Although the involvement of the extracellular signal-regulated kinases 1 and 2 (ERK1/2) pathway in the regulation of cytostatic factor (CSF) activity; as well as in microtubules organization during meiotic maturation of oocytes; has already been described in detail; rather less attention has been paid to the role of ERK1/2 in the regulation of mRNA translation. However; important data on the role of ERK1/2 in translation during oocyte meiosis have been documented. This review focuses on recent findings regarding the regulation of translation and the role of ERK1/2 in this process in the meiotic cycle of mammalian oocytes. The specific role of ERK1/2 in the regulation of mammalian target of rapamycin (mTOR); eukaryotic translation initiation factor 4E (eIF4E) and cytoplasmic polyadenylation element binding protein 1 (CPEB1) activity is addressed along with additional focus on the other key players involved in protein translation.

Department of Cell Biology Faculty of Science Charles University Prague Albertov 6 12843 Prague 2 Czech Republic

Institute of Animal Physiology and Genetics Academy of Sciences of the Czech Republic Rumburska 89 27721 Libechov Czech Republic

Zobrazit více v PubMed

Tanaka M., Kihara M., Hennebold J.D., Eppig J.J., Viveiros M.M., Emery B.R., Carrell D.T., Kirkman N.J., Meczekalski B., Zhou J., et al. H1FOO is coupled to the initiation of oocytic growth. Biol. Reprod. 2005;72:135–142. doi: 10.1095/biolreprod.104.032474. PubMed DOI

Alizadeh Z., Kageyama S.I., Aoki F. Degradation of maternal mRNA in mouse embryos: Selective degradation of specific mRNAs after fertilization. Mol. Reprod. Dev. 2005;72:281–290. doi: 10.1002/mrd.20340. PubMed DOI

Chen J., Melton C., Suh N., Oh J.S., Horner K., Xie F., Sette C., Blelloch R., Conti M. Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Genes Dev. 2011;25:755–766. doi: 10.1101/gad.2028911. PubMed DOI PMC

Sheets M.D., Fox C.A., Hunt T., Vande Woude G., Wickens M. The 3′-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev. 1994;8:926–938. doi: 10.1101/gad.8.8.926. PubMed DOI

Richter J.D., Lasko P. Translational control in oocyte development. Cold Spring Harb. Perspect. Biol. 2011;3:a002758. doi: 10.1101/cshperspect.a002758. PubMed DOI PMC

Clarke H.J. Mouse Development. Volume 55. Springer; Berlin/Heidelberg, Germany: 2012. pp. 1–21. DOI

Hamatani T., Daikoku T., Wang H., Matsumoto H., Carter M.G., Ko M.S.H., Dey S.K. Global gene expression analysis identifies molecular pathways distinguishing blastocyst dormancy and activation. Proc. Natl. Acad. Sci. USA. 2004;101:10326–10331. doi: 10.1073/pnas.0402597101. PubMed DOI PMC

Mehlmann L.M. Stops and starts in mammalian oocytes: Recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction. 2005;130:791–799. doi: 10.1530/rep.1.00793. PubMed DOI

Piqué M., López J.M., Foissac S., Guigó R., Méndez R. A Combinatorial Code for CPE-Mediated Translational Control. Cell. 2008;132:434–448. doi: 10.1016/j.cell.2007.12.038. PubMed DOI

Gosden R., Lee B. Portrait of an oocyte: Our obscure origin. J. Clin. Investig. 2010;120:973–983. doi: 10.1172/JCI41294. PubMed DOI PMC

Chen J., Torcia S., Xie F., Lin C.J., Cakmak H., Franciosi F., Horner K., Onodera C., Song J.S., Cedars M.I., et al. Somatic cells regulate maternal mRNA translation and developmental competence of mouse oocytes. Nat. Cell Biol. 2013;15:1415–1423. doi: 10.1038/ncb2873. PubMed DOI PMC

Piccioni F., Zappavigna V., Verrotti A.C. Translational regulation during oogenesis and early development: The cap-poly(A) tail relationship. C. R. Biol. 2005;328:863–881. doi: 10.1016/j.crvi.2005.05.006. PubMed DOI

Barkoff A.F., Dickson K.S., Gray N.K., Wickens M. Translational control of cyclin B1 mRNA during meiotic maturation: Coordinated repression and cytoplasmic polyadenylation. Dev. Biol. 2000;220:97–109. doi: 10.1006/dbio.2000.9613. PubMed DOI

Gorbsky G.J. The spindle checkpoint and chromosome segregation in meiosis. FEBS J. 2015;282:2471–2487. doi: 10.1111/febs.13166. PubMed DOI PMC

Schultz G.A., Clough J.R., Johnson M.H. Presence of cap structures in the messenger RNA of mouse eggs. Development. 1980;56:139–156. PubMed

Radford H.E., Meijer H.A., de Moor C.H. Translational control by cytoplasmic polyadenylation in Xenopus oocytes. Biochim. Biophys. Acta (BBA) Gene Regul. Mech. 2008;1779:217–229. doi: 10.1016/j.bbagrm.2008.02.002. PubMed DOI PMC

Brook M., Smith J.W.S., Gray N.K. The DAZL and PABP families: RNA-binding proteins with interrelated roles in translational control in oocytes. Reproduction. 2009;137:595–617. doi: 10.1530/REP-08-0524. PubMed DOI

