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Reproductive Biology and Endocrinology

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Open Access 01-12-2010 | Research

Mammalian oocytes are targets for prostaglandin E2 (PGE2) action

Authors: Diane M Duffy, Lynda K McGinnis, Catherine A VandeVoort, Lane K Christenson

Published in: Reproductive Biology and Endocrinology | Issue 1/2010

Abstract

Background

The ovulatory gonadotropin surge increases synthesis of prostaglandin E2 (PGE2) by the periovulatory follicle. PGE2 actions on granulosa cells are essential for successful ovulation. The aim of the present study is to determine if PGE2 also acts directly at the oocyte to regulate periovulatory events.

Methods

Oocytes were obtained from monkeys and mice after ovarian follicular stimulation and assessed for PGE2 receptor mRNA and proteins. Oocytes were cultured with vehicle or PGE2 and assessed for cAMP generation, resumption of meiosis, and in vitro fertilization.

Results

Germinal vesicle intact (GV) oocytes from both monkeys and mice expressed mRNA for the PGE2 receptors EP2, EP3, and EP4. EP2 and EP4 proteins were detected by confocal microscopy in oocytes of both species. Monkey and mouse oocytes responded to PGE2 as well as agonists selective for EP2 and EP4 receptors with elevated cAMP, consistent with previous identification of EP2 and EP4 as Gαs/adenylyl cyclase coupled receptors. Incubation of mouse GV stage oocytes with PGE2 delayed oocyte nuclear maturation in vitro, but PGE2 treatment did not alter the percentage of mouse oocytes that fertilized successfully. PGE2 treatment also decreased the percentage of monkey oocytes that resumed meiosis in vitro. In contrast with mouse oocytes, the percentage of monkey oocytes which fertilized in vitro was lower after treatment with PGE2. Monkey oocytes with intact cumulus showed delayed nuclear maturation, but fertilization rate was not affected by PGE2 treatment.

Conclusions

Monkey and mouse oocytes express functional PGE2 receptors. PGE2 acts directly at mammalian oocytes to delay nuclear maturation. Surrounding cumulus cells modulate the effect of PGE2 to alter subsequent fertilization.

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Duffy DM, Stouffer RL: The ovulatory gonadotrophin surge stimulates cyclooxygenase expression and prostaglandin production by the monkey follicle. Molecular Human Reproduction. 2001, 7: 731-739. 10.1093/molehr/7.8.731.CrossRefPubMed

Tsafriri A, Reich R: Molelcular aspects of mammalian ovulation. Experimental and Clinical Endocrinology and Diabetes. 1999, 107: 1-11. 10.1055/s-0029-1212066.CrossRefPubMed

Duffy DM, Stouffer RL: Follicular administration of a cyclooxygenase inhibitor can prevent oocyte release without alteration of normal luteal function in rhesus monkeys. Human Reproduction. 2002, 17: 2825-2831. 10.1093/humrep/17.11.2825.CrossRefPubMed

Sogn JH, Curry TE, Brannstrom M, Lemaire WJ, Koos RD, Papkoff H, Janson PO: Inhibition of follicle-stimulating hormone-induced ovulation by indomethacin in the perfused rat ovary. Biology of Reproduction. 1987, 36: 536-542. 10.1095/biolreprod36.3.536.CrossRefPubMed

Hizaki H, Segi E, Sugimoto Y, Hirose M, Saji T, Ushikubi F, Matsuoka T, Noda Y, Tanaka T, Yoshida N: Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP 2. Proceedings of the National Academy of Sciences, USA. 1999, 96: 10501-10506. 10.1073/pnas.96.18.10501.CrossRef

Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, Dey SK: Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell. 1997, 91: 197-208. 10.1016/S0092-8674(00)80402-X.CrossRefPubMed

Narumiya S, Sugimoto T, Ushikubi F: Prostanoid receptors: structures, properties, and functions. Physiological Reviews. 1999, 79: 1193-1226.PubMed

