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J. Biol. Chem., Vol. 279, Issue 18, 18633-18640, April 30, 2004

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Degradation of Polyubiquitinated Cyclin B Is Blocked by the MAPK Pathway at the Metaphase I Arrest in Starfish Oocytes^*

Eiko Oita, Kaori Harada, and Kazuyoshi Chiba

From the Department of Biology, Ochanomizu University, 2-1-1 Ohtsuka, Tokyo 112-8610, Japan

In the starfish ovary, maturing oocytes stimulated by 1-methyladenine undergo synchronous germinal vesicle breakdown and then arrest in metaphase of the first meiotic division (metaphase I). Immediately after spawning, an increase of intracellular pH (pH_i) from 7.0 to 7.3 is induced by Na⁺/H⁺ antiporter in oocytes, and meiosis reinitiation occurs. Here we show that an endogenous substrate of the proteasome, polyubiquitinated cyclin B, was stable at pH 7.0, whereas it was degraded at pH 7.3. When the MAPK pathway was blocked by MEK inhibitor U0126, degradation of polyubiquitinated cyclin B occurred even at pH 7.0 without an increase of the peptidase activity of the proteasome. These results indicate that the proteasome activity at pH 7.0 is sufficient for degradation of polyubiquitinated cyclin B and that the MAPK pathway blocks the degradation of polyubiquitinated cyclin B in the maturing oocytes in the ovary. Immediately after spawning, the increase in pH_i mediated by Na⁺/H⁺ antiporter cancels the inhibitory effects of the MAPK pathway, resulting in the degradation of polyubiquitinated cyclin B and the release of the arrest. Thus, the key step of metaphase I arrest in starfish oocytes occurs after the polyubiqutination of cyclin B but before cyclin B proteolysis by the proteasome.

Received for publication, October 9, 2003 , and in revised form, February 23, 2004.

^* This work was supported by a grant from the Human Frontier Science program, grants from the Ministry of Education, Culture, Sports, and Sciences of Japan, and funds from the Cooperative Program provided by the Ocean Research Institute, University of Tokyo. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed. Tel.: 81-3-5978-5370; Fax: 81-3-5978-5370; E-mail: kchiba{at}cc.ocha.ac.jp.

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