Kyriakis J.M., Avruch J. Mammalian MAPK Signal Transduction Pathways Activated by Stress and Inflammation: A 10-Year Update. Physiol. Rev. 2012;92:689–737. doi: 10.1152/physrev.00028.2011. PubMed DOI

Peti W., Page R. Molecular basis of MAP kinase regulation. Protein Sci. 2013;22:1698–1710. doi: 10.1002/pro.2374. PubMed DOI PMC

Liu Y., Shepherd E.G., Nelin L.D. MAPK phosphatases—Regulating the immune response. Nat. Rev. Immunol. 2007;7:202–212. doi: 10.1038/nri2035. PubMed DOI

Arthur J.S.C., Ley S.C. Mitogen-activated protein kinases in innate immunity. Nat. Rev. Immunol. 2013;13:679–692. doi: 10.1038/nri3495. PubMed DOI

Johnson G.L. Defining MAPK interactomes. ACS Chem. Biol. 2011;6:18–20. doi: 10.1021/cb100384z. PubMed DOI

Pimienta G., Pascual J. Canonical and alternative MAPK signalling. Cell Cycle. 2007;6:2628–2632. doi: 10.4161/cc.6.21.4930. PubMed DOI

Chen Z., Cobb M.H. Regulation of stress-responsive mitogen-activated protein (MAP) kinase pathways by TAO2. J. Biol. Chem. 2001;276:16070–16075. doi: 10.1074/jbc.M100681200. PubMed DOI

Pearson G., Robinson F., Beers Gibson T., Xu B., Karandikar M., Berman K., Cobb M.H. Mitogen-Activated Protein (MAP) Kinase Pathways: Regulation and Physiological Functions. Endocr. Rev. 2001;22:153–183. doi: 10.1210/er.22.2.153. PubMed DOI

Owens D.M., Keyse S.M. Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene. 2007;26:3203–3213. doi: 10.1038/sj.onc.1210412. PubMed DOI

Johnson G.L., Nakamura K. The c-jun kinase/stress-activated pathway: Regulation, function and role in human disease. Biochim. Biophys. Acta (BBA) Mol. Cell Res. 2007;1773:1341–1348. doi: 10.1016/j.bbamcr.2006.12.009. PubMed DOI PMC

Shaul Y.D., Seger R. The MEK/ERK cascade: From signalling specificity to diverse functions. Biochim. Biophys. Acta (BBA) Mol. Cell Res. 2007;1773:1213–1226. doi: 10.1016/j.bbamcr.2006.10.005. PubMed DOI

Knight T., Irving J.A.E. Ras/Raf/MEK/ERK Pathway Activation in Childhood Acute Lymphoblastic Leukemia and Its Therapeutic Targeting. Front. Oncol. 2014;4:1–12. doi: 10.3389/fonc.2014.00160. PubMed DOI PMC

Roskoski R. ERK1/2 MAP kinases: Structure, function, and regulation. Pharmacol. Res. 2012;66:105–143. doi: 10.1016/j.phrs.2012.04.005. PubMed DOI

Gaestel M. MAPK-Activated Protein Kinases (MKs): Novel Insights and Challenges. Front. Cell Dev. Biol. 2016;3:1–6. doi: 10.3389/fcell.2015.00088. PubMed DOI PMC

Anjum R., Blenis J. The RSK family of kinases: Emerging roles in cellular signalling. Nat. Rev. Mol. Cell Biol. 2008;9:747–758. doi: 10.1038/nrm2509. PubMed DOI

Waskiewicz A.J., Flynn A., Proud C.G., Cooper J.A. Mitogen-activated protein kinases activate the serine/threonine kinaseses Mnk1 and Mnk2. EMBO J. 1997;16:1909–1920. doi: 10.1093/emboj/16.8.1909. PubMed DOI PMC

Roux P.P., Topisirovic I. Regulation of mRNA translation by signalling pathways. Cold Spring Harb. Perspect. Biol. 2012;4:1–24. doi: 10.1101/cshperspect.a012252. PubMed DOI PMC

Buxade M., Morrice N., Krebs D.L., Proud C.G. The PSF·p54nrb complex is a novel Mnk substrate that binds the mRNA for tumor necrosis factor α. J. Biol. Chem. 2008;283:57–65. doi: 10.1074/jbc.M705286200. PubMed DOI

Scheper G.C., Morrice N.A., Kleijn M., Proud C.G. The Mitogen-Activated Protein Kinase Signal-Integrating Kinase Mnk2 Is a Eukaryotic Initiation Factor 4E Kinase with High Levels of Basal Activity in Mammalian Cells The Mitogen-Activated Protein Kinase Signal-Integrating Kinase Mnk2 Is a Eukaryotic Initi. Mol. Cell. Biol. 2001;21:743–754. doi: 10.1128/MCB.21.3.743-754.2001. PubMed DOI PMC

Andreou A.Z., Harms U., Klostermeier D. eIF4B stimulates eIF4A ATPase and unwinding activities by direct interaction through its 7-repeats region. RNA Biol. 2017;14:113–123. doi: 10.1080/15476286.2016.1259782. PubMed DOI PMC

Magnuson B., Ekim B., Fingar D.C. Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem. J. 2012;441:1–21. doi: 10.1042/BJ20110892. PubMed DOI