Markosyan N, Dozier BL, Lattanzio FA, Duffy DM: Primate granulosa cell response via prostaglandin E2 receptors increases late in the periovulatory interval. Biology of Reproduction. 2006, 75: 868-876. 10.1095/biolreprod.106.053769.CrossRefPubMed

Segi E, Haraguchi K, Sugimoto Y, Tsuji M, Tsunekawa H, Tamba S, Tsuboi K, Tanaka S, Ichikawa A: Expression of messenger RNA for prostaglandin E receptor subtypes EP4/EP2 and cyclooxygenase isozymes in mouse periovulatory follicles and oviducts during superovulation. Biology of Reproduction. 2003, 68: 804-811. 10.1095/biolreprod.102.003590.CrossRefPubMed

10.

Takahashi T, Morrow JD, Wang H, Dey SK: Cyclooxygenase-2 derived prostaglandin E2 directs oocyte maturation by differentially influencing multiple signaling pathways. The Journal of Biological Chemistry. 2006, 281: 37117-37129. 10.1074/jbc.M608202200.CrossRefPubMed

11.

Markosyan N, Duffy DM: Prostaglandin E2 acts via multiple receptors to regulate plasminogen-dependent proteolysis in the primate periovulatory follicle. Endocrinology. 2009, 150: 435-444. 10.1210/en.2008-0591.PubMedCentralCrossRefPubMed

12.

Calder MD, Caveney AN, Sirard MA, Watson AJ: Effect of serum and cumulus cell expansion on marker gene transcripts in bovine cumulus-oocyte complexes during maturation in vitro. Fertility and Sterility. 2005, 83: 1077-1085. 10.1016/j.fertnstert.2004.12.012.CrossRefPubMed

13.

Duffy DM, Dozier BL, Seachord CL: Prostaglandin dehydrogenase (PGDH) and prostaglandin levels in periovulatory follicles: Implications for control of primate ovulation by PGE2. Journal of Clinical Endocrinology and Metabolism. 2005, 90: 1021-1027. 10.1210/jc.2004-1229.CrossRefPubMed

14.

Wolf DP, Alexander M, Zelinski-Wooten MB, Stouffer RL: Maturity and fertility of rhesus monkey oocytes collected at different intervals after an ovulatory stimulus (human chorionic gonadotropin) in in vitro fertilization cycles. Molecular Reproduction and Development. 1996, 43: 76-81. 10.1002/(SICI)1098-2795(199601)43:1<76::AID-MRD10>3.0.CO;2-2.CrossRefPubMed

15.

Van de Velde H, Nagy ZP, Joris H, De Vos A, Van Steirteghem AC: Effects of different hyaluronidase concentrations and mechanical procedures for cumulus cell removal on the outcome of intracytoplasmic injection. Human Reproduction. 1997, 12: 2246-2250. 10.1093/humrep/12.10.2246.CrossRefPubMed

16.

Nyholt de Prada JK, VandeVoort CA: Growth hormone and in vitro maturation of rhesus macaque oocytes and subsequent embryo development. Journal of Assisted Reproduction and Genetics. 2008, 25: 145-158. 10.1007/s10815-008-9208-3.PubMedCentralCrossRef

17.

Sarason RL, VandeVoort CA, Mader DR, Overstreet JW: The use of nonmetal electrodes in electroejaculation of restrained by unanesthetized macaques. Journal of Medical Primatology. 1991, 20: 122-125.PubMed

18.

Dong Q, Rodenburg SE, Huang C, VandeVoort CA: Effect of prefreezing conditions on semen cryopreservation of rhesus monkey. Theriogenology. 2008, 70: 61-66. 10.1016/j.theriogenology.2008.02.008.PubMedCentralCrossRefPubMed

19.

Chaffin CL, Stouffer RL: Expression of matrix metalloproteinases and their tissue inhibitor messenger ribonucleic acids in macaque periovulatory granulosa cells: Time course and steroid regulation. Biology of Reproduction. 1999, 61: 14-21. 10.1095/biolreprod61.1.14.CrossRefPubMed

20.

