The Journal of Cell Biology, Vol 108, 1431-1444, Copyright © 1989 by The Rockefeller University Press

ARTICLES

The role of cyclin B in meiosis I

JM Westendorf, KI Swenson and JV Ruderman
Program in Cell and Developmental Biology, Harvard Medical School, Boston, Massachusetts 02115.

In clams, fertilization is followed by the prominent synthesis of two cyclins, A and B. During the mitotic cell cycles, the two cyclins are accumulated and then destroyed near the end of each metaphase. Newly synthesized cyclin B is complexed with a small set of other proteins, including a kinase that phosphorylates cyclin B in vitro. While both cyclins can act as general inducers of entry into M phase, the two are clearly distinguished by their amino acid sequences (70% nonidentity) and by their different modes of expression in oocytes and during meiosis. In contrast to cyclin A, which is stored solely as maternal mRNA, oocytes contain a stockpile of cyclin B protein, which is stored in large, rapidly sedimenting aggregates. Fertilization results in the release of cyclin B to a more disperse, soluble form. Since the first meiotic division in clams can proceed even when new protein synthesis is blocked, these results strongly suggest it is the fertilization- triggered unmasking of cyclin B protein that drives cells into meiosis I. We propose that the unmasking of maternal cyclin B protein allows it to interact with cdc2 protein kinase, which is also stored in oocytes, and that the formation of this cyclin B/cdc2 complex generates active M phase-promoting factor.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Facebook    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