Sonenberg N., Hinnebusch A.G. Regulation of Translation Inition in Eukaryotes: Mechanisms and Biological Targrts. Cell. 2013;136:731–745. doi: 10.1016/j.cell.2009.01.042. PubMed DOI PMC

Gotoh Y., Masuyama N., Dell K., Shirakabe K., Nishida E. Initiation of Xenopus oocyte maturation by activation of the mitogen-activated protein kinase cascade. J Biol. Chem. 1995;270:25898–25904. doi: 10.1074/jbc.270.43.25898. PubMed DOI

Kubelka M., Anger M., Kalous J., Schultz R.M., Motlík J. Chromosome condensation in pig oocytes: Lack of a requirement for either cdc2 kinase or MAP kinase activity. Mol. Reprod. Dev. 2002;63:110–118. doi: 10.1002/mrd.10176. PubMed DOI

Kalous J., Kubelka M., Motlík J. The effect of PD98059 on MAPK regulation in cumulus-enclosed and cumulus-free mouse oocytes. Zygote. 2003;11:61–68. doi: 10.1017/S0967199403001084. PubMed DOI

Fan H.-Y., Sun Q.-Y. Involvement of Mitogen-Activated Protein Kinase Cascade During Oocyte Maturation and Fertilization in Mammals1. Biol. Reprod. 2004;70:535–547. doi: 10.1095/biolreprod.103.022830. PubMed DOI

Zhang Y.L., Liu X.M., Ji S.Y., Sha Q.Q., Zhang J., Fan H.Y. ERK1/2 Activities Are Dispensable for Oocyte Growth but Are Required for Meiotic Maturation and Pronuclear Formation in Mouse. J. Genet. Genom. 2015;42:477–485. doi: 10.1016/j.jgg.2015.07.004. PubMed DOI

Verlhac M.H., Kubiak J.Z., Weber M., Géraud G., Colledge W.H., Evans M.J., Maro B. Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development. 1996;122:815–822. PubMed

Paronetto M.P., Giorda E., Carsetti R., Rossi P., Geremia R., Sette C. Functional interaction between p90Rsk2 and Emi1 contributes to the metaphase arrest of mouse oocytes. EMBO J. 2004;23:4649–4659. doi: 10.1038/sj.emboj.7600448. PubMed DOI PMC

Lefebvre C., Emilie Terret M., Djiane A., Rassinier P., Maro B., Verlhac M.H. Meiotic spindle stability depends on MAPK-interacting and spindle-stabilizing protein (MISS), a new MAPK substrate. J. Cell Biol. 2002;157:603–613. doi: 10.1083/jcb.200202052. PubMed DOI PMC

Terret M.E. DOC1R: A MAP kinase substrate that control microtubule organization of metaphase II mouse oocytes. Development. 2003;130:5169–5177. doi: 10.1242/dev.00731. PubMed DOI

Schmidt A. Cytostatic factor: An activity that puts the cell cycle on hold. J. Cell Sci. 2006;119:1213–1218. doi: 10.1242/jcs.02919. PubMed DOI

Posada J., Yew N., Ahn N.G., Vande Woude G.F., Cooper J.A. Mos stimulates MAP kinase in Xenopus oocytes and activates a MAP kinase kinase in vitro. Mol. Cell. Biol. 1993;13:2546–2553. doi: 10.1128/MCB.13.4.2546. PubMed DOI PMC

Hashimoto N., Watanabe N., Furuta Y., Tamemoto H., Sagata N., Yokoyama M., Okazaki K., Nagayoshi M., Takeda N., Ikawa Y., et al. Parthenogenetic activation of c-mos mice. Nature. 1994;370:68–71. doi: 10.1038/370068a0. PubMed DOI

Choi T., Rulong S., Resau J., Fukasawa K., Matten W., Kuriyama R., Mansour S., Ahn N., Vande Woude G.F. Mos/mitogen-activated protein kinase can induce early meiotic phenotypes in the absence of maturation-promoting factor: A novel system for analyzing spindle formation during meiosis I. Proc. Natl. Acad. Sci. USA. 1996;93:4730–4735. doi: 10.1073/pnas.93.10.4730. PubMed DOI PMC

Gross S.D., Lewellyn A.L., Maller J.L. A Constitutively Active Form of the Protein Kinase p90Rsk1 Is Sufficient to Trigger the G2/M Transition in Xenopus Oocytes. J. Biol. Chem. 2001;276:46099–46103. doi: 10.1074/jbc.C100496200. PubMed DOI

Bhatt R.R., Ferrell J.E., Jr. The Protein Kinase p90 Rsk as an Essential Mediator of Cytostatic Factor Activity. Science. 2016;286:1362–1365. doi: 10.1126/science.286.5443.1362. PubMed DOI

Zachariae W., Nasmyth K. Whose end is destruction: Cell division and the anaphase- promoting complex. Genes Dev. 1999;13:2039–2058. doi: 10.1101/gad.13.16.2039. PubMed DOI

Prinz S., Hwang E.S., Visintin R., Amon A. The regulation of Cdc20 proteolysis reveals a role for the APC components Cdc23 and Cdc27 during S phase and early mitosis. Curr. Biol. 1998;8:750–760. doi: 10.1016/S0960-9822(98)70298-2. PubMed DOI

Fang G., Yu H., Kirschner M.W. The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation. Genes Dev. 1998;12:1871–1883. doi: 10.1101/gad.12.12.1871. PubMed DOI PMC

