Dynamic expression of Epac and Rap1 in mouse oocytes and preimplantation embryos

Wang,Jun‑Chao; Geng,Ying; Han,Ying; Luo,Hai‑Ning; Zhang,Yun‑Shan

doi:10.3892/etm.2018.6253

Dynamic expression of Epac and Rap1 in mouse oocytes and preimplantation embryos

Authors:
- Jun‑Chao Wang
- Ying Geng
- Ying Han
- Hai‑Ning Luo
- Yun‑Shan Zhang
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Affiliations: Center for Reproductive Medicine, Tianjin Central Hospital of Obstetrics and Gynaecology, Tianjin 300100, P.R. China
Published online on: June 6, 2018 https://doi.org/10.3892/etm.2018.6253
Pages: 523-528
Copyright: © Wang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Cyclic adenosine monophosphate (cAMP) is an important secondary messenger that has long been recognized to control the initiation of meiosis through the activation of protein kinase A (PKA) in mammalian oocytes. However, PKA is not the only target for cAMP. Recent studies on cAMP‑dependent and PKA‑independent pathways suggest that Ras‑related protein‑1 (Rap1) is activated through its cAMP‑responsive guanine exchange factors (cAMP‑GEFs), which comprises the involvement of exchange proteins directly activated by cAMP (Epac) in various cellular processes. The aim of the present study was to investigate the possible implication of a cAMP/Epac/Rap1 pathway in mouse oocytes and embryos. Reverse transcription polymerase chain reaction and immunohistochemistry assays demonstrated the expression of Epac and Rap1 in oocytes and embryos at different stages. Immunofluorescene demonstrated that Epac and Rap1 had different dynamic subcellular localizations and expression patterns in oocytes and embryos at different stages. It was therefore indicated that Epac and Rap1 may have multiple and specific functions during oocyte maturation and embryonic development.

