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New B-type cyclin synthesis is required between meiosis I and II during Xenopus oocyte maturation

Helfrid Hochegger¹, Andrea Klotzbücher², Jane Kirk¹, Mike Howell¹, Katherine le Guellec^3,*, Kate Fletcher¹, Tod Duncan¹, Muhammad Sohail⁴ and Tim Hunt^1,

¹ ICRF Clare Hall Laboratories, South Mimms, Hertfordshire EN6 3LD, UK
² Institut für Molekulare Medizin, Klinik für Tumorbiologie, Universität Freiburg, Breisacher Strasse 117, 79121 Freiburg, Germany
³ Unité de Biologie et Genetique du Development, CNRS UPR 41, Université Rennes I, Avenue du General Leclerc, 35042 Rennes, France
⁴ Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK
^* Deceased June 2001

Author for correspondence (e-mail: tim.hunt{at}icrf.icnet.uk)

Accepted July 5, 2001

Progression through meiosis requires two waves of maturation promoting factor (MPF) activity corresponding to meiosis I and meiosis II. Frog oocytes contain a pool of inactive ‘pre-MPF’ consisting of cyclin-dependent kinase 1 bound to B-type cyclins, of which we now find three previously unsuspected members, cyclins B3, B4 and B5. Protein synthesis is required to activate pre-MPF, and we show here that this does not require new B-type cyclin synthesis, probably because of a large maternal stockpile of cyclins B2 and B5. This stockpile is degraded after meiosis I and consequently, the activation of MPF for meiosis II requires new cyclin synthesis, principally of cyclins B1 and B4, whose translation is strongly activated after meiosis I. If this wave of new cyclin synthesis is ablated by antisense oligonucleotides, the oocytes degenerate and fail to form a second meiotic spindle. The effects on meiotic progression are even more severe when all new protein synthesis is blocked by cycloheximide added after meiosis I, but can be rescued by injection of indestructible B-type cyclins. B-type cyclins and MPF activity are required to maintain c-mos and MAP kinase activity during meiosis II, and to establish the metaphase arrest at the end of meiotic maturation. We discuss the interdependence of c-mos and MPF, and reveal an important role for translational control of cyclin synthesis between the two meiotic divisions.

Key words: Cell cycle, Meiosis, Maturation promoting factor, Eg-2, c-mos, Antisense oligonuceotides, Cycloheximide, Cyclin-dependent kinase, Xenopus laevis, Xenopus tropicalis

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