Vanoosthuyse V., Valsdottir R., Javerzat J.-P., Hardwick K.G. Kinetochore targeting of fission yeast Mad and Bub proteins is essential for spindle checkpoint function but not for all chromosome segregation roles of Bub1p. Mol. Cell. Biol. 2004;24:9786–9801. doi: 10.1128/MCB.24.22.9786-9801.2004. PubMed DOI PMC

Maller J.L., Schwab M.S., Gross S.D., Taieb F.E., Roberts B.T., Tunquist B.J. The mechanism of CSF arrest in vertebrate oocytes. Mol. Cell. Endocrinol. 2002;187:173–178. doi: 10.1016/S0303-7207(01)00695-5. PubMed DOI

Schwab M.S., Roberts B.T., Gross S.D., Tunquist B.J., Taieb F.E., Lewellyn A.L., Maller J.L. Bub1 is activated by the protein kinase p90(Rsk) during Xenopus oocyte maturation. Curr. Biol. 2001;11:141–150. doi: 10.1016/S0960-9822(01)00045-8. PubMed DOI

Ni H., Sheng X., Cui X., Gu M., Liu Y., Qi X., Xing S., Guo Y. Epidermal growth factor-mediated mitogen-activated protein Kinase3/1 pathway is conducive to in vitro maturation of sheep oocytes. PLoS ONE. 2015;10:e0120418. doi: 10.1371/journal.pone.0120418. PubMed DOI PMC

Ebeling S., Labudda A., Meinecke B. In vitro ageing of porcine oocytes: Changes in phosphorylation of the mitogen-activated protein kinase (MAPK) and parthenogenetic activability. Reprod. Domest. Anim. 2010;45:398–404. doi: 10.1111/j.1439-0531.2010.01588.x. PubMed DOI

Ma W., Zhang D., Hou Y., Li Y.-H., Sun Q.-Y., Sun X.-F., Wang W.-H. Reduced expression of MAD2, BCL2, and MAP kinase activity in pig oocytes after in vitro aging are associated with defects in sister chromatid segregation during meiosis II and embryo fragmentation after activation. Biol. Reprod. 2005;72:373–383. doi: 10.1095/biolreprod.104.030999. PubMed DOI

Sun S.C., Xiong B., Lu S.S., Sun Q.Y. MEK1/2 is a critical regulator of microtubule assembly and spindle organization during rat oocyte meiotic maturation. Mol. Reprod. Dev. 2008;75:1542–1548. doi: 10.1002/mrd.20891. PubMed DOI

Miyagaki Y., Kanemori Y., Baba T. Possible involvement of mitogen- and stress-activated protein kinase 1, MSK1, in metaphase-II arrest through phosphorylation of EMI2 in mouse oocytes. Dev. Biol. 2011;359:73–81. doi: 10.1016/j.ydbio.2011.08.021. PubMed DOI

Tiwari M., Gupta A., Sharma A., Prasad S., Pandey A.N., Yadav P.K., Pandey A.K., Shrivastav T.G., Chaube S.K. Role of Mitogen Activated Protein Kinase and Maturation Promoting Factor During the Achievement of Meiotic Competency in Mammalian Oocytes. J. Cell. Biochem. 2018;119:123–129. doi: 10.1002/jcb.26184. PubMed DOI

Suzuki T., Suzuki E., Yoshida N., Kubo A., Li H., Okuda E., Amanai M., Perry A.C.F. Mouse Emi2 as a distinctive regulatory hub in second meiotic metaphase. Development. 2010;137:3281–3291. doi: 10.1242/dev.052480. PubMed DOI PMC

Munroe D., Jacobson A. mRNA poly(A) tail, a 3′ enhancer of translational initiation. Mol. Cell. Biol. 1990;10:3441–3455. doi: 10.1128/MCB.10.7.3441. PubMed DOI PMC

Richter J.D., Sonenberg N. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature. 2005;433:477–480. doi: 10.1038/nature03205. PubMed DOI

Mendez R., Hake L.E., Andresson T., Littlepage L.E., Ruderman J.V., Richter J.D. Phosphorylation of CPE binding factor by Eg2 regulates translation of c- mos mRNA. Nature. 2000;404:302–307. doi: 10.1038/35005126. PubMed DOI

Gingras A., Raught B., Sonenberg N. eIF4 Initiation Factors: Effectors of mRNA Recruitment to Ribosomes and Regulators. Annu. Rev. Biochem. 1999;68:913–963. doi: 10.1146/annurev.biochem.68.1.913. PubMed DOI

Pyronnet S., Imataka H., Gingras A.C., Fukunaga R., Hunter T., Sonenberg N. Human eukaryotic translation initiation factor 4G (eIF4G) recruits Mnk1 to phosphorylate eIF4E. EMBO J. 1999;18:270–279. doi: 10.1093/emboj/18.1.270. PubMed DOI PMC

Harms U., Andreou A.Z., Gubaev A., Klostermeier D. EIF4B, eIF4G and RNA regulate eIF4A activity in translation initiation by modulating the eIF4A conformational cycle. Nucleic Acids Res. 2014;42:7911–7922. doi: 10.1093/nar/gku440. PubMed DOI PMC

Etchison D., Milburn S.C., Edery I., Sonenberg N., Hershey J.W. Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotc initiation factor 3 and a cap binding protein complex. J. Biol. Chem. 1982;257:14806–14810. PubMed

