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JOURNAL ARTICLES
Analysis of the mechanism(s) of metaphase I arrest in maturing mouse oocytes
A. Hampl, J.J. Eppig
Development 1995 121: 925-933;
A. Hampl
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J.J. Eppig
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Summary

Fully grown mouse oocytes are normally competent to progress from prophase I to metaphase II without interruption. However, growing mouse oocytes initially become only partially competent to undergo meiotic maturation. Meiotic maturation in these oocytes does not progress beyond metaphase I. In contrast to the oocytes of most strains of mice, most oocytes of strain LT/Sv mice become arrested at metaphase I even when they are fully grown. The initiation of oocyte maturation is correlated with an increase in p34cdc2 kinase activity that continues to rise until metaphase I. The transition into anaphase I is normally correlated with a decrease in p34cdc2 kinase activity. This study demonstrated that metaphase I arrest in both partially competent growing oocytes and fully grown LT/Sv oocytes is correlated with a sustained elevation of p34cdc2 kinase activity. In fact, p34cdc2 activity continued to increase during the time when activity normally decreased. In normally maturing oocytes, some, but not all, of the cyclin B, the regulatory protein associated with p34cdc2, became degraded in oocytes that entered anaphase I. In contrast, the amount of cyclin B present in the metaphase I-arrested oocytes continued to increase at the time when it was being degraded in normal oocytes progressing to metaphase II. These results suggest that the progression of meiosis is arrested at metaphase I in both groups of oocytes because of continued p34cdc2 kinase activity sustained, at least in part, by restricted degradation of cyclin B.(ABSTRACT TRUNCATED AT 250 WORDS)

Reference

    1. Choi T.,
    2. Aoki F.,
    3. Mori M.,
    4. Yamashita M.,
    5. Nagahama Y.,
    6. Kohmoto K.
    (1991) Activation of p34cdc2protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development 113, 789–795
    OpenUrlAbstract
    1. De Smedt V.,
    2. Crozet N.,
    3. Gall L.
    (1994) Morphological and functional changes accompanying the acquisition of meiotic competence in ovarian goat oocyte. J. Exp. Zool 269, 128–139
    OpenUrlCrossRefPubMedWeb of Science
    1. Draetta G.,
    2. Beach D.
    (1988) Activation of cdc2 protein kinase during mitosis in human cells: cell cycle-dependent phosphorylation and subunit rearrangement. Cell 54, 17–26
    OpenUrlCrossRefPubMedWeb of Science
    1. Draetta G.,
    2. Luca F.,
    3. Westendorf J.,
    4. Brizuela L.,
    5. Ruderman J.,
    6. Beach D.
    (1989) cdc2 protein kinase is complexed with both cyclin A and B: evidence for proteolytic inactivation of MPF. Cell 56, 829–838
    OpenUrlCrossRefPubMedWeb of Science
    1. Ducibella T.,
    2. Kurasawa S.,
    3. Duffy P.,
    4. Kopf G. S.,
    5. Schultz R. M.
    (1993) Regulation of the polyspermy block in the mouse egg: maturation-dependent differences in cortical granule exocytosis and zona pellucida modifications induced by inositol 1,4,5-trisphosphate and an activator of protein kinase C. Bio. Reprod 48, 1251–1257
    OpenUrlAbstract
    1. Dunphy W. G.,
    2. Brizuela L.,
    3. Beach D.,
    4. Newport J.
    (1988) The Xenopus cdc2 protein is a component of MPF, a cytoplasmic regulator of mitosis. Cell 54, 423–431
    OpenUrlCrossRefPubMedWeb of Science
    1. Edwards R. G.
    (1965) Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208, 349–351
    OpenUrlCrossRefPubMed
    1. Eppig J. J.,
    2. Schultz R. M.,
    3. O'Brien M.,
    4. Chesnel F.
    (1994) Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. Dev. Biol 164, 1–9
    OpenUrlCrossRefPubMedWeb of Science
    1. Eppig J. J.,
    2. Wigglesworth K.
    (1994) Atypical maturation of oocytes of strain I/LnJ mice. Human Reprod 9, 1136–1142
    OpenUrlAbstract/FREE Full Text
    1. Fujiwara T.,
    2. Nakada K.,
    3. Shirakawa H.,
    4. Miyazaki S.
    (1993) Development of inositol trisphosphate-induced calcium release mechanism during maturation of hamster oocytes. Dev. Biol 156, 69–79
