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Post-transcriptional and post-translational regulation during mouse oocyte maturation

  • Received : 2011.01.31
  • Published : 2011.03.31

Abstract

The meiotic process from the primordial stage to zygote in female germ cells is mainly adjusted by post-transcriptional regulation of pre-existing maternal mRNA and post-translational modification of proteins. Several key proteins such as the cell cycle regulator, Cdk1/cyclin B, are post-translationally modified for precise control of meiotic progression. The second messenger (cAMP), kinases (PKA, Akt, MAPK, Aurora A, CaMK II, etc), phosphatases (Cdc25, Cdc14), and other proteins (G-protein coupled receptor, phosphodiesterase) are directly or indirectly involved in this process. Many proteins, such as CPEB, maskin, eIF4E, eIF4G, 4E-BP, and 4E-T, post-transcriptionally regulate mRNA via binding to the cap structure at the 5' end of mRNA or its 3' untranslated region (UTR) to generate a closed-loop structure. The 3' UTR of the transcript is also implicated in post-transcriptional regulation through an association with proteins such as CPEB, CPSF, GLD-2, PARN, and Dazl to modulate poly(A) tail length. RNA interfering is a new regulatory mechanism of the amount of mRNA in the mouse oocyte. This review summarizes information about post-transcriptional and post-translational regulation during mouse oocyte meiotic maturation.

Keywords

References

  1. Eppig, J. J. (1993) Regulation of mammalian oocyte maturation;in The Ovary, Adashi, E. Y. and Leung, P. C. K.(eds.), Raven Press, Ltd., New York, USA.
  2. Saitou, M., Barton, S. C. and Surani, M. A. (2002) A molecularprogramme for the specification of germ cell fatein mice. Nature 418, 293-300. https://doi.org/10.1038/nature00927
  3. Molyneaux, K. A., Stallock, J., Schaible, K. and Wylie, C.(2001) Time-lapse analysis of living mouse germ cellmigration. Dev. Biol. 240, 488-498. https://doi.org/10.1006/dbio.2001.0436
  4. Godin, I. and Wylie, C. C. (1991) TGF beta 1 inhibits proliferationand has a chemotropic effect on mouse primordialgerm cells in culture. Development 113, 1451-1457.
  5. Tsafriri, A., and Dekel, N. (eds.) (1994) Molecular mechanisms in ovulation. Academic Press, San Diego, USA.
  6. Bornslaeger, E. A., Mattei, P. and Schultz, R. M. (1986)Involvement of cAMP-dependent protein kinase and proteinphosphorylation in regulation of mouse oocytematuration. Dev. Biol. 114, 453-462. https://doi.org/10.1016/0012-1606(86)90209-5
  7. Maller, J. L. and Krebs, E. G. (1977) Progesterone-stimulatedmeiotic cell division in Xenopus oocytes. Inductionby regulatory subunit and inhibition by catalytic subunitof adenosine 3':5'-monophosphate-dependent protein kinase.J. Biol. Chem. 252, 1712-1718.
