CDC2A (CDK1)-mediated phosphorylation of MSY2 triggers maternal mRNA degradation during mouse oocyte maturation

Developmental Biology

Volumn 321, Issue 1, 2008, Pages 205-215

  Medvedev, Sergey ^a   Yang, Juxiang ^a   Hecht, Norman B ^a   Schultz, Richard M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Mouse oocyte; mRNA degradation; mRNA stability; MSY2; Oocyte maturation; Protein phosphorylation; RNA binding protein

Indexed keywords

CYCLIN DEPENDENT KINASE 1; MESSENGER RNA; MILRINONE; MOUSE SPECIFIC Y BOX PROTEIN; RNA BINDING PROTEIN; ROSCOVITINE;

ANIMAL EXPERIMENT; ARTICLE; MOUSE; NONHUMAN; OOCYTE MATURATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA DEGRADATION;

EID: 49049120288     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.06.016     Document Type: Article

References (52)

1. Bachvarova R., and DeLeon V. Polyadenylated RNA of mouse ova and loss of maternal RNA in early development. Dev. Biol. 74 (1980) 1-8
2. Bouvet P., Matsumoto K., and Wolffe A.P. Sequence-specific RNA recognition by the Xenopus Y-box proteins. An essential role for the cold shock domain. J. Biol. Chem. 270 (1995) 28297-28303
3. Brower P.T., Gizang E., Boreen S.M., and Schultz R.M. Biochemical studies of mammalian oogenesis: synthesis and stability of various classes of RNA during growth of the mouse oocyte in vitro. Dev. Biol. 86 (1981) 373-383
4. Chapman D.L., and Wolgemuth D.J. Identification of a mouse B-type cyclin which exhibits developmentally regulated expression in the germ line. Mol. Reprod. Dev. 33 (1992) 259-269
5. Chatot C.L., Ziomek C.A., Bavister B.D., Lewis J.L., and Torres I. An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J. Reprod. Fertil. 86 (1989) 679-688
6. Davies H.G., Giorgini F., Fajardo M.A., and Braun R.E. A sequence-specific RNA binding complex expressed in murine germ cells contains MSY2 and MSY4. Dev. Biol. 221 (2000) 87-100
7. de Vantéry C., Stutz A., Vassalli J.D., and Schorderet-Slatkine S. Acquisition of meiotic competence in growing mouse oocytes is controlled at both translational and posttranslational levels. Dev. Biol. 187 (1997) 43-54
8. DeRenzo C., and Seydoux G. A clean start: degradation of maternal proteins at the oocyte-to-embryo transition. Trends Cell Biol. 14 (2004) 420-426
9. Deschamps S., Jacquemin-Sablon H., Triqueneaux G., Mulner-Lorillon O., Potier M., Le Caer J.P., Dautry F., and le Maire M. mRNP3 and mRNP4 are phosphorylatable by casein kinase II in Xenopus oocytes, but phosphorylation does not modify RNA-binding affinity. FEBS Lett. 412 (1997) 495-500
10. Eulalio A., Behm-Ansmant I., and Izaurralde E. P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev., Mol. Cell Biol. 8 (2007) 9-22
11. Evdokimova V., Ruzanov P., Anglesio M.S., Sorokin A.V., Ovchinnikov L.P., Buckley J., Triche T.J., Sonenberg N., and Sorensen P.H. Akt-mediated YB-1 phosphorylation activates translation of silent mRNA species. Mol. Cell. Biol. 26 (2006) 277-292
12. Giraldez A.J., Mishima Y., Rihel J., Grocock R.J., Van Dongen S., Inoue K., Enright A.J., and Schier A.F. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312 (2006) 75-79
13. Gu W., Tekur S., Reinbold R., Eppig J.J., Choi Y.C., Zheng J.Z., Murray M.T., and Hecht N.B. Mammalian male and female germ cells express a germ cell-specific Y-box protein, MSY2. Biol. Reprod. 59 (1998) 1266-1274