Pain V.M. Initiation of protein synthesis in eukaryotic cells. Eur. J. Biochem. 1996;236:747–771. doi: 10.1111/j.1432-1033.1996.00747.x. PubMed DOI

Méthot N., Song M.S., Sonenberg N. A region rich in aspartic acid, arginine, tyrosine, and glycine (DRYG) mediates eukaryotic initiation factor 4B (eIF4B) self-association and interaction with eIF3. Mol. Cell. Biol. 1996;16:5328–5334. doi: 10.1128/MCB.16.10.5328. PubMed DOI PMC

Vornlocher H., Hanachi P., Ribeiro S. A 110-Kilodalton Subunit of Translation Initiation Factor eIF3 and an Associated 135-kilodalton Protein Are Encoded by theSaccharomyces cerevisiae TIF32 and TIF31Genes. J. Biol. Chem. 1999;274:16802–16812. doi: 10.1074/jbc.274.24.16802. PubMed DOI

Pause A., Belsham G.J., Gingras A.-C., Donzé O., Lin T.-A., Lawrence J.C., Sonenberg N. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature. 1994;371:762–767. doi: 10.1038/371762a0. PubMed DOI

Josse L., Xie J., Proud C.G., Smales C.M. mTORC1 signalling and eIF4E/4E-BP1 translation initiation factor stoichiometry influence recombinant protein productivity from GS-CHOK1 cells. Biochem. J. 2016;473:4651–4664. doi: 10.1042/BCJ20160845. PubMed DOI PMC

Gingras A.C., Raught B., Gygi S.P., Niedzwiecka A., Miron M., Burley S.K., Polakiewicz R.D., Wyslouch-Cieszynska A., Aebersold R., Sonenberg N. Hierarchical phosphorylation of the translation inhibitor 4E-BP1. Genes Dev. 2001;15:2852–2864. doi: 10.1101/gad.912401. PubMed DOI PMC

Vander Haar E., Lee S.I., Bandhakavi S., Griffin T.J., Kim D.H. Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat. Cell Biol. 2007;9:316–323. doi: 10.1038/ncb1547. PubMed DOI

Marcotrigiano J., Gingras A.C., Sonenberg N., Burley S.K. Cocrystal Structure of the Messenger RNA 5′ Cap-Binding Protein (eIF4E) Bound to 7-methyl-GDP. Cell. 1997;89:951–961. doi: 10.1016/S0092-8674(00)80280-9. PubMed DOI

Matsuo H., Li H., McGuire A.M., Mark Fletcher C., Gingras A.C., Sonenberg N., Wagner G. Structure of translation factor elF4E bound to m7GDP and interaction with 4E-binding protein. Nat. Struct. Biol. 1997;4:717–724. doi: 10.1038/nsb0997-717. PubMed DOI

Scheper G.C., Proud C.G. Does phosphorylation of the cap-binding protein eIF4E play a role in translation initiation? Eur. J. Biochem. 2002;269:5350–5359. doi: 10.1046/j.1432-1033.2002.03291.x. PubMed DOI PMC

Slepenkov S.V., Darzynkiewicz E., Rhoads R.E. Stopped-flow kinetic analysis of eIF4E and phosphorylated eIF4E binding to cap analogs and capped oligoribonucleotides: Evidence for a one-step binding mechanism. J. Biol. Chem. 2006;281:14927–14938. doi: 10.1074/jbc.M601653200. PubMed DOI

Morley S.J., Naegele S. Phosphorylation of eukaryotic initiation factor (eIF) 4E is not required for de novo protein synthesis following recovery from hypertonic stress in human kidney cells. J. Biol. Chem. 2002;277:32855–32859. doi: 10.1074/jbc.C200376200. PubMed DOI

Zuberek J., Jemielity J., Jablonowska A., Stepinski J., Dadlez M., Stolarski R., Darzynkiewicz E. Influence of Electric Charge Variation at Residues 209 and 159 on the Interaction of eIF4E with the mRNA 5′ Terminus. Biochemistry. 2004;43:5370–5379. doi: 10.1021/bi030266t. PubMed DOI

Dowling R., Topisirovic I., Alain T., Bidinosti M. mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs Supplemental data. Science. 2010;328:1172–1176. doi: 10.1126/science.1187532. PubMed DOI PMC

Thoreen C.C., Chantranupong L., Keys H.R., Wang T., Gray N.S., Sabatini D.M. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature. 2012;485:109–113. doi: 10.1038/nature11083. PubMed DOI PMC

Walsh D., Mohr I. Coupling 40S ribosome recruitment to modification of a cap-binding initiation factor by eIF3 subunit e. Genes Dev. 2014;28:835–840. doi: 10.1101/gad.236752.113. PubMed DOI PMC

Naegele S., Morley S.J. Molecular cross-talk between MEK1/2 and mTOR signalling during recovery of 293 cells from hypertonic stress. J. Biol. Chem. 2004;279:46023–46034. doi: 10.1074/jbc.M404945200. PubMed DOI

McGrew L.L., Dworkin-Rastl E., Dworkin M.B., Richter J.D. Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev. 1989;3:803–815. doi: 10.1101/gad.3.6.803. PubMed DOI