  8. Huchon, D., Ozon, R., Fischer, E. H. and Demaille, J. G.(1981) The pure inhibitor of cAMP-dependent protein kinaseinitiates Xenopus laevis meiotic maturation. A 4-stepscheme for meiotic maturation. Mol. Cell Endocrinol. 22,211-222. https://doi.org/10.1016/0303-7207(81)90092-7
  9. Conti, M., Andersen, C. B., Richard, F., Mehats, C., Chun,S. Y., Horner, K., Jin, C. and Tsafriri, A. (2002) Role of cyclicnucleotide signaling in oocyte maturation. Mol. CellEndocrinol. 187, 153-159. https://doi.org/10.1016/S0303-7207(01)00686-4
  10. Horner, K., Livera, G., Hinckley, M., Trinh, K., Storm, D.and Conti, M. (2003) Rodent oocytes express an active adenylylcyclase required for meiotic arrest. Dev. Biol. 258, 385-396. https://doi.org/10.1016/S0012-1606(03)00134-9
  11. Kalinowski, R. R., Berlot, C. H., Jones, T. L., Ross, L. F.,Jaffe, L. A. and Mehlmann, L. M. (2004) Maintenance ofmeiotic prophase arrest in vertebrate oocytes by a Gs protein-mediated pathway. Dev. Biol. 267, 1-13. https://doi.org/10.1016/j.ydbio.2003.11.011
  12. Mehlmann, L. M. (2005) Oocyte-specific expression ofGpr3 is required for the maintenance of meiotic arrest inmouse oocytes. Dev. Biol. 288, 397-404. https://doi.org/10.1016/j.ydbio.2005.09.030
  13. Mehlmann, L. M., Jones, T. L. and Jaffe, L. A. (2002)Meiotic arrest in the mouse follicle maintained by a Gsprotein in the oocyte. Science 297, 1343-1345. https://doi.org/10.1126/science.1073978
  14. Han, S. J., Chen, R., Paronetto, M. P. and Conti, M. (2005)Wee1B is an oocyte-specific kinase involved in the controlof meiotic arrest in the mouse. Curr. Biol. 15, 1670-1676. https://doi.org/10.1016/j.cub.2005.07.056
  15. Parker, L. L., Atherton-Fessler, S. and Piwnica-Worms, H.(1992) p107wee1 is a dual-specificity kinase that phosphorylatesp34cdc2 on tyrosine 15. Proc. Natl. Acad. Sci.U.S.A. 89, 2917-2921. https://doi.org/10.1073/pnas.89.7.2917
  16. Kaldis, P., Russo, A. A., Chou, H. S., Pavletich, N. P. andSolomon, M. J. (1998) Human and yeast cdk-activatingkinases (CAKs) display distinct substrate specificities. Mol.Biol. Cell 9, 2545-2560. https://doi.org/10.1091/mbc.9.9.2545
  17. Donzelli, M. and Draetta, G. F. (2003) Regulating mammaliancheckpoints through Cdc25 inactivation. EMBORep. 4, 671-677. https://doi.org/10.1038/sj.embor.embor887
  18. Duckworth, B. C., Weaver, J. S. and Ruderman, J. V.(2002) G2 arrest in Xenopus oocytes depends on phosphorylationof cdc25 by protein kinase A. Proc. Natl.Acad. Sci. U.S.A. 99, 16794-16799. https://doi.org/10.1073/pnas.222661299
  19. Pirino, G., Wescott, M. P. and Donovan, P. J. (2009)Protein kinase A regulates resumption of meiosis by phosphorylationof Cdc25B in mammalian oocytes. Cell Cycle8, 665-670. https://doi.org/10.4161/cc.8.4.7846
  20. Lincoln, A. J., Wickramasinghe, D., Stein, P., Schultz, R.M., Palko, M. E., De Miguel, M. P., Tessarollo, L. andDonovan, P. J. (2002) Cdc25b phosphatase is required forresumption of meiosis during oocyte maturation. Nat. Genet. 30, 446-449. https://doi.org/10.1038/ng856