14. Hamatani T., Carter M.G., Sharov A.A., and Ko M.S. Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6 (2004) 117-131
15. Herbert T.P., and Hecht N.B. The mouse Y-box protein, MSY2, is associated with a kinase on non-polysomal mouse testicular mRNAs. Nucleic Acids Res. 27 (1999) 1747-1753
16. Jiang W., Hou Y., and Inouye M. CspA, the major cold-shock protein of Escherichia coli, is an RNA chaperone. J. Biol. Chem. 272 (1997) 196-202
17. Kalous J., Solc P., Baran V., Kubelka M., Schultz R.M., and Motlik J. PKB/AKT is involved in resumption of meiosis in mouse oocytes. Biol. Cell 98 (2006) 111-123
18. Latham K.E., Garrels J.I., Chang C., and Solter D. Quantitative analysis of protein synthesis in mouse embryos. I. Extensive reprogramming at the one- and two-cell stages. Development 112 (1991) 921-932
19. Moore G.P.M. The RNA polymerase activity of the preimplantation mouse embryo. J. Embryol. Exp. Morph. 34 (1975) 291-298
20. Moore G.P.M., and Lintern-Moore S. Transcription of the mouse oocyte genome. Biol. Reprod. 17 (1978) 865-870
21. Moos J., Visconti P.E., Moore G.D., Schultz R.M., and Kopf G.S. Potential role of mitogen-activated protein kinase in pronuclear envelope assembly and disassembly following fertilization of mouse eggs. Biol. Reprod. 53 (1995) 692-699
22. Murchison E.P., Stein P., Xuan Z., Pan H., Zhang M.Q., Schultz R.M., and Hannon G.J. Critical roles for Dicer in the female germline. Genes Dev. 21 (2007) 682-693
23. Phillips K.P., Petrunewich M.A., Collins J.L., Booth R.A., Liu X.J., and Baltz J.M. Inhibition of MEK or cdc2 kinase parthenogenetically activates mouse eggs and yields the same phenotypes as Mos(-/-) parthenogenotes. Dev. Biol. 247 (2002) 210-223
24. Puschendorf M., Stein P., Oakeley E.J., Schultz R.M., Peters A.H., and Svoboda P. Abundant transcripts from retrotransposons are unstable in fully grown mouse oocytes. Biochem. Biophys. Res. Commun. 347 (2006) 36-43
25. Ross J. A hypothesis to explain why translation inhibitors stabilize mRNAs in mammalian cells: mRNA stability and mitosis. BioEssays 19 (1997) 527-529
26. Salvetti A., Batistoni R., Deri P., Rossi L., and Sommerville J. Expression of DjY1, a protein containing a cold shock domain and RG repeat motifs, is targeted to sites of regeneration in planarians. Dev. Biol. 201 (1998) 217-229
27. Schindelin H., Jiang W., Inouye M., and Heinemann U. Crystal structure of CspA, the major cold shock protein of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 5119-5123
28. Schultz R.M. Regulation of zygotic gene activation in the mouse. BioEssays 15 (1993) 531-538
29. Schultz R.M., and Wassarman P.M. Biochemical studies of mammalian oogenesis: protein synthesis during oocyte growth and meiotic maturation. J. Cell Sci. 24 (1977) 167-194
30. Semotok J.L., Cooperstock R.L., Pinder B.D., Vari H.K., Lipshitz H.D., and Smibert C.A. Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr. Biol. 15 (2005) 284-294
31. Sommerville J., and Ladomery M. Masking of mRNA by Y-box proteins. FASEB J. 10 (1996) 435-443
32. Stitzel M.L., and Seydoux G. Regulation of the oocyte-to-zygote transition. Science 316 (2007) 407-408
33. Su Y.Q., Sugiura K., Woo Y., Wigglesworth K., Kamdar S., Affourtit J., and Eppig J.J. Selective degradation of transcripts during meiotic maturation of mouse oocytes. Dev. Biol. 302 (2007) 104-117
34. Svoboda P., Stein P., Hayashi H., and Schultz R.M. Selective reduction of dormant maternal mRNAs in mouse oocytes by RNA interference. Development 127 (2000) 4147-4156
