Abstract
We have measured the levels of cyclin mRNAs and polypeptides during oogenesis, progesterone-induced oocyte maturation, and immediately after egg activation in the frog, Xenopus laevis. The mRNA for each cyclin is present at a constant level of approximately 5 x 10(7) molecules per oocyte from the earliest stages of oogenesis until after fertilization. The levels of polypeptides show more complex patterns of accumulation. The B-type cyclins are first detectable in stage IV and V oocytes. Cyclin B2 polypeptide is present at approximately 2 x 10(9) molecules (150 pg) per oocyte by stage VI. The amount increases after progesterone treatment, but returns to its previous level after GVBD and undergoes no further change until it is destroyed at fertilization. Cyclin B1 is present at 4 x 10(8) molecules per oocyte in stage VI oocytes, and rises steadily during maturation, ultimately reaching similar levels to cyclin B2 in unfertilized eggs. Unlike the B-type cyclins, cyclin A is barely detectable in stage VI oocytes, and only starts to be made in significant amounts after oocytes are exposed to progesterone. A portion of all the cyclins are destroyed after germinal vesicle breakdown (GVBD), and cyclins B1 and B2 also experience posttranslational modifications during oocyte maturation. Progesterone strongly stimulates both cyclin and p34cdc2 synthesis in these oocytes, but whereas cyclin synthesis continues in eggs and after fertilization, synthesis of p34cdc2 declines strongly after GVBD. The significance of these results is discussed in terms of the activation and inactivation of maturation-promoting factor.
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- Anderson C. W., Baum P. R., Gesteland R. F. Processing of adenovirus 2-induced proteins. J Virol. 1973 Aug;12(2):241–252. doi: 10.1128/jvi.12.2.241-252.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brizuela L., Draetta G., Beach D. p13suc1 acts in the fission yeast cell division cycle as a component of the p34cdc2 protein kinase. EMBO J. 1987 Nov;6(11):3507–3514. doi: 10.1002/j.1460-2075.1987.tb02676.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cyert M. S., Kirschner M. W. Regulation of MPF activity in vitro. Cell. 1988 Apr 22;53(2):185–195. doi: 10.1016/0092-8674(88)90380-7. [DOI] [PubMed] [Google Scholar]
- Dorée M., Peaucellier G., Picard A. Activity of the maturation-promoting factor and the extent of protein phosphorylation oscillate simultaneously during meiotic maturation of starfish oocytes. Dev Biol. 1983 Oct;99(2):489–501. doi: 10.1016/0012-1606(83)90298-1. [DOI] [PubMed] [Google Scholar]
- Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
- Dunphy W. G., Brizuela L., Beach D., Newport J. The Xenopus cdc2 protein is a component of MPF, a cytoplasmic regulator of mitosis. Cell. 1988 Jul 29;54(3):423–431. doi: 10.1016/0092-8674(88)90205-x. [DOI] [PubMed] [Google Scholar]
- Dunphy W. G., Newport J. W. Fission yeast p13 blocks mitotic activation and tyrosine dephosphorylation of the Xenopus cdc2 protein kinase. Cell. 1989 Jul 14;58(1):181–191. doi: 10.1016/0092-8674(89)90414-5. [DOI] [PubMed] [Google Scholar]
- Erikson E., Maller J. L. Biochemical characterization of the p34cdc2 protein kinase component of purified maturation-promoting factor from Xenopus eggs. J Biol Chem. 1989 Nov 25;264(33):19577–19582. [PubMed] [Google Scholar]
- Freeman R. S., Kanki J. P., Ballantyne S. M., Pickham K. M., Donoghue D. J. Effects of the v-mos oncogene on Xenopus development: meiotic induction in oocytes and mitotic arrest in cleaving embryos. J Cell Biol. 1990 Aug;111(2):533–541. doi: 10.1083/jcb.111.2.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Félix M. A., Labbé J. C., Dorée M., Hunt T., Karsenti E. Triggering of cyclin degradation in interphase extracts of amphibian eggs by cdc2 kinase. Nature. 1990 Jul 26;346(6282):379–382. doi: 10.1038/346379a0. [DOI] [PubMed] [Google Scholar]