Fox C.A., Sheets M.D., Wickens M.P. Poly(A) addition during maturation of frog oocytes: Distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU. Genes Dev. 1989;3:2151–2162. doi: 10.1101/gad.3.12b.2151. PubMed DOI

Paris J., Swenson K., Piwnica-Worms H., Richter J.D. Maturation-specific polyadenylation: In vitro activation by p34(cdc2) and phosphorylation of a 58-kD CPE-binding protein. Genes Dev. 1991;5:1697–1708. doi: 10.1101/gad.5.9.1697. PubMed DOI

Hake L.E., Richter J.D. CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell. 1994;79:617–627. doi: 10.1016/0092-8674(94)90547-9. PubMed DOI

Mendez R., Barnard D., Richter J.D. Differential mRNA translation and meiotic progression require Cdc2-mediated CPEB destruction. EMBO J. 2002;21:1833–1844. doi: 10.1093/emboj/21.7.1833. PubMed DOI PMC

Hodgman R., Tay J., Mendez R., Richter J.D. CPEB phosphorylation and cytoplasmic polyadenylation are catalyzed by the kinase IAK1/Eg2 in maturing mouse oocytes. Development. 2001;128:2815–2822. PubMed

Tomek W., Wollenhaupt K. The “closed loop model” in controlling mRNA translation during development. Anim. Reprod. Sci. 2012;134:2–8. doi: 10.1016/j.anireprosci.2012.08.005. PubMed DOI

Siemer C., Smiljakovic T., Bhojwani M., Leiding C., Kanitz W., Kubelka M., Tomek W. Analysis of mRNA associated factors during bovine oocyte maturation and early embryonic development. Mol. Reprod. Dev. 2009;76:1208–1219. doi: 10.1002/mrd.21096. PubMed DOI

Ellederova Z., Kovarova H., Melo-Sterza F., Livingstone M., Tomek W., Kubelka M. Suppression of translation during in vitro maturation of pig oocytes despite enhanced formation of cap-binding protein complex eIF4F and 4E-BP1 hyperphosphorylation. Mol. Reprod. Dev. 2006;73:68–76. doi: 10.1002/mrd.20368. PubMed DOI

Tomek W., Melo Sterza F.A., Kubelka M., Wollenhaupt K., Torner H., Anger M., Kanitz W. Regulation of translation during in vitro maturation of bovine oocytes: The role of MAP kinase, eIF4E (cap binding protein) phosphorylation, and eIF4E-BP1. Biol. Reprod. 2002;66:1274–1282. doi: 10.1095/biolreprod66.5.1274. PubMed DOI

Susor A., Jansova D., Cerna R., Danylevska A., Anger M., Toralova T., Malik R., Supolikova J., Cook M.S., Oh J.S., et al. Temporal and spatial regulation of translation in the mammalian oocyte via the mTOR-eIF4F pathway. Nat. Commun. 2015;6:1–12. doi: 10.1038/ncomms7078. PubMed DOI PMC

Jansova D., Koncicka M., Tetkova A., Cerna R., Malik R., del Llano E., Kubelka M., Susor A. Regulation of 4E-BP1 activity in the mammalian oocyte. Cell Cycle. 2017;16:927–939. doi: 10.1080/15384101.2017.1295178. PubMed DOI PMC

Šušor A., Jelínková L., Karabínová P., Torner H., Tomek W., Kovářová H., Kubelka M. Regulation of cap-dependent translation initiation in the early stage porcine parthenotes. Mol. Reprod. Dev. 2008;75:1716–1725. doi: 10.1002/mrd.20913. PubMed DOI

Mayer S., Wrenzycki C., Tomek W. Inactivation of mTor arrests bovine oocytes in the metaphase-I stage, despite reversible inhibition of 4E-BP1 phosphorylation. Mol. Reprod. Dev. 2014;81:363–375. doi: 10.1002/mrd.22305. PubMed DOI

Severance A.L., Latham K.E. PLK1 regulates spindle association of phosphorylated eukaryotic translation initiation factor 4E binding protein, and spindle function in mouse oocytes. Am. J. Physiol. Cell Physiol. 2017;313:C501–C515. doi: 10.1152/ajpcell.00075.2017. PubMed DOI PMC

Lapasset L., Pradet-Balade B., Vergé V., Lozano J.C., Oulhen N., Cormier P., Peaucellier G. Cyclin B synthesis and rapamycin-sensitive regulation of protein synthesis during starfish oocyte meiotic divisions. Mol. Reprod. Dev. 2008;75:1617–1626. doi: 10.1002/mrd.20905. PubMed DOI

Ma X.M., Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 2009;10:307–318. doi: 10.1038/nrm2672. PubMed DOI

Fukunaga R., Hunter T. MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J. 1997;16:1921–1933. doi: 10.1093/emboj/16.8.1921. PubMed DOI PMC

Messina V., Di Sauro A., Pedrotti S., Adesso L., Latina A., Geremia R., Rossi P., Sette C. Differential contribution of the MTOR and MNK pathways to the regulation of mRNA translation in meiotic and postmeiotic mouse male germ cells. Biol. Reprod. 2010;83:607–615. doi: 10.1095/biolreprod.110.085050. PubMed DOI

Li Y., Yue P., Deng X., Ueda T., Fukunaga R., Khuri F.R., Sun S.-Y. Protein Phosphatase 2A Negatively Regulates Eukaryotic Initiation Factor 4E Phosphorylation and eIF4F Assembly through Direct Dephosphorylation of Mnk and eIF4E. Neoplasia. 2010;12:848–855. doi: 10.1593/neo.10704. PubMed DOI PMC

