Control of chromosome behavior in amphibian oocytes. II. The effect of inhibitors of RNA and protein synthesis on the induction of chromosome condensation in transplanted brain nuclei by oocyte cytoplasm.

Ziegler, David H.; Masui, Yoshio

doi:10.1083/jcb.68.3.620

Cited by 58 publications

(25 citation statements)

References 15 publications

(8 reference statements)

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“…Thus, it seems very likely that while nuclear material is dispensable for surface changes such as cortical maturity, it is indispensable for MPF reactivation or entry into meiosis II, in (amphibian) oocytes. In this regard, we note that, unlike normal counterparts arrested at metaphase II, mature enucleated oocytes from both amphibians and mice cannot stably condense exogenously introduced chromatin (25,40), which probably reflects a lack of (stable) MPF in such oocytes (25).…”

Section: Discussionmentioning

confidence: 99%

Essential role of germinal vesicle material in the meiotic cell cycle of Xenopus oocytes

Iwashita

Hayano

Sagata

1998

Proc. Natl. Acad. Sci. U.S.A.

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In almost all animal species, immature oocytes are arrested naturally in the first meiotic prophase, with a large nucleus called the germinal vesicle. A number of previous studies showed that both activation of maturation͞M phase-promoting factor (MPF) (assayed by semiquantitative cytological methods) and some other maturational events occur essentially normally in enucleated oocytes from many amphibian species and mice. Hence, for nearly three decades, it has generally been believed that nuclear material is dispensable for MPF activation and the meiotic cell cycle in vertebrate oocytes. Here, we have challenged this view by examining the histone H1 kinase activities and the molecular forms of MPF in experimentally manipulated Xenopus oocytes. We show that oocytes injected with nuclear material undergo much more rapid MPF activation and maturation than uninjected control oocytes. Conversely, enucleated oocytes, unlike nucleated counterparts, undergo only weak MPF activation in meiosis I and no detectable MPF reactivation in meiosis II, the latter accompanying inhibitory tyrosine phosphorylation of cdc2 kinase, the catalytic subunit of MPF. These results argue strongly that nuclear material is indispensable for the meiotic cell cycle, particularly MPF reactivation (or cdc2 tyrosine dephosphorylation) on entry into meiosis II, in Xenopus oocytes. The classical and general view may thus need reconsideration.

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Section: Discussionmentioning

confidence: 99%

Essential role of germinal vesicle material in the meiotic cell cycle of Xenopus oocytes

Iwashita

Hayano

Sagata

1998

Proc. Natl. Acad. Sci. U.S.A.

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“…8 Chromosomes condensed to a metaphase state from brain nuclei injected into a maturing oocyte with MPF (Ziegler and Masui, 1976a). 8 Chromosomes condensed to a metaphase state from brain nuclei injected into a maturing oocyte with MPF (Ziegler and Masui, 1976a).…”

Section: The Ubiquitous Role Of Mpf In the Control Of Nuclear Activitymentioning

confidence: 99%

From oocyte maturation to the in vitro cell cycle: the history of discoveries of Maturation-Promoting Factor (MPF) and Cytostatic Factor (CSF)

2001

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“…The latter two pathways can be uncoupled from the meiotic maturation process, and cooperate with each other to develop the DNA-replication inducing activity during MI, which will probably play an essential role in initiating S phase after fertilization. However, in Rana pipiens oocytes, it has been reported that transcriptional inhibition prevents chromosome condensation (15). As we did not perform cytological analysis, it is possible that transcription during early MI is also required for chromosome condensation in Xenopus oocytes.…”

Section: Discussionmentioning

confidence: 82%

“…During maturation, protein expression is mostly regulated at the translational level (7, 9 -11) by polyadenylation of the pre-existing mRNAs (12), or by unmasking translationally silent mRNAs (13). Inhibition of transcription has little effect on activation of MPF and initiation of meiotic maturation in response to PG (10,14,15). Therefore, although relatively high levels of transcription (mostly of rRNA) occur during MI (16,17), this has been assumed simply to enable enough RNA to accumulate for early embryonic development.…”

mentioning

confidence: 99%

Transcription Factor E2F and Cyclin E-Cdk2 Complex Cooperate to Induce Chromosomal DNA Replication in Xenopus Oocytes

Akamatsu

Tanaka

Kato

1998

Journal of Biological Chemistry

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Although no chromosomal DNA replication actually occurs during Xenopus oocyte maturation, the capability develops during the late meiosis I (MI) phase in response to progesterone. This ability, however, is suppressed by Mos proteins and maturation/mitosis promoting factor during the second meiosis phase (meiosis II; MII) until fertilization. Inhibition of RNA synthesis by actinomycin D during early MI prevented induction of the replication ability, but did not interfere with initiation of the meiotic cell cycle progression characterized by oscillation of the maturation/mitosis promoting factor activity and germinal vesicle breakdown. Microinjection of recombinant proteins such as dominantnegative E2F or universal Cdk inhibitors, p21 and p27, but not wild type human E2F-1 or Cdk4-specific inhibitor, p19, into maturing oocytes during MI abolished induction of the DNA replication ability. Co-injection of human E2F-1 and cyclin E proteins into immature oocytes allowed them to initiate DNA replication even in the absence of progesterone treatment. Injection of cyclin E alone, which was sufficient to activate endogenous Cdk2 kinase, failed to induce DNA replication. Moreover, the activation of Cdk2 was not affected under the conditions where DNA replication was blocked by actinomycin D. Thus, like somatic cells, both activities of E2F and cyclin E-Cdk2 complex are required for induction of the DNA replication ability in maturing Xenopus oocytes, and enhancement of both activities enables oocytes to override DNA-replication inhibitory mechanisms that specifically lie in maturing oocytes.

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Control of chromosome behavior in amphibian oocytes. II. The effect of inhibitors of RNA and protein synthesis on the induction of chromosome condensation in transplanted brain nuclei by oocyte cytoplasm.

Cited by 58 publications

References 15 publications

Essential role of germinal vesicle material in the meiotic cell cycle of Xenopus oocytes

Essential role of germinal vesicle material in the meiotic cell cycle of Xenopus oocytes

From oocyte maturation to the in vitro cell cycle: the history of discoveries of Maturation-Promoting Factor (MPF) and Cytostatic Factor (CSF)

Transcription Factor E2F and Cyclin E-Cdk2 Complex Cooperate to Induce Chromosomal DNA Replication in Xenopus Oocytes

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