MATURATION HORMONE-INDUCED AN INCREASE IN THE TRANSLATIONAL ACTIVITY OF STARFISH OOCYTES COINCIDENT WITH THE PHOSPHORYLATION OF THE MESSENGER-RNA CAP-BINDING PROTEIN, EIF-4E, AND THE ACTIVATION OF SEVERAL KINASES

The stimulation of translation in starfish oocytes by the maturation h ormone, 1-methyladenine (1-MA), requires the activation or mobilizatio n of both initiation factors and mRNAs [Xu and Hille, Cell Regul. 1:10 57, 1990]. We identify here the translational initiation complex, elF- 4F, and the guanine nucleotide exchange factor for elf-2, elF-2B, as t he rate controlling components of protein synthesis in immature oocyte s of the starfish, Pisaster orchraceus. Increased phosphorylation of e lf-4E, the cap binding subunit of the elF-4F complex, is coincident wi th the initial increase in translational activity during maturation of these oocytes. Significantly, protein kinase C activity increased dur ing oocyte maturation in parallel with the increase in elF-4E phosphor ylation and protein synthesis. An increase in the activities of cdc2 k inase and mitogen-activated myelin basic protein kinase (MBP kinase) s imilarly coincide with the increase in elf-4E phosphorylation. However , neither cdc2 kinase nor MBP kinase phosphorylates elF-4E in vitro. C asein kinase II activity does not change during oocyte maturation, and therefore, cannot be responsible for the activation of translation. T reatment of oocytes with phorbol 12-myristate 13-acetate, an activator of protein kinase C, for 30 min prior to the addition of 1-MA resulte d in the inhibition of 1-MA-induced phosphorylation of elF-4E, transla tional activation, and germinal vesicle breakdown. Therefore, protein kinase C may phosphorylate elF-4E, after very early events of maturati on. Another possibility is that elF-4E is phosphorylated by an unknown kinase that is activated by the cascade of reactions stimulated by 1- MA. In conclusion, our results suggest a role for the phosphorylation of elF-4E in the activation of translation during maturation, similar to translational regulation during the stimulation of growth in mammal ian cells. (C) 1993 Wiley-Liss, Inc.