Shveygert M., Kaiser C., Bradrick S.S., Gromeier M. Regulation of Eukaryotic Initiation Factor 4E (eIF4E) Phosphorylation by Mitogen-Activated Protein Kinase Occurs through Modulation of Mnk1-eIF4G Interaction. Mol. Cell. Biol. 2010;30:5160–5167. doi: 10.1128/MCB.00448-10. PubMed DOI PMC

Ellederová Z., Cais O., Šušor A., Uhlířová K., Kovářová H., Jelínková L., Tomek W., Kubelka M. ERK1/2 map kinase metabolic pathway is responsible for phosphorylation of translation initiation factor eIF4E during in vitro maturation of pig oocytes. Mol. Reprod. Dev. 2008;75:309–317. doi: 10.1002/mrd.20690. PubMed DOI

Brook M., Gray N.K. The role of mammalian poly(A)-binding proteins in co-ordinating mRNA turnover. Biochem. Soc. Trans. 2012;40:856–864. doi: 10.1042/BST20120100. PubMed DOI PMC

Ivshina M., Lasko P., Richter J.D. Cytoplasmic Polyadenylation Element Binding Proteins in Development, Health, and Disease. Annu. Rev. Cell Dev. Biol. 2014;30:393–415. doi: 10.1146/annurev-cellbio-101011-155831. PubMed DOI

Huarte J., Stutz A., O’Connell M.L., Gubler P., Belin D., Darrow A.L., Strickland S., Vassalli J.D. Transient translational silencing by reversible mRNA deadenylation. Cell. 1992;69:1021–1030. doi: 10.1016/0092-8674(92)90620-R. PubMed DOI

Nishimura Y., Kano K., Naito K. Porcine CPEB1 is involved in Cyclin B translation and meiotic resumption in porcine oocytes. Anim. Sci. J. 2010;81:444–452. doi: 10.1111/j.1740-0929.2010.00755.x. PubMed DOI

Kim J.H., Richter J.D. Opposing Polymerase-Deadenylase Activities Regulate Cytoplasmic Polyadenylation. Mol. Cell. 2006;24:173–183. doi: 10.1016/j.molcel.2006.08.016. PubMed DOI

Fernández-Miranda G., Méndez R. The CPEB-family of proteins, translational control in senescence and cancer. Ageing Res. Rev. 2012;11:460–472. doi: 10.1016/j.arr.2012.03.004. PubMed DOI

de Moor C.H., Richter J.D. The Mos pathway regulates cytoplasmic polyadenylation in Xenopus oocytes. Mol. Cell. Biol. 1997;17:6419–6426. doi: 10.1128/MCB.17.11.6419. PubMed DOI PMC

Brunet S., Dumont J., Lee K.W., Kinoshita K., Hikal P., Gruss O.J., Maro B., Verlhac M.H. Meiotic regulation of TPX2 protein levels governs cell cycle progression in mouse oocytes. PLoS ONE. 2008;3:e3338. doi: 10.1371/journal.pone.0003338. PubMed DOI PMC

Yu C., Ji S.Y., Sha Q.Q., Dang Y., Zhou J.J., Zhang Y.L., Liu Y., Wang Z.W., Hu B., Sun Q.Y., et al. BTG4 is a meiotic cell cycle-coupled maternal-zygotic-transition licensing factor in oocytes. Nat. Struct. Mol. Biol. 2016;23:387–394. doi: 10.1038/nsmb.3204. PubMed DOI

Setoyama D., Yamashita M., Sagata N. Mechanism of degradation of CPEB during Xenopus oocyte maturation. Proc. Natl. Acad. Sci. USA. 2007;104:18001–18006. doi: 10.1073/pnas.0706952104. PubMed DOI PMC

Keady B.T., Kuo P., Martínez S.E., Yuan L., Hake L.E. MAPK interacts with XGef and is required for CPEB activation during meiosis in Xenopus oocytes. J. Cell Sci. 2007;120:1093–1103. doi: 10.1242/jcs.03416. PubMed DOI

Komrskova P., Susor A., Malik R., Prochazkova B., Liskova L., Supolikova J., Hladky S., Kubelka M. Aurora kinase A is not involved in CPEB1 phosphorylation and cyclin B1 mRNA polyadenylation during meiotic maturation of porcine oocytes. PLoS ONE. 2014;9 doi: 10.1371/journal.pone.0101222. PubMed DOI PMC

Sha Q.-Q., Dai X.-X., Dang Y., Tang F., Liu J., Zhang Y.-L., Fan H.-Y. A MAPK cascade couples maternal mRNA translation and degradation to meiotic cell cycle progression in mouse oocytes. Development. 2017;144:452–463. doi: 10.1242/dev.144410. PubMed DOI

Mulner-Lorillon O., Chassé H., Morales J., Bellé R., Cormier P. MAPK/ERK activity is required for the successful progression of mitosis in sea urchin embryos. Dev. Biol. 2017;421:194–203. doi: 10.1016/j.ydbio.2016.11.018. PubMed DOI

Kracmarova J. Role of MAPK in Regulation of Cytoplasmic Polyadenylation during Meiotic Maturation of Mammalian Oocytes. University Charles; Prague, Czech Republic: 2017.