- Gautier J., Maller J. L. Cyclin B in Xenopus oocytes: implications for the mechanism of pre-MPF activation. EMBO J. 1991 Jan;10(1):177–182. doi: 10.1002/j.1460-2075.1991.tb07934.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gautier J., Minshull J., Lohka M., Glotzer M., Hunt T., Maller J. L. Cyclin is a component of maturation-promoting factor from Xenopus. Cell. 1990 Feb 9;60(3):487–494. doi: 10.1016/0092-8674(90)90599-a. [DOI] [PubMed] [Google Scholar]
- Gerhart J., Wu M., Kirschner M. Cell cycle dynamics of an M-phase-specific cytoplasmic factor in Xenopus laevis oocytes and eggs. J Cell Biol. 1984 Apr;98(4):1247–1255. doi: 10.1083/jcb.98.4.1247. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Golden L., Schafer U., Rosbash M. Accumulation of individual pA+ RNAs during oogenesis of Xenopus laevis. Cell. 1980 Dec;22(3):835–844. doi: 10.1016/0092-8674(80)90560-7. [DOI] [PubMed] [Google Scholar]
- Gould K. L., Nurse P. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature. 1989 Nov 2;342(6245):39–45. doi: 10.1038/342039a0. [DOI] [PubMed] [Google Scholar]
- Gurdon J. B., Wickens M. P. The use of Xenopus oocytes for the expression of cloned genes. Methods Enzymol. 1983;101:370–386. doi: 10.1016/0076-6879(83)01028-9. [DOI] [PubMed] [Google Scholar]
- Labbé J. C., Capony J. P., Caput D., Cavadore J. C., Derancourt J., Kaghad M., Lelias J. M., Picard A., Dorée M. MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. EMBO J. 1989 Oct;8(10):3053–3058. doi: 10.1002/j.1460-2075.1989.tb08456.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lehner C. F., O'Farrell P. H. The roles of Drosophila cyclins A and B in mitotic control. Cell. 1990 May 4;61(3):535–547. doi: 10.1016/0092-8674(90)90535-m. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maller J. L. Xenopus oocytes and the biochemistry of cell division. Biochemistry. 1990 Apr 3;29(13):3157–3166. doi: 10.1021/bi00465a001. [DOI] [PubMed] [Google Scholar]
- Masui Y., Markert C. L. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool. 1971 Jun;177(2):129–145. doi: 10.1002/jez.1401770202. [DOI] [PubMed] [Google Scholar]
- Meijer L., Guerrier P. Maturation and fertilization in starfish oocytes. Int Rev Cytol. 1984;86:129–196. doi: 10.1016/s0074-7696(08)60179-5. [DOI] [PubMed] [Google Scholar]
- Miake-Lye R., Newport J., Kirschner M. Maturation-promoting factor induces nuclear envelope breakdown in cycloheximide-arrested embryos of Xenopus laevis. J Cell Biol. 1983 Jul;97(1):81–91. doi: 10.1083/jcb.97.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Minshull J., Blow J. J., Hunt T. Translation of cyclin mRNA is necessary for extracts of activated xenopus eggs to enter mitosis. Cell. 1989 Mar 24;56(6):947–956. doi: 10.1016/0092-8674(89)90628-4. [DOI] [PubMed] [Google Scholar]
- Minshull J., Golsteyn R., Hill C. S., Hunt T. The A- and B-type cyclin associated cdc2 kinases in Xenopus turn on and off at different times in the cell cycle. EMBO J. 1990 Sep;9(9):2865–2875. doi: 10.1002/j.1460-2075.1990.tb07476.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Minshull J., Murray A., Colman A., Hunt T. Xenopus oocyte maturation does not require new cyclin synthesis. J Cell Biol. 1991 Aug;114(4):767–772. doi: 10.1083/jcb.114.4.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Minshull J., Pines J., Golsteyn R., Standart N., Mackie S., Colman A., Blow J., Ruderman J. V., Wu M., Hunt T. The role of cyclin synthesis, modification and destruction in the control of cell division. J Cell Sci Suppl. 1989;12:77–97. doi: 10.1242/jcs.1989.supplement_12.8. [DOI] [PubMed] [Google Scholar]