    OpenUrlCrossRefPubMedWeb of Science
    1. Fulka J., Jr.,
    2. Jung T.,
    3. Moor R. M.
    (1992) The fall of biological maturation promoting factor (MPF) and histone H1 kinase activity during anaphase and telophase in mouse oocytes. Mol. Reprod. Dev 32, 378–382
    OpenUrlCrossRefPubMedWeb of Science
    1. Fulton B. P.,
    2. Whittingham D. G.
    (1978) Activation of mammalian oocytes by intracellular injection of calcium. Nature 273, 149–151
    OpenUrlCrossRefPubMed
    1. Gallant P.,
    2. Nigg E. A.
    (1992) Cyclin B2 undergoes cell cycle-dependent nuclear translocation and, when expressed as a non-destructible mutant, causes mitotic arrest in HeLa cells. J. Cell Biol 117, 213–224
    OpenUrlAbstract/FREE Full Text
    1. Hampl A.,
    2. Eppig J. J.
    (1995) Translational regulation of the gradual increase in histone H1 kinase activity in maturing mouse oocytes. Mol. Reprod. Dev 40, 9–15
    OpenUrlCrossRefPubMedWeb of Science
    1. Hashimoto H.,
    2. Kishimoto T.
    (1988) Regulation of meiotic metaphase by a cytoplasmic maturation-promoting factor during mouse oocyte maturation. Dev. Biol 126, 242–252
    OpenUrlCrossRefPubMedWeb of Science
    1. Hunt T.,
    2. Luca F. C.,
    3. Ruderman J. V.
    (1992) The requirements for protein synthesis and degradation, and the control of destruction of cyclins A and B in the meiotic and mitotic cell cycles of the clam embryo. J. Cell Biol 116, 707–724
    OpenUrlAbstract/FREE Full Text
    1. Kaufman M. H.,
    2. Speirs S.
    (1987) The postimplantation development of spontaneous digynic tripliod embryos in LT/Sv strain mice. Development 101, 383–391
    OpenUrlAbstract
    1. Kobayashi H.,
    2. Minshull J.,
    3. Ford C.,
    4. Golsteyn R.,
    5. Poon R.,
    6. Hunt T.
    (1991) On the synthesis and destruction of A-and B-type cyclins during oogenesis and meiotic maturation in Xenopus laevis. J. Cell Biol 114, 755–765
    OpenUrlAbstract/FREE Full Text
    1. Kubiak J. Z.,
    2. Weber M.,
    3. de Pennart H.,
    4. Winston N. J.,
    5. Maro B.
    (1993) The metaphase II arrest in mouse oocytes is controlled through microtubule-dependent destruction of cyclin B in the presence of CSF. EMBO J 12, 3773–3778
    OpenUrlPubMedWeb of Science
    1. Laemmli U. K.
    (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 277, 680–685
    OpenUrl
    1. Lorca T.,
    2. Labbe J.-C.,
    3. Devault A.,
    4. Fesquet D.,
    5. Capony J.-P.,
    6. Cavadore J.-C.,
    7. Le Bouffant F.,
    8. Doree M.
    (1992) Dephosphorylation of cdc2 on threonine161 is required for cdc2 kinase inactivation and normal anaphase. EMBO J 11, 2381–2390
    OpenUrlPubMedWeb of Science
    1. Luca F. C.,
    2. Shibuya E. K.,
    3. Dohrmann C. E.,
    4. Ruderman J. V.
    (1991) Both cyclin A 60 and B 97 are stable and arrest cells in M-phase, but only cyclin B 97 turns on cyclin destruction. EMBO J 10, 4311–4320
    OpenUrlPubMedWeb of Science
    1. Meijer L.,
    2. Arion D.,
    3. Golsteyn R.,
    4. Pines J.,
    5. Brizuela L.,
    6. Hunt T.,
    7. Beach D.
    (1989) Cyclin is a component of the sea urchin egg M-phase specific histone H1 kinase. EMBO J 8, 2275–2282
    OpenUrlPubMedWeb of Science
    1. Moreno S.,
    2. Hayles J.,
    3. Nurse P.
    (1989) Regulation of p34cdc2protein kinase during mitosis. Cell 58, 361–372
    OpenUrlCrossRefPubMedWeb of Science
    1. Motlik J.,
    2. Crozet N.,
    3. Fulka J.
    (1984) Meiotic competence in vitro of pig oocytes isolated from early antral follicles. J. Reprod. Fert 72, 323–328
    OpenUrlAbstract/FREE Full Text
    1. Murray A. W.,
    2. Kirschner M. W.
    (1989) Cyclin synthesis drives the early embryonic cell cycle. Nature 339, 275–280