Patsoula E, Loutradis D, Drakakis P, Kallianidis K, Bletsa R, Michalas S: Expression of mRNA for the LH and FSH receptors in mouse oocytes and preimplantation embryos. Reproduction. 2001, 121: 455-461. 10.1530/rep.0.1210455.CrossRefPubMed

21.

Dong Q, Correa LC, VandeVoort CA: Rhesus monkey sperm cryopreservation with TEST-yolk extender in the absence of permeable cryoprotectant. Cryobiology. 2009, 58: 20-27. 10.1016/j.cryobiol.2008.09.014.PubMedCentralCrossRefPubMed

22.

Schramm RD, Paprocki AM, VandeVoort CA: Causes of developmental failure of in-vitro matured rhesus monkey oocytes: Impairment in embryonic genome activation. Human Reproduction. 2003, 18: 826-833. 10.1093/humrep/deg144.CrossRefPubMed

23.

McGinnis LK, Kinsey WH, Albertini DF: Functions of fyn kinase in the completion of meiosis in mouse oocytes. Developmental Biology. 2009, 327: 280-287. 10.1016/j.ydbio.2008.11.038.PubMedCentralCrossRefPubMed

24.

McGinnis LK, Albertini DF: Dynamics of protein phosphorylation during meiotic maturation. Journal of Assisted Reproduction and Genetics. 2010, 27: 169-182. 10.1007/s10815-010-9391-x.PubMedCentralCrossRefPubMed

25.

Summers MC, McGinnis LK, Lawitts JA, Biggers JD: Mouse embryo development following IVF in media containing either L-glutamine or glycyl-L-glutamine. Human Reproduction. 2005, 20: 1364-1371. 10.1093/humrep/deh756.CrossRefPubMed

26.

Schroeder AC, Schultz RM, Kopf GS, Taylor FR, Becker RB, Eppig JJ: Fetuin inhibits zona pellucida hardening and conversion of ZP2 to ZP2f during spontaneous mouse oocyte maturation in vitro in the absence of serum. Biology of Reproduction. 1990, 43: 891-897. 10.1095/biolreprod43.5.891.CrossRefPubMed

27.

Spiro RG: Studies on fetuin, a glycoprotein in fetal serum. I. Isolation, chemical composition, and physiochemical properties. The Journal of Biological Chemistry. 1960, 235: 2860-2869.PubMed

28.

McGinnis LK, Albertini DF, Kinsey WH: Localized activation of Src-family protein kinases in the mouse egg. Developmental Biology. 2007, 306: 241-254. 10.1016/j.ydbio.2007.03.024.PubMedCentralCrossRefPubMed

29.

Fiedler SD, Carletti MZ, Hong X, Christenson LK: Hormonal regulation of micro RNA expression in periovulatory mouse mural granulosa cells. Biology of Reproduction. 2008, 79: 1030-1037. 10.1095/biolreprod.108.069690.PubMedCentralCrossRefPubMed

30.

Yin H, Duffy DM, Gosden RG: Comparative maturation of cynomolgus monkey oocytes in vivo and in vitro. Reproductive Biology and Endocrinology. 2006, 4: 14-10.1186/1477-7827-4-14.PubMedCentralCrossRefPubMed

31.

Narko K, Saukkonen K, Ketola I, Butzow R, Heikinheimo K, Ristimaki A: Regulated expression of prostaglandin E2 receptors EP2 and EP4 in human ovarian granulosa-luteal cells. Journal of Clinical Endocrinology and Metabolism. 2001, 86: 1765-1768. 10.1210/jc.86.4.1765.CrossRefPubMed

32.

Bridges PJ, Komar CM, Fortune JE: Gonadotropin-induced expression of messenger ribonucleic acid for cyclooxygenase-2 and production of prostaglandins E and F2α in bovine preovulatory follicles are regulated by the progesterone receptor. Endocrinology. 2006, 147: 4713-4722. 10.1210/en.2005-1575.CrossRefPubMed

33.