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1	Conti M, Andersen CB, Richard F, Mehats C, Chun SY, Homer K, Jin C and Tsafriri A: Role of cyclic nucleotide signaling in oocyte maturation. Mol Cell Endocrinol. 187:153–159. 2002. View Article : Google Scholar : PubMed/NCBI
2	Eppig JJ, Vivieros MM, Marin-Bivens C and de La Fuente R: 2004, The Ovary. Leung PCK: &. Adashi EY: Elsevier, Academic Press; pp. 113–129, 2004. View Article : Google Scholar
3	Meijer L, Dostmann W, Genieser HG, Butt E and Jastorff B: Starfish oocyte maturation: Evidence for a cyclic AMP-dependent inhibitory pathway. Dev Biol. 133:58–66. 1989. View Article : Google Scholar : PubMed/NCBI
4	Jalabert G, Fostier A, Breton B and Weil Cin: Vertebrate Endocrinology: Fundamentals and Biomedical Implications. (Pang PKT &. Schreibman MP: 4A. New York; Academic Press; pp. 113–129. 1991
5	Chaube SK and Haider S: J Exp Zool. 277:166–170. 1997. View Article : Google Scholar
6	Josefberg LB and Dekel N: Translational and post-translational modifications in meiosis of the mammalian oocyte. Mol Cell Endocrinol. 187:161–171. 2002. View Article : Google Scholar : PubMed/NCBI
7	de Rooij J, Zwartkruis FJ, Verheijen MH, Cool RH, Nijman SM, Wittinghofer A and Bos JL: Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature. 396:474–477. 1998. View Article : Google Scholar : PubMed/NCBI
8	Kawasaki H, Springett GM, Mochizuki N, Toki S, Nakay M, Matsuda M, Houseman DE and Graybiel AM: A family of cAMP-binding proteins that directly activate Rap1. Science. 282:2275–2279. 1998. View Article : Google Scholar : PubMed/NCBI
9	Schmitt A and Nebreda AR: Inhibition of xenopus oocyte meiotic maturation by catalytically inactive protein kinase a. Proc Natl Acad Sci USA. 99:4361–4366. 2002. View Article : Google Scholar : PubMed/NCBI
10	Pace MC and Thomas P: Steroid-induced oocyte maturation in Atlantic croaker (Micropogonias undulatus) is dependent on activation of the phosphatidylinositol 3-kinase/Akt signal transduction pathway. Biol Reprod. 73:988–996. 2005. View Article : Google Scholar : PubMed/NCBI
11	Brennesvik EO, Ktori C, Ruzzin J, Jebens E, Shepherd PR and Jensen J: Adrenaline potentiates insulin-stimulated PKB activation via cAMP and Epac: Implications for cross talk between insulin and adrenaline. Cell Signal. 17:1551–1559. 2005. View Article : Google Scholar : PubMed/NCBI
12	Hucho TB, Dina OA and Levine JD: Epac mediates a cAMP-to-PKC signaling in inflammatory pain: An isolectin B4(+) neuron-specific mechanism. J Neurosci. 25:6119–6126. 2005. View Article : Google Scholar : PubMed/NCBI
13	Branham MT, Mayorga LS and Tomes CN: Calcium-induced acrosomal exocytosis requires cAMP acting through a protein kinase A-independent, Epac-mediated pathway. J Biol Chem. 281:8656–8666. 2006. View Article : Google Scholar : PubMed/NCBI
14	Robert S: Regulation of the amyloid precursor protein ectodomain shedding by the 5-HT4 receptor and Epac. FEBS Lett. 579:1136–1142. 2005. View Article : Google Scholar : PubMed/NCBI
15	Rangarajan S, Enserink JM, Kuiperij HB, de Rooij J, Price LS, Schwede F and Bos JL: Cyclic AMP induces integrin-mediated cell adhesion through Epac and Rap1 upon stimulation of the beta 2-adrenergic receptor. J Cell Biol. 160:487–493. 2003. View Article : Google Scholar : PubMed/NCBI
16	Fukuhara S, Sakurai A, Sano H, Yamagishi A, Somekawa S, Takakura N, Saito Y, Kangawa K and Mochizuki N: Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol Cell Biol. 25:136–146. 2005. View Article : Google Scholar : PubMed/NCBI
17	Kwon G, Pappan KL, Marshall CA, Schaffer JE and McDaniel ML: cAMP Dose-dependently prevents palmitate-induced apoptosis by both protein kinase A- and cAMP-guanine nucleotide exchange factor-dependent pathways in beta-cells. J Biol Chem. 279:8938–8945. 2004. View Article : Google Scholar : PubMed/NCBI
18	Misra UK and Pizzo SV: Coordinate regulation of forskolin-induced cellular proliferation in macrophages by protein kinase A/cAMP-response element-binding protein (CREB) and Epac1-Rap1 signaling: Effects of silencing CREB gene expression on Akt activation. J Biol Chem. 280:38276–38289. 2005. View Article : Google Scholar : PubMed/NCBI
19	Bryn T, Mahic M, Enserink JM, Schwede F, Aandahl EM and Tasken K: The cyclic AMP-Epac1-Rap1 pathway is dissociated from regulation of effector functions in monocytes but acquires immunoregulatory function in mature macrophages. J Immunol. 176:7361–7370. 2006. View Article : Google Scholar : PubMed/NCBI
20	Gonzalez-Robayna IJ, Falender AE, Ochsner S, Firestone GL and Richards JS: Follicle-Stimulating hormone (FSH) stimulates phosphorylation and activation of protein kinase B (PKB/Akt) and serum and glucocorticoid-lnduced kinase (Sgk): Evidence for A kinase-independent signaling by FSH in granulosa cells. Mol Endocrinol. 14:1283–1300. 2000. View Article : Google Scholar : PubMed/NCBI
21	Chin EC and Abayasekara DR: Progesterone secretion by luteinizing human granulosa cells: A possible cAMP-dependent but PKA-independent mechanism involved in its regulation. J Endocrinol. 183:51–60. 2004. View Article : Google Scholar : PubMed/NCBI
22	Beranger F, Goud B, Tavitian A and de Gunzburg J: Association of the Ras-antagonistic Rap1/Krev-1 proteins with the Golgi complex. Proc Natl Acad Sci. 88:1606–1610. 1991. View Article : Google Scholar : PubMed/NCBI
23	Maridonneau-Parini I and de Gunzburg J: Association of rap1 and rap2 proteins with the specific granules of human neutrophils Translocation to the plasma membrane during cell activation. J Biol Chem. 267:6396–6402. 1992.PubMed/NCBI
24	Zwartkruis FJ and Bos JL: Ras and Rap1: Two highly related small GTPases with distinct function. Exp Cell Res. 253:157–165. 1999. View Article : Google Scholar : PubMed/NCBI
25	Dodge-Kafka KL, Soughayer J, Pare GC, Carlisle Michel JJ, Langeberg LK, Kapiloff MS and Scott JD: The protein kinase A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature. 437:574–578. 2005. View Article : Google Scholar : PubMed/NCBI
26	Dekel N: Protein phosphorylation/dephosphorylation in the meiotic cell cycle of mammalian oocytes. Rev Reprod. 1:82–88. 1996. View Article : Google Scholar : PubMed/NCBI
27	Duckworth BC, Weaver JS and Ruderman JV: G2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A. Proc Natl Acad Sci USA. 99:16794–16799. 2002. View Article : Google Scholar : PubMed/NCBI
28	Choi T, Aoki F, Mori M, Yamashita M, Nagahama Y and Kohomoto K: Activation of p34cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development. 113:789–795. 1991.PubMed/NCBI
29	Verlhac MH, Kubiak JZ, Clarke HJ and Maro B: Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development. 120:1017–1025. 1994.PubMed/NCBI
30	Pincus G and Enzmann EV: The comparative behavior of mammalian eggs in vivo and in vitro: I. the activation of ovarian eggs. J Exp Med. 62:655–675. 1935.
31	Webb RJ, Marshall F, Swann K and Carroll J: Follicle-stimulating hormone induces a gap junction-dependent dynamic change in [cAMP] and protein kinase a in mammalian oocytes. Dev Biol. 246:441–451. 2002. View Article : Google Scholar : PubMed/NCBI
32	Webb RJ, Tinworth L, Thomas GM, Zaccolo M and Carroll J: Developmentally acquired PKA localisation in mouse oocytes and embryos. Dev Biol. 317:36–45. 2008. View Article : Google Scholar : PubMed/NCBI
33	Vossler MR, Yao H, York RD, Pan MG, Rim CS and Stork PJ: cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell. 89:73–82. 1997. View Article : Google Scholar : PubMed/NCBI
34	York RD, Yao H, Dillon T, Ellig CL, Eckert SP, McCleskey EW and Stork PJ: Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature. 392:622–626. 1998. View Article : Google Scholar : PubMed/NCBI
35	Sun QY, Breitbart H and Schatten H: Role of the MAPK cascade in mammalian germ cells. Reprod Fertil Dev. 11:443–450. 1999. View Article : Google Scholar : PubMed/NCBI
36	Fan HY and Sun QY: Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol Reprod. 70:535–547. 2004. View Article : Google Scholar : PubMed/NCBI
37	Araki K, Naito K, Haraguchi S, Suzuki R, Yokoyama M, Inoue M, Aizawa S, Toyoda Y and Sato E: Meiotic abnormalities of c-mos knockout mouse oocytes: Activation after first meiosis or entrance into third meiotic metaphase. Biol Reprod. 55:1315–1324. 1996. View Article : Google Scholar : PubMed/NCBI