  21. Shitsukawa, K., Andersen, C. B., Richard, F. J., Horner, A.K., Wiersma, A., van Duin, M. and Conti, M. (2001)Cloning and characterization of the cyclic guanosinemonophosphate-inhibited phosphodiesterase PDE3A expressedin mouse oocyte. Biol. Reprod. 65, 188-196. https://doi.org/10.1095/biolreprod65.1.188
  22. Matten, W., Daar, I. and Vande Woude, G. F. (1994)Protein kinase A acts at multiple points to inhibit Xenopusoocyte maturation. Mol. Cell Biol. 14, 4419-4426. https://doi.org/10.1128/MCB.14.7.4419
  23. Masciarelli, S., Horner, K., Liu, C., Park, S. H., Hinckley,M., Hockman, S., Nedachi, T., Jin, C., Conti, M. andManganiello, V. (2004) Cyclic nucleotide phosphodiesterase3A-deficient mice as a model of female infertility. J.Clin. Invest. 114, 196-205. https://doi.org/10.1172/JCI21804
  24. Han, S. J., Vaccari, S., Nedachi, T., Andersen, C. B.,Kovacina, K. S., Roth, R. A. and Conti, M. (2006) Proteinkinase B/Akt phosphorylation of PDE3A and its role inmammalian oocyte maturation. EMBO J. 25, 5716-5725. https://doi.org/10.1038/sj.emboj.7601431
  25. Peters, J. M. (2006) The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev.Mol. Cell Biol. 7, 644-656. https://doi.org/10.1038/nrm1988
  26. Pesin, J. A. and Orr-Weaver, T. L. (2008) Regulation ofAPC/C activators in mitosis and meiosis. Annu. Rev. CellDev. Biol. 24, 475-499. https://doi.org/10.1146/annurev.cellbio.041408.115949
  27. Jin, F., Hamada, M., Malureanu, L., Jeganathan, K. B.,Zhou, W., Morbeck, D. E. and van Deursen, J. M. (2010)Cdc20 is critical for meiosis I and fertility of female mice.PLoS Genet 6, e1001147. doi:10.1371/journal.pgen.1001147.
  28. Reis, A., Chang, H. Y., Levasseur, M. and Jones, K. T.(2006) APCcdh1 activity in mouse oocytes prevents entryinto the first meiotic division. Nat. Cell Biol. 8, 539-540. https://doi.org/10.1038/ncb1406
  29. Holt, J. E., Weaver, J. and Jones, K. T. (2010) Spatial regulationof APCCdh1-induced cyclin B1 degradation maintainsG2 arrest in mouse oocytes. Development 137,1297-1304. https://doi.org/10.1242/dev.047555
  30. Schindler, K. and Schultz, R. M. (2009) CDC14B actsthrough FZR1 (CDH1) to prevent meiotic maturation ofmouse oocytes. Biol. Reprod. 80, 795-803. https://doi.org/10.1095/biolreprod.108.074906
  31. Yew, N., Mellini, M. L. and Vande Woude, G. F. (1992)Meiotic initiation by the mos protein in Xenopus. Nature355, 649-652. https://doi.org/10.1038/355649a0
  32. Fulka, J., Jr., Motlik, J., Fulka, J. and Jilek, F. (1986) Effectof cycloheximide on nuclear maturation of pig and mouseoocytes. J. Reprod. Fertil. 77, 281-285. https://doi.org/10.1530/jrf.0.0770281
  33. Mendez, R. and Richter, J. D. (2001) Translational controlby CPEB: a means to the end. Nat. Rev. Mol. Cell Biol. 2,521-529. https://doi.org/10.1038/35080081
  34. Ule, J. and Darnell, R. B. (2006) RNA binding proteinsand the regulation of neuronal synaptic plasticity. Curr.Opin. Neurobiol. 16, 102-110. https://doi.org/10.1016/j.conb.2006.01.003
  35. Audic, Y. and Hartley, R. S. (2004) Post-transcriptionalregulation in cancer. Biol. Cell 96, 479-498. https://doi.org/10.1016/j.biolcel.2004.05.002