Steinberg SF, Brunton LL: Compartmentation of G protein-coupled signaling pathways in cardiac myocytes. Annual Review of Pharmacology and Toxicology. 2001, 41: 751-773. 10.1146/annurev.pharmtox.41.1.751.CrossRefPubMed

34.

Grigsby PL, Sooranna SR, Adu-Amankwa B, Pitzer B, Brockman DE, Johnson MR, Myatt L: Regional expression of prostaglandin E2 and F2alpha receptors in human myometrium, amnion, and choriodecidua with advancing gestation and labor. Biology of Reproduction. 2006, 75: 297-305. 10.1095/biolreprod.106.051987.CrossRefPubMed

35.

Vivarelli E, Conti M, De Felici M, Siracusa G: Meiosic resumption and intracellular cAMP levels in mouse oocytes treated with compounds which act on cAMP metabolism. Cell Differentiation. 1983, 12: 271-276. 10.1016/0045-6039(83)90023-4.CrossRefPubMed

36.

Bilodeau S, Fortier MA, Sirard MA: Effect of adenylate cyclase stimulation on meiotic resumption and cyclic AMP content of zona-free and cumulus-enclosed bovine oocytes in vitro. Journal of Reproduction and Fertility. 1993, 97: 5-11. 10.1530/jrf.0.0970005.CrossRefPubMed

37.

DiLuigi A, Weitzman VN, Pace MC, Siano LJ, Maier D, Mehlmann LM: Meiotic arrest in human oocytes is maintained by a Gs singaling pathway. Biology of Reproduction. 2008, 78: 667-672. 10.1095/biolreprod.107.066019.PubMedCentralCrossRefPubMed

38.

Mehlmann LM, Saeki Y, Tanaka S, Brennan TJ, Evsikov AV, Pendola FL, Knowles BB, Eppig JJ, Jaffe LA: The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science. 2004, 306: 1947-1950. 10.1126/science.1103974.CrossRefPubMed

39.

Conti M, Andersen CB, Richard F, Mehats C, Chun SY, Horner K, Jin C, Tsafriri A: Role of cyclic nucleotide signaling in oocyte maturation. Molecular and Cellular Endocrinology. 2002, 187: 153-159. 10.1016/S0303-7207(01)00686-4.CrossRefPubMed

40.

Sela-Abramovich S, Edry I, Galiani D, Nevo N, Dekel N: Disruption of gap junctional communication within the ovarian follicle induces oocyte maturation. Endocrinology. 2006, 147: 2280-2286. 10.1210/en.2005-1011.CrossRefPubMed

41.

Mehlmann LM: Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction. 2005, 130: 791-799. 10.1530/rep.1.00793.CrossRefPubMed

42.

Wong WYL, Richards JS: Evidence for two antigenically distinct molecular weight variants of prostaglandin H synthase in the rat ovary. Molecular Endocrinology. 1991, 5: 1269-1279. 10.1210/mend-5-9-1269.CrossRefPubMed

43.

Sirois J: Induction of prostaglandin endoperoxide synthase-2 by human chorionic gonadotropin in bovine preovulatory follicles in vivo. Endocrinology. 1994, 135: 841-848. 10.1210/en.135.3.841.PubMed

44.

Sirois J, Dore M: The late induction of prostaglandin G/H synthase-2 in equine preovulatory follicles supports its role as a determinant of the ovulatory process. Endocrinology. 1997, 138: 4427-4434. 10.1210/en.138.10.4427.PubMed

Title: Mammalian oocytes are targets for prostaglandin E2 (PGE2) action
Authors: Diane M Duffy
Lynda K McGinnis
Catherine A VandeVoort
Lane K Christenson
Publication date: 01-12-2010
Publisher: BioMed Central
Published in: Reproductive Biology and Endocrinology / Issue 1/2010
Electronic ISSN: 1477-7827
DOI: https://doi.org/10.1186/1477-7827-8-131

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Mammalian oocytes are targets for prostaglandin E2 (PGE2) action

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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