Differential regulation of histone H1 and ribosomal S6 kinases during sea star oocyte maturation.

In the preceding paper [Pelech, S.L., Meijer, L., & Krebs, E.G. (1987) Biochemistry (preceding paper in this issue)], at least three activated kinases were detected in soluble extracts from sea star oocytes induced to undergo maturation by 1-methyladenine (1-MeAde). Coincident with nuclear envelope breakdown (20 min after exposure to 1-MeAde), there was a rapid activation of a histone H1 kinase that eluted from DEAE-Sephacel with a conductivity of approximately 6 mmho. By contrast, 60-min treatment of the oocytes with 1-MeAde was required for maximal activation of two kinases, each of which phosphorylated a synthetic peptide, Arg-Arg-Leu-Ser-Ser-Leu-Arg-Ala (RRLSSLRA), patterned after a phosphorylation site sequence from ribosomal protein S6. These RRLSSLRA kinases were released from DEAE-Sephacel with elution conductivities of approximately 6 and approximately 10.5 mmho. The 1-MeAde dose-response curves for maturation induction and activation of the histone H1 and RRLSSLRA kinases were superimposable. Both oocyte maturation and the activation of the kinases required the presence of 1-MeAde during the hormone-dependent period. When 1-MeAde was removed after this period, full histone H1 kinase activation still occurred and maturation was induced. Forskolin pretreatment of the oocytes, by elevating the basal cAMP level more than 35-fold, doubled the hormone-dependent period and similarly delayed the onset of histone H1 kinase activation by 1-MeAde. However, postmaturation activation of the RRLSSLRA kinases was completely blocked by forskolin.(ABSTRACT TRUNCATED AT 250 WORDS)