  36. Baroux, C., Autran, D., Gillmor, C. S., Grimanelli, D. andGrossniklaus, U. (2008) The maternal to zygotic transitionin animals and plants. Cold Spring Harb. Symp. Quant.Biol. 73, 89-100. https://doi.org/10.1101/sqb.2008.73.053
  37. Sonenberg, N. and Hinnebusch, A. G. (2009) Regulationof translation initiation in eukaryotes: mechanisms and biologicaltargets. Cell 136, 731-745. https://doi.org/10.1016/j.cell.2009.01.042
  38. Matsuo, H., Li, H., McGuire, A. M., Fletcher, C. M., Gingras, A. C., Sonenberg, N. and Wagner, G. (1997)Structure of translation factor eIF4E bound to m7GDP andinteraction with 4E-binding protein. Nat. Struct. Biol. 4,717-724. https://doi.org/10.1038/nsb0997-717
  39. Tschopp, C., Knauf, U., Brauchle, M., Zurini, M., Ramage,P., Glueck, D., New, L., Han, J. and Gram, H. (2000)Phosphorylation of eIF-4E on Ser 209 in response to mitogenicand inflammatory stimuli is faithfully detected byspecific antibodies. Mol. Cell Biol. Res. Commun. 3, 205-211. https://doi.org/10.1006/mcbr.2000.0217
  40. Whalen, S. G., Gingras, A. C., Amankwa, L., Mader, S.,Branton, P. E., Aebersold, R. and Sonenberg, N. (1996)Phosphorylation of eIF-4E on serine 209 by protein kinaseC is inhibited by the translational repressors, 4E-bindingproteins. J. Biol. Chem. 271, 11831-11837. https://doi.org/10.1074/jbc.271.20.11831
  41. Joshi, B., Cai, A. L., Keiper, B. D., Minich, W. B., Mendez,R., Beach, C. M., Stepinski, J., Stolarski, R., Darzynkiewicz,E. and Rhoads, R. E. (1995) Phosphorylation of eukaryoticprotein synthesis initiation factor 4E at Ser-209. J. Biol.Chem. 270, 14597-14603. https://doi.org/10.1074/jbc.270.24.14597
  42. Ueda, T., Watanabe-Fukunaga, R., Fukuyama, H., Nagata,S. and Fukunaga, R. (2004) Mnk2 and Mnk1 are essentialfor constitutive and inducible phosphorylation of eukaryoticinitiation factor 4E but not for cell growth or development.Mol. Cell Biol. 24, 6539-6549. https://doi.org/10.1128/MCB.24.15.6539-6549.2004
  43. McKendrick, L., Morley, S. J., Pain, V. M., Jagus, R. andJoshi, B. (2001) Phosphorylation of eukaryotic initiationfactor 4E (eIF4E) at Ser209 is not required for protein synthesisin vitro and in vivo. Eur. J. Biochem. 268, 5375-5385. https://doi.org/10.1046/j.0014-2956.2001.02478.x
  44. Lachance, P. E., Miron, M., Raught, B., Sonenberg, N. andLasko, P. (2002) Phosphorylation of eukaryotic translationinitiation factor 4E is critical for growth. Mol. Cell Biol.22, 1656-1663. https://doi.org/10.1128/MCB.22.6.1656-1663.2002
  45. Zhang, Y., Li, Y. and Yang, D. Q. (2008) Phosphorylationof eIF-4E positively regulates formation of the eIF-4F translationinitiation complex following DNA damage. Biochem.Biophys. Res. Commun. 367, 54-59. https://doi.org/10.1016/j.bbrc.2007.12.118
  46. Pyronnet, S., Imataka, H., Gingras, A. C., Fukunaga, R.,Hunter, T. and Sonenberg, N. (1999) Human eukaryotictranslation initiation factor 4G (eIF4G) recruits mnk1 tophosphorylate eIF4E. EMBO J. 18, 270-279. https://doi.org/10.1093/emboj/18.1.270