35. Swamynathan S.K., Nambiar A., and Guntaka R.V. Role of single-stranded DNA regions and Y-box proteins in transcriptional regulation of viral and cellular genes. FASEB J. 12 (1998) 515-522
36. Tafuri S.R., and Wolffe A.P. Xenopus Y-box transcription factors: molecular cloning, functional analysis and developmental regulation. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 9028-9032
37. Tekur S., Pawlak A., Guellaen G., and Hecht N.B. Contrin, the human homologue of a germ-cell Y-box-binding protein: cloning, expression, and chromosomal localization. J. Androl. 20 (1999) 135-144
38. Thieringer H.A., Singh K., Trivedi H., and Inouye M. Identification and developmental characterization of a novel Y-box protein from Drosophila melanogaster. Nucleic Acids Res. 25 (1997) 4764-4770
39. Verlhac M.H., Kubiak J.Z., Clarke H.J., and Maro B. Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 120 (1994) 1017-1025
40. Wang Q.T., Piotrowska K., Ciemerych M.A., Milenkovic L., Scott M.P., Davis R.W., and Zernicka-Goetz M. A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev. Cell 6 (2004) 133-144
41. Wiersma A., Hirsch B., Tsafriri A., Hanssen R.G., Van de Kant M., Kloosterboer H.J., Conti M., and Hsueh A.J. Phosphodiesterase 3 inhibitors suppress oocyte maturation and consequent pregnancy without affecting ovulation and cyclicity in rodents. J. Clin. Invest. 102 (1998) 532-537
42. Wolffe A.P. Structural and functional properties of the evolutionarily ancient Y-box family of nucleic acid binding proteins. BioEssays 16 (1994) 245-251
43. Wolffe A.P., Tafuri S., Ranjan M., and Familari M. The Y-box factors: a family of nucleic acid binding proteins conserved from Escherichia coli to man. New Biol. 4 (1992) 290-298
44. Yang J., Medvedev S., Reddi P.P., Schultz R.M., and Hecht N.B. The DNA/RNA-binding protein MSY2 marks specific transcripts for cytoplasmic storage in mouse male germ cells. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 1513-1518
45. Yang J., Medvedev S., Yu J., Tang L.C., Agno J.E., Matzuk M.M., Schultz R.M., and Hecht N.B. Absence of the DNA-/RNA-binding protein MSY2 results in male and female infertility. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 5755-5760
46. Yang J., Morales C.R., Medvedev S., Schultz R.M., and Hecht N.B. In the absence of the mouse DNA/RNA-binding protein MSY2 messenger RNA instability leads to spermatogenic arrest. Biol. Reprod. 76 (2007) 48-54
47. Yu J., Hecht N.B., and Schultz R.M. Expression of MSY2 in mouse oocytes and preimplantation embryos. Biol. Reprod. 65 (2001) 1260-1270
48. Yu J., Hecht N.B., and Schultz R.M. RNA-binding properties and translation repression in vitro by germ cell-specific MSY2 protein. Biol. Reprod. 67 (2002) 1093-1098
49. Yu J., Hecht N.B., and Schultz R.M. Requirement for RNA-binding activity of MSY2 for cytoplasmic localization and retention in mouse oocytes. Dev. Biol. 255 (2003) 249-262
50. Yu J., Deng M., Medvedev S., Yang J., Hecht N.B., and Schultz R.M. Transgenic RNAi-mediated reduction of MSY2 in mouse oocytes results in reduced fertility. Dev. Biol. 268 (2004) 195-206
51. Zeng F., and Schultz R.M. RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Dev. Biol. 283 (2005) 40-57
52. Zeng F., Baldwin D.A., and Schultz R.M. Transcript profiling during preimplantation mouse development. Dev. Biol. 272 (2004) 483-496