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J. Biol. Chem., Vol. 278, Issue 43, 42505-42514, October 24, 2003

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The M-phase-promoting Factor Modulates the Sensitivity of the Ca²⁺ Stores to Inositol 1,4,5-Trisphosphate via the Actin Cytoskeleton^*

Dmitri Lim, Emanuela Ercolano, Keiichiro Kyozuka, Gilda A. Nusco, Francesco Moccia, Klaus Lange¶, and Luigia Santella||

From the Laboratory of Cell Biology, Stazione Zoologica A. Dohrn, I-80121 Naples, Italy, the Asamushi Marine Biological Station, Aomori 039-3501, Japan, and ^¶Kladower Damn 25b, 14089 Berlin, Germany

The resumption of the meiotic cycle (maturation) induced by 1-methyladenine in prophase-arrested starfish oocytes is indicated by the breakdown of the germinal vesicle and is characterized by the increased sensitivity of the Ca²⁺ stores to inositol 1,4,5-trisphosphate (InsP₃) to InsP₃ starting at the animal hemisphere (where the germinal vesicle was originally located) and propagating along the animal/vegetal axis of the oocyte. This initiates Ca²⁺ signals around the germinal vesicle before nuclear envelope breakdown. Previous studies have suggested that the final activation of the maturation-promoting factor (MPF), a cyclin-dependent kinase, which is the major element controlling the entry of eukaryotic cells into the M phase, occurs in the nucleus. MPF is then exported to the cytoplasm where its activity is autocatalytically amplified following a similar animal/vegetal spatial pattern. We have investigated whether activated MPF was involved in the increased sensitivity of the Ca²⁺ response to InsP₃. We have found that the development of increased sensitivity of the Ca²⁺ stores to InsP₃ receptors together with the Ca²⁺ signals in the perinuclear region was blocked in oocytes treated with the specific MPF inhibitor roscovitine. That the nuclear MPF activation is indeed required for changes of the InsP₃ receptors sensitivity was shown by enucleating or by dissecting oocytes into vegetal and animal hemispheres prior to the addition of 1-MA. MPF activity 50 min after 1-methyladenine addition was much lower in the enucleated oocytes and in the vegetal hemisphere, which did not contain the germinal vesicle, as compared with the animal hemisphere, which did contain it. The Ca²⁺ increase induced by InsP₃ under these experimental conditions correlated with the changes in actin cytoskeleton induced by MPF.

Received for publication, February 21, 2003 , and in revised form, June 18, 2003.

^* 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.: 39-081-5833-289; Fax: 39-081-7641-355; E-mail: santella{at}szn.it.

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