: 10.1016/0092-8674(94)90445-6. View

Iiri T, Farfel Z, Bourne H . Conditional activation defect of a human Gsalpha mutant. Proc Natl Acad Sci U S A. 1997; 94(11):5656-61. PMC: 20834. DOI: 10.1073/pnas.94.11.5656. View

10.

PINCUS G, Enzmann E . THE COMPARATIVE BEHAVIOR OF MAMMALIAN EGGS IN VIVO AND IN VITRO : I. THE ACTIVATION OF OVARIAN EGGS. J Exp Med. 2009; 62(5):665-75. PMC: 2133299. DOI: 10.1084/jem.62.5.665. View

11.

Webb R, Marshall F, Swann K, Carroll J . Follicle-stimulating hormone induces a gap junction-dependent dynamic change in [cAMP] and protein kinase a in mammalian oocytes. Dev Biol. 2002; 246(2):441-54. DOI: 10.1006/dbio.2002.0630. View

12.

Nijenhuis W, Oosterom J, Adan R . AgRP(83-132) acts as an inverse agonist on the human-melanocortin-4 receptor. Mol Endocrinol. 2001; 15(1):164-71. DOI: 10.1210/mend.15.1.0578. View

13.

Eppig J, Coleman D . Hypoxanthine and adenosine in murine ovarian follicular fluid: concentrations and activity in maintaining oocyte meiotic arrest. Biol Reprod. 1985; 33(5):1041-9. DOI: 10.1095/biolreprod33.5.1041. View

14.

Moravcova Z, Rudajev V, Stohr J, Novotny J, cerny J, Parenti M . Long-term agonist stimulation of IP prostanoid receptor depletes the cognate G(s)alpha protein in membrane domains but does not change the receptor level. Biochim Biophys Acta. 2004; 1691(1):51-65. DOI: 10.1016/j.bbamcr.2003.12.004. View

15.

Mehlmann L . Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction. 2005; 130(6):791-9. DOI: 10.1530/rep.1.00793. View

16.

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

17.

Eggerickx D, Denef J, Labbe O, Hayashi Y, Refetoff S, Vassart G . Molecular cloning of an orphan G-protein-coupled receptor that constitutively activates adenylate cyclase. Biochem J. 1995; 309 ( Pt 3):837-43. PMC: 1135708. DOI: 10.1042/bj3090837. View

18.

Aida T, Oda S, Awaji T, Yoshida K, Miyazaki S . Expression of a green fluorescent protein variant in mouse oocytes by injection of RNA with an added long poly(A) tail. Mol Hum Reprod. 2001; 7(11):1039-46. DOI: 10.1093/molehr/7.11.1039. View

19.

Huang C, Duncan J, GILMAN A, Mumby S . Persistent membrane association of activated and depalmitoylated G protein alpha subunits. Proc Natl Acad Sci U S A. 1999; 96(2):412-7. PMC: 15150. DOI: 10.1073/pnas.96.2.412. View

20.

Ransnas L, Svoboda P, Jasper J, Insel P . Stimulation of beta-adrenergic receptors of S49 lymphoma cells redistributes the alpha subunit of the stimulatory G protein between cytosol and membranes. Proc Natl Acad Sci U S A. 1989; 86(20):7900-3. PMC: 298179. DOI: 10.1073/pnas.86.20.7900. View