  47. Mader, S., Lee, H., Pause, A. and Sonenberg, N. (1995)The translation initiation factor eIF-4E binds to a commonmotif shared by the translation factor eIF-4 gamma and thetranslational repressors 4E-binding proteins. Mol. CellBiol. 15, 4990-4997. https://doi.org/10.1128/MCB.15.9.4990
  48. Dostie, J., Ferraiuolo, M., Pause, A., Adam, S. A. andSonenberg, N. (2000) A novel shuttling protein, 4E-T, mediatesthe nuclear import of the mRNA 5' cap-binding protein,eIF4E. EMBO J. 19, 3142-3156. https://doi.org/10.1093/emboj/19.12.3142
  49. Heesom, K. J. and Denton, R. M. (1999) Dissociation ofthe eukaryotic initiation factor-4E/4E-BP1 complex involvesphosphorylation of 4E-BP1 by an mTOR-associatedkinase. FEBS Lett. 457, 489-493. https://doi.org/10.1016/S0014-5793(99)01094-7
  50. Lapasset, L., Pradet-Balade, B., Verge, V., Lozano, J. C.,Oulhen, N., Cormier, P. and Peaucellier, G. (2008) CyclinB synthesis and rapamycin-sensitive regulation of proteinsynthesis during starfish oocyte meiotic divisions. Mol.Reprod. Dev. 75, 1617-1626. https://doi.org/10.1002/mrd.20905
  51. Messina, V., Di Sauro, A., Pedrotti, S., Adesso, L., Latina,A., Geremia, R., Rossi, P. and Sette, C. (2010) Differentialcontribution of the MTOR and MNK pathways to the regulationof mRNA translation in meiotic and postmeioticmouse male germ cells. Biol. Reprod. 83, 607-615. https://doi.org/10.1095/biolreprod.110.085050
  52. Henderson, M. A., Cronland, E., Dunkelbarger, S., Contreras,V., Strome, S. and Keiper, B. D. (2009) A germline-specific isoform of eIF4E (IFE-1) is required for efficienttranslation of stored mRNAs and maturation of bothoocytes and sperm. J. Cell Sci. 122, 1529-1539. https://doi.org/10.1242/jcs.046771
  53. Villaescusa, J. C., Allard, P., Carminati, E., Kontogiannea,M., Talarico, D., Blasi, F., Farookhi, R. and Verrotti, A. C.(2006) Clast4, the murine homologue of human eIF4E-Transporter,is highly expressed in developing oocytesand post-translationally modified at meiotic maturation.Gene 367, 101-109. https://doi.org/10.1016/j.gene.2005.09.026
  54. Zappavigna, V., Piccioni, F., Villaescusa, J. C. and Verrotti,A. C. (2004) Cup is a nucleocytoplasmic shuttling proteinthat interacts with the eukaryotic translation initiation factor4E to modulate Drosophila ovary development. Proc.Natl. Acad. Sci. U.S.A. 101, 14800-14805. https://doi.org/10.1073/pnas.0406451101
  55. Piccioni, F., Zappavigna, V. and Verrotti, A. C. (2005) Acup full of functions. RNA Biol. 2, 125-128. https://doi.org/10.4161/rna.2.4.2416
  56. Minshall, N., Reiter, M. H., Weil, D. and Standart, N.(2007) CPEB interacts with an ovary-specific eIF4E and4E-T in early Xenopus oocytes. J. Biol. Chem. 282, 37389-37401. https://doi.org/10.1074/jbc.M704629200
  57. Xu, X., Vatsyayan, J., Gao, C., Bakkenist, C. J. and Hu, J.(2010) HDAC2 promotes eIF4E sumoylation and activatesmRNA translation gene specifically. J. Biol. Chem. 285,18139-18143. https://doi.org/10.1074/jbc.C110.131599
  58. Wang, Z. B., Ou, X. H., Tong, J. S., Li, S., Wei, L.,Ouyang, Y. C., Hou, Y., Schatten, H. and Sun, Q. Y.(2010) The SUMO pathway functions in mouse oocytematuration. Cell Cycle 9, 2638-2644.
