The Mitogen-Activated Protein Kinase Signaling Pathway Stimulates Mos mRNA Cytoplasmic Polyadenylation during Xenopus Oocyte Maturation

• Published in: Molecular and cellular biology Vol. 19; no. 3; pp. 1990 - 1999
• Main Authors: Howard, Emily L., Charlesworth, Amanda, Welk, Joseph, MacNicol, Angus M.
• Format: Journal Article
• Language: English
• Published: United States Taylor & Francis 01.03.1999; American Society for Microbiology
• Subjects: Animals; Calcium-Calmodulin-Dependent Protein Kinases - metabolism; Cell Growth and Development; Cyclin B - genetics; Cyclin B1; Cytoplasm; Freshwater; Maturation-Promoting Factor - metabolism; Oocytes - physiology; Poly A; Protein Biosynthesis; Proto-Oncogene Proteins c-mos - genetics; RNA, Messenger; Signal Transduction; Xenopus
• ISSN: 1098-5549; 0270-7306; 1098-5549
• DOI: 10.1128/MCB.19.3.1990

The Mos protein kinase is a key regulator of vertebrate oocyte maturation. Oocyte-specific Mos protein expression is subject to translational control. In the frog Xenopus, the translation of Mos protein requires the progesterone-induced polyadenylation of the maternal Mos mRNA, which is present in the oocyte cytoplasm. Both the Xenopus p42 mitogen-activated protein kinase (MAPK) and maturation-promoting factor (MPF) signaling pathways have been proposed to mediate progesterone-stimulated oocyte maturation. In this study, we have determined the relative contributions of the MAPK and MPF signaling pathways to Mos mRNA polyadenylation. We report that progesterone-induced Mos mRNA polyadenylation was attenuated in oocytes expressing the MAPK phosphatase rVH6. Moreover, inhibition of MAPK signaling blocked progesterone-induced Mos protein accumulation. Activation of the MAPK pathway by injection of RNA encoding Mos was sufficient to induce both the polyadenylation of synthetic Mos mRNA substrates and the accumulation of endogenous Mos protein in the absence of MPF signaling. Activation of MPF, by injection of cyclin B1 RNA or purified cyclin B1 protein, also induced both Mos protein accumulation and Mos mRNA polyadenylation. However, this action of MPF required MAPK activity. By contrast, the cytoplasmic polyadenylation of maternal cyclin B1 mRNA was stimulated by MPF in a MAPK-independent manner, thus revealing a differential regulation of maternal mRNA polyadenylation by the MAPK and MPF signaling pathways. We propose that MAPK-stimulated Mos mRNA cytoplasmic polyadenylation is a key component of the positive-feedback loop, which contributes to the all-or-none process of oocyte maturation.