Martins J.P.S., Liu X., Oke A., Arora R., Franciosi F., Viville S., Laird D.J., Fung J.C., Conti M. DAZL and CPEB1 regulate mRNA translation synergistically during oocyte maturation. J. Cell Sci. 2016;129:1271–1282. doi: 10.1242/jcs.179218. PubMed DOI PMC

Eberhart C.G., Maines J.Z., Wasserman S.A. Meiotic cell cycle requirement for a fly homologue of human deleted in Azoospermia. Nature. 1996;381:783–785. doi: 10.1038/381783a0. PubMed DOI

Ruggiu M., Speed R., Taggart M., McKay S.J., Kilanowski F., Saunders P., Dorin J., Cooke H.J. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature. 1997;389:73–77. doi: 10.1038/37987. PubMed DOI

Eckerdt F., Pascreau G., Phistry M., Lewellyn A.L., DePaoli-Roach A.A., Maller J.L. Phosphorylation of TPX2 by Plx1 enhances activation of Aurora A. Cell Cycle. 2009;8:2413–2419. doi: 10.4161/cc.8.15.9086. PubMed DOI

Helmke K.J., Heald R. TPX2 levels modulate meiotic spindle size and architecture in Xenopus egg extracts. J. Cell Biol. 2014;206:385–393. doi: 10.1083/jcb.201401014. PubMed DOI PMC

Bianchini A., Loiarro M., Bielli P., Busà R., Paronetto M.P., Loreni F., Geremia R., Sette C. Phosphorylation of eIF4E by MNKs supports protein synthesis, cell cycle progression and proliferation in prostate cancer cells. Carcinogenesis. 2008;29:2279–2288. doi: 10.1093/carcin/bgn221. PubMed DOI

Schlessinger J. Cell Signaling by Receptor Tyrosine Kinases A large group of genes in all eukaryotes encode for. October. 2000;103:211–225. doi: 10.1016/j.cell.2010.06.011. PubMed DOI

Karar J., Maity A. PI3K/AKT/mTOR Pathway in Angiogenesis. Front. Mol. Neurosci. 2011;4:1–8. doi: 10.3389/fnmol.2011.00051. PubMed DOI PMC

Mendoza M.C., Er E.E., Blenis J. The Ras-ERK and PI3K-mTOR pathways: Cross-talk and compensation. TRENDS Biochem. Sci. 2011;36:320–328. doi: 10.1016/j.tibs.2011.03.006. PubMed DOI PMC

Lehr S., Kotzka J., Avci H., Sickmann A., Meyer H.E., Herkner A., Muller-Wieland D. Identification of major ERK-related phosphorylation sites in Gab1. Biochemistry. 2004;43:12133–12140. doi: 10.1021/bi049753e. PubMed DOI

Rodriguez-Viciana P., Warne P.H., Dhand R., Vanhaesebroeck B., Gout I., Fry M.J., Waterfield M.D., Downward J. Phosphatidylinositol-3-OH kinase direct target of Ras. Nature. 1994;370:527–532. doi: 10.1038/370527a0. PubMed DOI

Dhillon A.S., Meikle S., Yazici Z., Eulitz M., Kolch W. Regulation of Raf-1 activation and signalling by dephosphorylation. EMBO J. 2002;21:64–71. doi: 10.1093/emboj/21.1.64. PubMed DOI PMC

Nakdimon I., Walser M., Fröhli E., Hajnal A. PTEN Negatively Regulates MAPK Signaling during Caenorhabditis elegans Vulval Development. PLoS Genet. 2012;8:1–10. doi: 10.1371/journal.pgen.1002881. PubMed DOI PMC

McKay M.M., Morrison D.K. Integrating signals from RTKs to ERK/MAPK. Oncogene. 2007;26:3113–3121. doi: 10.1038/sj.onc.1210394. PubMed DOI

Fissore R.A., He C.L., Vande Woude G.F. Potential role of mitogen-activated protein kinase during meiosis resumption in bovine oocytes. Biol. Reprod. 1996;55:1261–1270. doi: 10.1095/biolreprod55.6.1261. PubMed DOI

Duncan F.E., Jasti S., Paulson A., Kelsh J.M., Fegley B., Gerton J.L. Age-associated dysregulation of protein metabolism in the mammalian oocyte. Aging Cell. 2017;16:1381–1393. doi: 10.1111/acel.12676. PubMed DOI PMC

Chao J.A., Yoon Y.J., Singer R.H. Imaging translation in single cells using fluorescent microscopy. Cold Spring Harb. Perspect. Biol. 2012;4:1–12. doi: 10.1101/cshperspect.a012310. PubMed DOI PMC

Romasko E.J., Amarnath D., Midic U., Latham K.E. Association of maternal mRNA and phosphorylated EIF4EBP1 variants with the spindle in mouse oocytes: Localized translational control supporting female meiosis in mammals. Genetics. 2013;195:349–358. doi: 10.1534/genetics.113.154005. PubMed DOI PMC

Guertin D.A., Sabatini D.M. Defining the Role of mTOR in Cancer. Cancer Cell. 2007;12:9–22. doi: 10.1016/j.ccr.2007.05.008. PubMed DOI

The translational oscillation in oocyte and early embryo development

Impact of Global Transcriptional Silencing on Cell Cycle Regulation and Chromosome Segregation in Early Mammalian Embryos