  59. Radford, H. E., Meijer, H. A. and de Moor, C. H. (2008)Translational control by cytoplasmic polyadenylation inXenopus oocytes. Biochim. Biophys. Acta. 1779, 217-229. https://doi.org/10.1016/j.bbagrm.2008.02.002
  60. Stebbins-Boaz, B., Cao, Q., de Moor, C. H., Mendez, R.and Richter, J. D. (1999) Maskin is a CPEB-associated factorthat transiently interacts with elF-4E. Mol. Cell 4,1017-1027. https://doi.org/10.1016/S1097-2765(00)80230-0
  61. Cao, Q. and Richter, J. D. (2002) Dissolution of the maskin-eIF4E complex by cytoplasmic polyadenylation and poly(A)-binding protein controls cyclin B1 mRNA translation and oocyte maturation. EMBO J. 21, 3852-3862. https://doi.org/10.1093/emboj/cdf353
  62. Hake, L. E. and Richter, J. D. (1994) CPEB is a specificityfactor that mediates cytoplasmic polyadenylation duringXenopus oocyte maturation. Cell 79, 617-627. https://doi.org/10.1016/0092-8674(94)90547-9
  63. Stebbins-Boaz, B., Hake, L. E. and Richter, J. D. (1996)CPEB controls the cytoplasmic polyadenylation of cyclin,Cdk2 and c-mos mRNAs and is necessary for oocyte maturationin Xenopus. EMBO J. 15, 2582-2592.
  64. Andresson, T. and Ruderman, J. V. (1998) The kinase Eg2is a component of the Xenopus oocyte progesterone-activatedsignaling pathway. EMBO J. 17, 5627-5637. https://doi.org/10.1093/emboj/17.19.5627
  65. Mendez, R., Murthy, K. G., Ryan, K., Manley, J. L. andRichter, J. D. (2000) Phosphorylation of CPEB by Eg2 mediatesthe recruitment of CPSF into an active cytoplasmicpolyadenylation complex. Mol. Cell 6, 1253-1259. https://doi.org/10.1016/S1097-2765(00)00121-0
  66. Mendez, R., Hake, L. E., Andresson, T., Littlepage, L. E.,Ruderman, J. V. and Richter, J. D. (2000) Phosphorylationof CPE binding factor by Eg2 regulates translation of c-mosmRNA. Nature 404, 302-307. https://doi.org/10.1038/35005126
  67. Kim, J. H. and Richter, J. D. (2006) Opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation.Mol. Cell 24, 173-183. https://doi.org/10.1016/j.molcel.2006.08.016
  68. Hodgman, R., Tay, J., Mendez, R. and Richter, J. D.(2001) CPEB phosphorylation and cytoplasmic polyadenylationare catalyzed by the kinase IAK1/Eg2 in maturingmouse oocytes. Development 128, 2815-2822.
  69. Racki, W. J. and Richter, J. D. (2006) CPEB controls oocytegrowth and follicle development in the mouse.Development 133, 4527-4537. https://doi.org/10.1242/dev.02651
  70. Nishimura, Y., Endo, T., Kano, K. and Naito, K. (2009)Porcine Aurora A accelerates Cyclin B and Mos synthesisand promotes meiotic resumption of porcine oocytes.Anim. Reprod. Sci. 113, 114-124. https://doi.org/10.1016/j.anireprosci.2008.05.074
  71. Yao, L. J., Zhong, Z. S., Zhang, L. S., Chen, D. Y.,Schatten, H. and Sun, Q. Y. (2004) Aurora-A is a criticalregulator of microtubule assembly and nuclear activity inmouse oocytes, fertilized eggs, and early embryos. Biol.Reprod. 70, 1392-1399. https://doi.org/10.1095/biolreprod.103.025155
  72. Atkins, C. M., Nozaki, N., Shigeri, Y. and Soderling, T. R.(2004) Cytoplasmic polyadenylation element binding protein-dependent protein synthesis is regulated by calcium/calmodulin-dependent protein kinase II. J. Neurosci. 24, 5193-5201. https://doi.org/10.1523/JNEUROSCI.0854-04.2004