    OpenUrlCrossRefPubMed
    1. Murray A. W.,
    2. Solomon M. J.,
    3. Kirschner M. W.
    (1989) The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 339, 280–286
    OpenUrlCrossRefPubMed
    1. Muschel R. J.,
    2. Zhang H. B.,
    3. McKenna W. G.
    (1993) Differential effect of ionizing radiation on the expression of cyclin A and cyclin B in HeLa cells. Cancer Res 53, 1128–1135
    OpenUrlAbstract/FREE Full Text
    1. Norbury C.,
    2. Nurse P.
    (1992) Animal cell cycles and their control. Ann. Rev. Biochem 61, 441–470
    OpenUrlCrossRefPubMedWeb of Science
    1. O'Keefe S. J.,
    2. Kiessling A. A.,
    3. Cooper G. M.
    (1991) The c-mos gene product is required for cyclin B accumulation during meiosis of mouse eggs. Proc. Natl. Acad. Sci. USA 88, 7869–7872
    OpenUrlAbstract/FREE Full Text
    1. O'Neill G. T.,
    2. Kaufman M. H.
    (1987) Ovulation and fertilization of primary and secondary oocytes in LT/Sv strain mice. Gamete Res 18, 27–36
    OpenUrlCrossRefPubMedWeb of Science
    1. Pines J.
    (1991) Cyclins: wheels within wheels. Cell Growth Differ 2, 305–310
    OpenUrlPubMedWeb of Science
    1. Rime H.,
    2. Neant I.,
    3. Guerrier P.,
    4. Ozon R.
    (1989) 6-Dimethylaminopurine (6-DMAP), a reversible inhibitor of the transition to metaphase during the first meiotic division of the mouse oocyte. Dev. Biol 133, 169–179
    OpenUrlCrossRefPubMedWeb of Science
    1. Schramm R. D.,
    2. Tennier M. T.,
    3. Boatman D. E.,
    4. Bavister B. D.
    (1993) Chromatin configurations and meiotic competence of oocytes are related to follicular diameter in nonstimulated rhesus monkeys. Biol. Reprod 48, 349–356
    OpenUrlAbstract
    1. Solomon M. J.,
    2. Glotzer M.,
    3. Lee T. H.,
    4. Philippe M.,
    5. Kirschner M. W.
    (1990) Cyclin activation of p34 cdc2. Cell 63, 1013–1024
    OpenUrlCrossRefPubMedWeb of Science
    1. Sorensen R. A.,
    2. Wassarman P. M.
    (1976) Relationship between growth and meiotic maturation of the mouse oocyte. Dev. Biol 50, 531–536
    OpenUrlCrossRefPubMedWeb of Science
    1. Szöllösi M. S.,
    2. Debey P.,
    3. Szöllösi D.,
    4. Rime H.,
    5. Vautier D.
    (1991) Chromatin behaviour under influence of puromycin and 6-DMAP at different stages of mouse oocyte maturation. Chromosoma 100, 339–354
    OpenUrlCrossRefPubMedWeb of Science
    1. Szöllösi M. S.,
    2. Kubiak J. Z.,
    3. Debey P.,
    4. Depennart H.,
    5. Szöllösi D.,
    6. Maro B.
    (1993) Inhibition of protein kinases by 6-dimethylaminopurine accelerates the transition to interphase in activated mouse oocytes. J. Cell Sci 104, 861–872
    OpenUrlAbstract/FREE Full Text
    1. Weber M.,
    2. Kubiak J. Z.,
    3. Arlinghaus R. B.,
    4. Pines J.,
    5. Maro B.
    (1991) c-mos proto-oncogene product is partly degraded after release from meiotic arrest and persists during interphase in mouse zygotes. Dev. Biol 148, 393–397
    OpenUrlCrossRefPubMed
    1. West J. D.,
    2. Webb S.,
    3. Kaufman M. H.
    (1993) Inheritance of a meiotic abnormality that causes the ovulation of primary oocytes and the production of digynic triploid mice. Genet. Res 62, 183–193
    OpenUrlPubMedWeb of Science
    1. Whitten W. K.
    (1971) Nutrient requirements for culture of preimplantation embryos in vitro. Advan. Biosci 6, 129–139
    OpenUrl
    1. Wickramasinghe D.,
    2. Ebert K. M.,
    3. Albertini D. F.
    (1991) Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes. Dev. Biol 143, 162–172
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Analysis of the mechanism(s) of metaphase I arrest in maturing mouse oocytes
A. Hampl, J.J. Eppig
Development 1995 121: 925-933;
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JOURNAL ARTICLES
Analysis of the mechanism(s) of metaphase I arrest in maturing mouse oocytes
A. Hampl, J.J. Eppig
Development 1995 121: 925-933;

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