Germinal vesicle material drives meiotic cell cycle of mouse oocyte through the 3′UTR-dependent control of cyclin B1 synthesis

Developmental Biology

Volumn 292, Issue 1, 2006, Pages 46-54

  Hoffmann, Steffen ^a   Tsurumi, Chizuko ^a   Kubiak, Jacek Z ^b   Polanski, Zbigniew ^a,c  

^a MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^b UNIVERSITÉ DE RENNES 1   (France)

^c JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

Cyclin B1; GV associated factor(s); MAP kinase; Meiotic maturation; Mouse oocyte; MPF; mRNA; Translational control

Indexed keywords

CYCLIN B1; CYCLIN DEPENDENT KINASE 1; GLOBIN; HISTONE H1; LUCIFERASE; MATURATION PROMOTING FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; RNA; CYCLIN B; HISTONE H1 KINASE; MESSENGER RNA; ONCOPROTEIN; PROTEIN KINASE;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL CYCLE; CELL MATURATION; CELL NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GERMINAL VESICLE; MEIOSIS; MOUSE; NONHUMAN; OOCYTE; OOCYTE MATURATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA SEQUENCE; SEQUENCE ANALYSIS; STATISTICAL SIGNIFICANCE; ANIMAL; BIOSYNTHESIS; CELL CULTURE; COMPARATIVE STUDY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALIA;

3' UNTRANSLATED REGIONS; ANIMALS; CDC2 PROTEIN KINASE; CELL NUCLEUS; CELLS, CULTURED; CYCLIN B; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MATURATION-PROMOTING FACTOR; MEIOSIS; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; OOCYTES; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-MOS; RNA, MESSENGER;

EID: 33646453544     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.12.052     Document Type: Article

References (49)