- Murray A. W., Kirschner M. W. Cyclin synthesis drives the early embryonic cell cycle. Nature. 1989 May 25;339(6222):275–280. doi: 10.1038/339275a0. [DOI] [PubMed] [Google Scholar]
- Newport J. W., Kirschner M. W. Regulation of the cell cycle during early Xenopus development. Cell. 1984 Jul;37(3):731–742. doi: 10.1016/0092-8674(84)90409-4. [DOI] [PubMed] [Google Scholar]
- Nurse P. Universal control mechanism regulating onset of M-phase. Nature. 1990 Apr 5;344(6266):503–508. doi: 10.1038/344503a0. [DOI] [PubMed] [Google Scholar]
- Paris J., Le Guellec R., Couturier A., Le Guellec K., Omilli F., Camonis J., MacNeill S., Philippe M. Cloning by differential screening of a Xenopus cDNA coding for a protein highly homologous to cdc2. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):1039–1043. doi: 10.1073/pnas.88.3.1039. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Paris J., Philippe M. Poly(A) metabolism and polysomal recruitment of maternal mRNAs during early Xenopus development. Dev Biol. 1990 Jul;140(1):221–224. doi: 10.1016/0012-1606(90)90070-y. [DOI] [PubMed] [Google Scholar]
- Pines J., Hunt T. Molecular cloning and characterization of the mRNA for cyclin from sea urchin eggs. EMBO J. 1987 Oct;6(10):2987–2995. doi: 10.1002/j.1460-2075.1987.tb02604.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pines J., Hunter T. p34cdc2: the S and M kinase? New Biol. 1990 May;2(5):389–401. [PubMed] [Google Scholar]
- Roy L. M., Swenson K. I., Walker D. H., Gabrielli B. G., Li R. S., Piwnica-Worms H., Maller J. L. Activation of p34cdc2 kinase by cyclin A. J Cell Biol. 1991 May;113(3):507–514. doi: 10.1083/jcb.113.3.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sagata N., Daar I., Oskarsson M., Showalter S. D., Vande Woude G. F. The product of the mos proto-oncogene as a candidate "initiator" for oocyte maturation. Science. 1989 Aug 11;245(4918):643–646. doi: 10.1126/science.2474853. [DOI] [PubMed] [Google Scholar]
- Smith L. D., Ecker R. E. The interaction of steroids with Rana pipiens Oocytes in the induction of maturation. Dev Biol. 1971 Jun;25(2):232–247. doi: 10.1016/0012-1606(71)90029-7. [DOI] [PubMed] [Google Scholar]
- Solomon M. J., Glotzer M., Lee T. H., Philippe M., Kirschner M. W. Cyclin activation of p34cdc2. Cell. 1990 Nov 30;63(5):1013–1024. doi: 10.1016/0092-8674(90)90504-8. [DOI] [PubMed] [Google Scholar]
- Standart N., Minshull J., Pines J., Hunt T. Cyclin synthesis, modification and destruction during meiotic maturation of the starfish oocyte. Dev Biol. 1987 Nov;124(1):248–258. doi: 10.1016/0012-1606(87)90476-3. [DOI] [PubMed] [Google Scholar]
- Swenson K. I., Farrell K. M., Ruderman J. V. The clam embryo protein cyclin A induces entry into M phase and the resumption of meiosis in Xenopus oocytes. Cell. 1986 Dec 26;47(6):861–870. doi: 10.1016/0092-8674(86)90801-9. [DOI] [PubMed] [Google Scholar]
- Wasserman W. J., Masui Y. Effects of cyclohexamide on a cytoplasmic factor initiating meiotic naturation in Xenopus oocytes. Exp Cell Res. 1975 Mar 15;91(2):381–388. doi: 10.1016/0014-4827(75)90118-4. [DOI] [PubMed] [Google Scholar]
- Westendorf J. M., Swenson K. I., Ruderman J. V. The role of cyclin B in meiosis I. J Cell Biol. 1989 Apr;108(4):1431–1444. doi: 10.1083/jcb.108.4.1431. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wu M., Gerhart J. C. Partial purification and characterization of the maturation-promoting factor from eggs of Xenopus laevis. Dev Biol. 1980 Oct;79(2):465–477. doi: 10.1016/0012-1606(80)90131-1. [DOI] [PubMed] [Google Scholar]