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J. Biol. Chem., Vol. 281, Issue 48, 37117-37129, December 1, 2006

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Cyclooxygenase-2-derived Prostaglandin E₂ Directs Oocyte Maturation by Differentially Influencing Multiple Signaling Pathways^*

Toshifumi Takahashi¹, Jason D. Morrow, Haibin Wang², and Sudhansu K. Dey^¶3

From the Departments of Pediatrics, Pharmacology, and ^¶Cell and Developmental Biology, Division of Reproductive and Developmental Biology, Vanderbilt University Medical Center, Nashville, Tennessee 37232

The process of oocyte maturation, which impacts ovulation and fertilization, is complex and requires an integration of the endocrine, paracrine, juxtacrine, and autocrine signaling pathways. This process involves an intimate interaction between the oocyte and encircling cumulus cells within a follicle, a unique venue for somatic and germ cell communication. Cumulus cell expansion and resumption of meiosis with germinal vesicle breakdown are major events in oocyte maturation. Cyclooxygenase-2 (COX-2)-derived prostaglandin E₂ (PGE₂) is a known critical mediator of oocyte maturation, but the diverse function of this lipid mediator in oocyte maturation, ovulation, and fertilization has not been fully appreciated. We show here that gonadotropins in coordination with PGE₂ signaling via its cell surface G-protein-coupled EP2 and EP4 receptor subtypes direct cumulus cell expansion and survival and oocyte meiotic maturation by differentially impacting cAMP-dependent protein kinase, MAPK, NF-B, and phosphatidylinositol 3-kinase/Akt pathways. This study is unique in the sense that it provides evidence for new site- and event-specific involvement of these signaling pathways under the influence of COX-2-derived PGE₂ during the critical stages of this somatic-germ cell interaction, an absolute requirement for oocyte maturation.

Received for publication, August 25, 2006 , and in revised form, September 27, 2006.

^* This work was supported in part by National Institutes of Health Grants, HD12304, HD33994, HD050315, and P01-CA-77839. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. 1 and 2.

¹ Present address: Dept. of Obstetrics and Gynecology, Yamagata University School of Medicine, 2-2-2 Iidanishi, Yamagata 990-9585, Japan.

² Recipient of the Solvay-Mortola research award from the Society for Gynecologic Investigation.

³ Recipient of Method to Extend Research in Time (MERIT) award from the NICHD, National Institutes of Health. To whom correspondence should be addressed. E-mail: sk.dey{at}vanderbilt.edu.

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