1. Balakier H., and Czolowska R. Cytoplasmic control of nuclear maturation in mouse oocytes. Exp. Cell Res. 110 (1977) 466-469
2. Balakier H., and Tarkowski A.K. The role of germinal vesicle karyoplasm in the development of male pronucleus in the mouse. Exp. Cell Res. 128 (1980) 79-85
3. Borsuk E. Anucleate fragments of parthenogenetic eggs and of maturing oocytes contain complementary factors required for development of a male pronucleus. Mol. Reprod. Dev. 29 (1991) 150-156
4. Cho W.K., Stern S., and Biggers J.D. Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J. Exp. Zool. 187 (1974) 383-386
5. Choi T., Aoki F., Mori M., Yamashita M., Nagahama Y., and Kohmoto K. Activation of p34cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development 113 (1991) 789-795
6. Ciemerych M.A., and Kubiak J.Z. Transient reactivation of CSF in parthenogenetic one-cell mouse embryos. Biol. Cell. 91 (1999) 641-647
7. Colledge W.H., Carlton M.B., Udy G.B., and Evans M.J. Disruption of c-mos causes parthenogenetic development of unfertilized mouse eggs. Nature (1994) 65-68
8. Fisher D., Coux O., Bompard-Marechal G., and Doree M. Germinal vesicle material is dispensable for oscillations in cdc2 and MAP kinase activities, cyclin B degradation and synthesis during meiosis in Xenopus oocytes. Biol. Cell. 90 (1998) 497-508
9. Fulton B.P., and Whittingham D.G. Activation of mammalian oocytes by intracellular injection of calcium. Nature 273 (1978) 149-151
10. Galas S., Barakat H., Doree M., and Picard A. A nuclear factor required for specific translation of cyclin B may control the timing of first meiotic cleavage in starfish oocytes. Mol. Biol. Cell 4 (1993) 1295-1306
11. Gautier J. The role of the germinal vesicle for the appearance of maturation-promoting factor activity in the axolotl oocyte. Dev. Biol. 123 (1987) 483-486
12. Gebauer F., Xu W., Cooper G.M., and Richter J.D. Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J. 13 (1994) 5712-5720
13. Hagting A., Karlsson C., Clute P., Jackman M., and Pines J. MPF localization is controlled by nuclear export. EMBO J. 17 (1998) 4127-4138
14. Hampl A., and Eppig J.J. Translational regulation of the gradual increase in histone H1 kinase activity in maturing mouse oocytes. Mol. Reprod. Dev. 40 (1995) 9-15
15. Hashimoto N., Watanabe N., Furuta Y., Tamemoto H., Sagata N., Yokoyama M., Okazaki K., Nagayoshi M., Takeda N., Ikawa Y., and Aizawa S. Parthenogenetic activation of oocytes in c-mos-deficient mice. Nature 370 (1994) 68-71
16. Hodgman R., Tay J., Mendez R., and Richter J.D. CPEB phosphorylation and cytoplasmic polyadenylation are catalyzed by the kinase IAK1/Eg2 in maturing mouse oocytes. Development 128 (2001) 2122-2815
17. Huarte J., Stutz A., O'Connell M.L., Gubler P., Belin D., Darrow A.L., Strickland S., and Vassalli J.D. Transient translational silencing by reversible mRNA deadenylation. Cell 69 (1992) 1021-1030
18. Hyslop L.A., Nixon V.L., Levasseur M., Chapman F., Chiba K., McDougall A., Venables J.P., Elliott D.J., and Jones K.T. Ca(2+)-promoted cyclin B1 degradation in mouse oocytes requires the establishment of a metaphase arrest. Dev. Biol. 269 (2004) 206-219
19. Iwashita J., Hayano Y., and Sagata N. Essential role of germinal vesicle material in the meiotic cell cycle of Xenopus oocytes. Proc. Natl Acad. Sci. U. S. A. 95 (1998) 4392-4397
20. Josefsberg L.B., Galiani D., Dantes A., Amsterdam A., and Dekel N. The proteasome is involved in the first metaphase-to-anaphase transition of meiosis in rat oocytes. Biol. Reprod. 62 (2000) 1270-1277
21. Kono T., Carroll J., Swann K., and Whittingham D.G. Nuclei from fertilized mouse embryos have calcium-releasing activity. Development 121 (1995) 1123-1128
22. Kubiak J.Z., Weber M., Geraud G., and Maro B. Cell cycle modification during the transitions between meiotic M-phases in mouse oocytes. J. Cell Sci. 102 (1992) 457-467
23. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
24. Lapasset L., Pradet-Balade B., Lozano J.C., Peaucellier G., and Picard A. Nuclear envelope breakdown may deliver an inhibitor of protein phosphatase 1 which triggers cyclin B translation in starfish oocytes. Dev. Biol. 285 (2005) 200-210
25. Ledan E., Polanski Z., Terret M.E., and Maro B. Meiotic maturation of the mouse oocyte requires an equilibrium between cyclin B synthesis and degradation. Dev. Biol. 232 (2001) 400-413
26. Marangos P., and Carroll J. The dynamics of cyclin B1 distribution during meiosis I in mouse oocytes. Reproduction 128 (2004) 153-162
27. Masui Y., and Markert C.L. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 177 (1971) 129-145
28. Mendez R., and Richter J.D. Translational control by CPEB: a means to the end. Nat. Rev., Mol. Cell Biol. 2 (2001) 521-529
29. In: Nagy A., Gertsenstain M., Vintersten K., and Behringer R. (Eds). Manipulating the Mouse Embryo. A Laboratory Manual (2003), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
30. Ogushi S., Fulka Jr. J., and Miyano T. Germinal vesicle materials are requisite for male pronucleus formation but not for change in the activities of CDK1 and MAP kinase during maturation and fertilization of pig oocytes. Dev. Biol. 286 (2005) 287-298
31. Picard A., and Doree M. The role of the germinal vesicle in producing maturation-promoting factor (MPF) as revealed by the removal and transplantation of nuclear material in starfish oocytes. Dev. Biol. 104 (1984) 357-365
32. Pines J., and Hunter T. Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J. Cell Biol. 115 (1991) 1-17
33. Polanski Z. Strain difference in the timing of meiosis resumption in mouse oocytes: involvement of a cytoplasmic factor(s) acting presumably upstream of the dephosphorylation of p34(cdc2) kinase. Zygote 5 (1997) 105-109
34. Polanski Z. Genetic background of the differences in timing of meiotic maturation in mouse oocytes: a study using recombinant inbred strains. J. Reprod. Fertil. 109 (1997) 109-114
35. Polanski Z., Ledan E., Brunet S., Louvet S., Verlhac M.H., Kubiak J.Z., and Maro B. Cyclin synthesis controls the progression of meiotic maturation in mouse oocytes. Development 125 (1998) 4989-4997
36. Polanski Z., Hoffmann S., and Tsurumi C. Oocyte nucleus controls progression through meiotic maturation. Dev. Biol. 281 (2005) 184-195
37. Schneider C., Newman R.A., Sutherland D.R., Asser U., and Greaves M.F. A one-step purification of membrane proteins using a high efficiency immunomatrix. J. Biol. Chem. 257 (1982) 10766-10769
38. Schorderet-Slatkine S., and Drury K.C. Progesterone induced maturation in oocytes of Xenopus laevis. Appearance of a 'maturation promoting factor' in enucleated oocytes. Cell Differ. 2 (1973) 247-254
39. Skoblina M.N., Pivnitsky K.K., and Kondratieva O.T. The role of germinal vesicle in maturation of Pleurodeles waltlii oocytes induced by steroids. Cell Differ. 14 (1984) 153-157
40. Sugiura, K., Naito, K., Endo T., Tojo, H., in press. Study of germinal vesicle requirement for the normal kinetics of maturation/M-Phase-Promoting Factor activity during porcine oocyte maturation. Biol. Reprod.
41. Tarkowski A.K. In vitro development of haploid mouse embryos produced by bisection of one-cell fertilized eggs. J. Embryol. Exp. Morphol. 38 (1977) 187-202
42. Tay J., Hodgman R., and Richter J.D. The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev. Biol. 221 (2000) 1-9
43. Tsurumi C., Hoffmann S., Graeser R., Geley S., and Polanski Z. The spindle assembly checkpoint is not essential for CSF arrest of mouse oocytes. J. Cell Biol. 167 (2004) 1037-1050
44. Vassalli J.D., Huarte J., Belin D., Gubler P., Vassalli A., O'Connell M.L., Parton L.A., Rickles R.J., and Strickland S. Regulated polyadenylation controls mRNA translation during meiotic maturation of mouse oocytes. Genes Dev. 12 (1989) 2163-2171
45. Verlhac M.-H., de Pennart H., Maro B., Cobb M.H., and Clarke H.J. MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev. Biol. 158 (1993) 330-340
46. 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
47. Verlhac M.H., Kubiak J.Z., Weber M., Geraud G., Colledge W.H., Evans M.J., and Maro B. Mos is required for MAP kinase activation and is involved in microtubule organization during meiotic maturation in the mouse. Development 122 (1996) 815-822
48. Winston N.J. Stability of cyclin B protein during meiotic maturation and the first mitotic cell division in mouse oocytes. Biol. Cell. 89 (1997) 211-219
49. Zernicka-Goetz M., Ciemerych M.A., Kubiak J.Z., Tarkowski A.K., and Maro B. Cytostatic factor inactivation is induced by a calcium-dependent mechanism present until the second cell cycle in fertilized but not in parthenogenetically activated mouse eggs. J. Cell Sci. 108 (1995) 469-474