  73. Su, Y. Q. and Eppig, J. J. (2002) Evidence that multifunctionalcalcium/calmodulin-dependent protein kinase II(CaM KII) participates in the meiotic maturation of mouseoocytes. Mol. Reprod. Dev. 61, 560-569. https://doi.org/10.1002/mrd.10034
  74. Kozak, M. (2006) Rethinking some mechanisms invokedto explain translational regulation in eukaryotes. Gene382, 1-11. https://doi.org/10.1016/j.gene.2006.06.004
  75. de Moor, C. H., Meijer, H. and Lissenden, S. (2005)Mechanisms of translational control by the 3' UTR in developmentand differentiation. Semin. Cell Dev. Biol. 16,49-58. https://doi.org/10.1016/j.semcdb.2004.11.007
  76. Hao, Z., Stoler, M. H., Sen, B., Shore, A., Westbrook, A.,Flickinger, C. J., Herr, J. C. and Coonrod, S. A. (2002)TACC3 expression and localization in the murine egg andovary. Mol. Reprod. Dev. 63, 291-299. https://doi.org/10.1002/mrd.90012
  77. Groisman, I., Huang, Y. S., Mendez, R., Cao, Q.,Theurkauf, W. and Richter, J. D. (2000) CPEB, maskin,and cyclin B1 mRNA at the mitotic apparatus: implicationsfor local translational control of cell division.Cell 103, 435-447. https://doi.org/10.1016/S0092-8674(00)00135-5
  78. Meijer, H. A., Radford, H. E., Wilson, L. S., Lissenden, S.and de Moor, C. H. (2007) Translational control of maskinmRNA by its 3' untranslated region. Biol. Cell 99, 239-250. https://doi.org/10.1042/BC20060112
  79. Kawahara, H., Imai, T., Imataka, H., Tsujimoto, M.,Matsumoto, K. and Okano, H. (2008) Neural RNA-bindingprotein Musashi1 inhibits translation initiation bycompeting with eIF4G for PABP. J. Cell Biol. 181,639-653. https://doi.org/10.1083/jcb.200708004
  80. Kee, K., Angeles, V. T., Flores, M., Nguyen, H. N. andReijo Pera, R. A. (2009) Human DAZL, DAZ and BOULEgenes modulate primordial germ-cell and haploid gameteformation. Nature 462, 222-225. https://doi.org/10.1038/nature08562
  81. Collier, B., Gorgoni, B., Loveridge, C., Cooke, H. J. andGray, N. K. (2005) The DAZL family proteins arePABP-binding proteins that regulate translation in germcells. EMBO J. 24, 2656-2666. https://doi.org/10.1038/sj.emboj.7600738
  82. Morton, S., Yang, H. T., Moleleki, N., Campbell, D. G.,Cohen, P. and Rousseau, S. (2006) Phosphorylation of theARE-binding protein DAZAP1 by ERK2 induces its dissociationfrom DAZ. Biochem. J. 399, 265-273. https://doi.org/10.1042/BJ20060681
  83. Urano, J., Fox, M. S. and Reijo Pera, R. A. (2005) Interactionof the conserved meiotic regulators, BOULE (BOL)and PUMILIO-2 (PUM2). Mol. Reprod. Dev. 71, 290-298. https://doi.org/10.1002/mrd.20270
  84. Liu, J., Linher, K. and Li, J. (2009) Porcine DAZL messengerRNA: its expression and regulation during oocytematuration. Mol. Cell Endocrinol. 311, 101-108. https://doi.org/10.1016/j.mce.2009.06.003
  85. Kuge, H., Brownlee, G. G., Gershon, P. D. and Richter, J.D. (1998) Cap ribose methylation of c-mos mRNA stimulatestranslation and oocyte maturation in Xenopuslaevis. Nucleic Acids Res. 26, 3208-3214. https://doi.org/10.1093/nar/26.13.3208
  86. Kuge, H. and Richter, J. D. (1995) Cytoplasmic 3' poly(A)addition induces 5' cap ribose methylation: implicationsfor translational control of maternal mRNA. EMBO J. 14,6301-6310.
  87. Gillian-Daniel, D. L., Gray, N. K., Astrom, J., Barkoff, A.and Wickens, M. (1998) Modifications of the 5' cap ofmRNAs during Xenopus oocyte maturation: independencefrom changes in poly(A) length and impact on translation.Mol. Cell Biol. 18, 6152-6163. https://doi.org/10.1128/MCB.18.10.6152
  88. Bachvarova, R., De Leon, V., Johnson, A., Kaplan, G. andPaynton, B. V. (1985) Changes in total RNA, polyadenylatedRNA, and actin mRNA during meiotic maturation ofmouse oocytes. Dev. Biol. 108, 325-331. https://doi.org/10.1016/0012-1606(85)90036-3
  89. Paynton, B. V., Rempel, R. and Bachvarova, R. (1988)Changes in state of adenylation and time course of degradationof maternal mRNAs during oocyte maturation andearly embryonic development in the mouse. Dev. Biol.129, 304-314. https://doi.org/10.1016/0012-1606(88)90377-6
  90. Parker, R. and Song, H. (2004) The enzymes and controlof eukaryotic mRNA turnover. Nat. Struct. Mol. Biol. 11,121-127. https://doi.org/10.1038/nsmb724
  91. Flemr, M., Ma, J., Schultz, R. M. and Svoboda, P. (2010)P-body loss is concomitant with formation of a messengerRNA storage domain in mouse oocytes. Biol. Reprod. 82,1008-1017. https://doi.org/10.1095/biolreprod.109.082057
  92. Paynton, B. V. and Bachvarova, R. (1994) Polyadenylationand deadenylation of maternal mRNAs during oocytegrowth and maturation in the mouse. Mol. Reprod. Dev.37, 172-180. https://doi.org/10.1002/mrd.1080370208
  93. Yekta, S., Shih, I. H. and Bartel, D. P. (2004) MicroRNA-directedcleavage of HOXB8 mRNA. Science 304, 594-596. https://doi.org/10.1126/science.1097434
  94. Fabian, M. R., Sonenberg, N. and Filipowicz, W. (2010)Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 79, 351-379. https://doi.org/10.1146/annurev-biochem-060308-103103
  95. Tam, O. H., Aravin, A. A., Stein, P., Girard, A., Murchison,E. P., Cheloufi, S., Hodges, E., Anger, M., Sachidanandam,R., Schultz, R. M. and Hannon, G. J. (2008) Pseudogene-derivedsmall interfering RNAs regulate gene expressionin mouse oocytes. Nature 453, 534-538. https://doi.org/10.1038/nature06904
  96. Watanabe, T., Totoki, Y., Toyoda, A., Kaneda, M., Kuramochi-Miyagawa, S., Obata, Y., Chiba, H., Kohara, Y., Kono, T., Nakano, T., Surani, M. A., Sakaki, Y. and Sasaki, H. (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453, 539-543. https://doi.org/10.1038/nature06908
  97. Murchison, E. P., Stein, P., Xuan, Z., Pan, H., Zhang, M.Q., Schultz, R. M. and Hannon, G. J. (2007) Critical rolesfor Dicer in the female germline. Genes Dev. 21, 682-693. https://doi.org/10.1101/gad.1521307
  98. Suh, N., Baehner, L., Moltzahn, F., Melton, C., Shenoy,A., Chen, J. and Blelloch, R. (2010) MicroRNA function isglobally suppressed in mouse oocytes and early embryos. Curr. Biol. 20, 271-277. https://doi.org/10.1016/j.cub.2009.12.044
  99. Goodfellow, I. G. and Roberts, L. O. (2008) Eukaryotic initiationfactor 4E. Int. J. Biochem. Cell Biol. 40, 2675-2680. https://doi.org/10.1016/j.biocel.2007.10.023
  100. Rhoads, R. E. (2009) eIF4E: new family members, newbinding partners, new roles. J. Biol. Chem. 284, 16711-16715. https://doi.org/10.1074/jbc.R900002200
  101. Wang, S., Kou, Z., Jing, Z., Zhang, Y., Guo, X., Dong,M., Wilmut, I. and Gao, S. (2010) Proteome of mouse oocytesat different developmental stages. Proc. Natl. Acad.Sci. U.S.A. 107, 17639-17644. https://doi.org/10.1073/pnas.1013185107

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