• Diederichs, S., Baumer, N., Ji, P., Metzelder, S. K., Idos, G. E., Cauvet, T., Wang, W., Moller, M., Pierschalski, S., Gromoll, J., Schrader, M. G., Koeffler, H. P., Berdel, W. E., Serve, H., Muller-Tidow, C. (2004). Identification of Interaction Partners and Substrates of the Cyclin A1-CDK2 Complex. J. Biol. Chem. 279: 33727-33741 [Abstract] [Full Text]  
• Marangos, P., Carroll, J. (2004). The dynamics of cyclin B1 distribution during meiosis I in mouse oocytes. Reproduction 128: 153-162 [Abstract] [Full Text]  
• Kuroda, T., Naito, K., Sugiura, K., Yamashita, M., Takakura, I., Tojo, H. (2004). Analysis of the Roles of Cyclin B1 and Cyclin B2 in Porcine Oocyte Maturation by Inhibiting Synthesis with Antisense RNA Injection. Biol. Reprod. 70: 154-159 [Abstract] [Full Text]  
• Terasaki, M., Okumura, E.-i., Hinkle, B., Kishimoto, T. (2003). Localization and Dynamics of Cdc2-Cyclin B during Meiotic Reinitiation in Starfish Oocytes. Mol. Biol. Cell 14: 4685-4694 [Abstract] [Full Text]  
• Nguyen, T. B., Manova, K., Capodieci, P., Lindon, C., Bottega, S., Wang, X.-Y., Refik-Rogers, J., Pines, J., Wolgemuth, D. J., Koff, A. (2002). Characterization and Expression of Mammalian Cyclin B3, a Prepachytene Meiotic Cyclin. J. Biol. Chem. 277: 41960-41969 [Abstract] [Full Text]  
• Kanatsu-Shinohara, M., Schultz, R. M., Kopf, G. S. (2000). Acquisition of Meiotic Competence in Mouse Oocytes: Absolute Amounts of p34cdc2, Cyclin B1, cdc25C, and wee1 in Meiotically Incompetent and Competent Oocytes. Biol. Reprod. 63: 1610-1616 [Abstract] [Full Text]  
• Dai, Y., Lee, C., Hutchings, A., Sun, Y., Moor, R. (2000). Selective Requirement for Cdc25C Protein Synthesis During Meiotic Progression in Porcine Oocytes. Biol. Reprod. 62: 519-532 [Abstract] [Full Text]  
• Bastians, H., Topper, L. M., Gorbsky, G. L., Ruderman, J. V. (1999). Cell Cycle-regulated Proteolysis of Mitotic Target Proteins. Mol. Biol. Cell 10: 3927-3941 [Abstract] [Full Text]  
• Mendenhall, M. D., Hodge, A. E. (1998). Regulation of Cdc28 Cyclin-Dependent Protein Kinase Activity during the Cell Cycle of the Yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62: 1191-1243 [Abstract] [Full Text]  
• Abrieu, A, Brassac, T, Galas, S, Fisher, D, Labbe, J., Doree, M (1998). The Polo-like kinase Plx1 is a component of the MPF amplification loop at the G2/M-phase transition of the cell cycle in Xenopus eggs. J. Cell Sci. 111: 1751-1757 [Abstract]  
• Desrivieres, S., Desrivières, S., Ferrari, S. (1997). Evidence for Different Mechanisms of Growth Inhibition of T-cell Lymphoma by Phorbol Esters and Concanavalin A. J. Biol. Chem. 272: 2470-2476 [Abstract] [Full Text]  
• Zhang, Y., Wang, Z., Ravid, K. (1996). The Cell Cycle in Polyploid Megakaryocytes Is Associated with Reduced Activity of Cyclin B1-dependent Cdc2 Kinase. J. Biol. Chem. 271: 4266-4272 [Abstract] [Full Text]  
• Kreutzer, M., Richards, J., De Silva-Udawatta, M., Temenak, J., Knoblich, J., Lehner, C., Bennett, K. (1995). Caenorhabditis elegans cyclin A- and B-type genes: a cyclin A multigene family, an ancestral cyclin B3 and differential germline expression. J. Cell Sci. 108: 2415-2424 [Abstract]  
• Ohsumi, K, Sawada, W, Kishimoto, T (1994). Meiosis-specific cell cycle regulation in maturing Xenopus oocytes. J. Cell Sci. 107: 3005-3013 [Abstract]  
• Gavin, A., Cavadore, J., Schorderet-Slatkine, S (1994). Histone H1 kinase activity, germinal vesicle breakdown and M phase entry in mouse oocytes. J. Cell Sci. 107: 275-283 [Abstract]  
• Koff, A, Ohtsuki, M, Polyak, K, Roberts, J., Massague, J (1993). Negative regulation of G1 in mammalian cells: inhibition of cyclin E-dependent kinase by TGF-beta. Science 260: 536-539 [Abstract]  
• Chapman, D., Wolgemuth, D. (1993). Isolation of the murine cyclin B2 cDNA and characterization of the lineage and temporal specificity of expression of the B1 and B2 cyclins during oogenesis, spermatogenesis and early embryogenesis. Development 118: 229-240 [Abstract]  
• Epstein, C B, Cross, F R (1992). CLB5: a novel B cyclin from budding yeast with a role in S phase.. Genes Dev. 6: 1695-1706 [Abstract]  
• Dalby, B, Glover, D. (1992). 3' non-translated sequences in Drosophila cyclin B transcripts direct posterior pole accumulation late in oogenesis and peri-nuclear association in syncytial embryos. Development 115: 989-997 [Abstract]  
• Paris, J, Swenson, K, Piwnica-Worms, H, Richter, J D (1991). Maturation-specific polyadenylation: in vitro activation by p34cdc2 and phosphorylation of a 58-kD CPE-binding protein.. Genes Dev. 5: 1697-1708 [Abstract]  
• O'Farrell, P., Leopold, P. (1991). A Consensus of Cyclin Sequences Reveals Homology with the ras Oncogene. Cold Spring Harb Symp Quant Biol 56: 83-92 [Abstract]  
• Fotedar, R., Roberts, J.M. (1991). Association of p34cdc with Replicating DNA. Cold Spring Harb Symp Quant Biol 56: 325-333 [Abstract]  
• Pines, J., Hunter, T. (1991). Human Cell Division: The Involvement of Cyclins A and B1, and Multiple cdc2s. Cold Spring Harb Symp Quant Biol 56: 449-463 [Abstract]  
• Lehner, C.F., Yakubovich, N., O'Farrell, P.H. (1991). Exploring the Role of Drosophila Cyclin A in the Regulation of S Phase. Cold Spring Harb Symp Quant Biol 56: 465-475 [Abstract]  
• Ruderman, J., Luca, F., Shibuya, E., Gavin, K., Boulton, T., Cobb, M. (1991). Control of the Cell Cycle in Early Embryos. Cold Spring Harb Symp Quant Biol 56: 495-502 [Abstract]  
• Devault, A., Cavadore, J.-C., Fesquet, D., Labbe, J.-C., Lorca, T., Picard, A., Strausfeld, U., Doree, M. (1991). Concerted Roles of Cyclin A, cdc25+ Mitotic Inducer, and Type 2A Phosphatase in Activating the Cyclin B/cdc2 Protein Kinase at the G2/M Phase Transition. Cold Spring Harb Symp Quant Biol 56: 503-513 [Abstract]  
• Piwnica-Worms, H., Atherton-Fessler, S., Lee, M.S., Ogg, S., Swenson, K.I., Parker, L.L. (1991). p107wee1 Is a Serine/Threonine and Tyrosine Kinase That Promotes the Tyrosine Phosphorylation of the Cyclin/p34cdc2 Complex. Cold Spring Harb Symp Quant Biol 56: 567-576 [Abstract]  
• Glover, D.M., Llamazares, S., Girdham, C., Maldonado-Codina, G., Moreira, A., Tavares, A., Sunkel, C.E., Gonzalez, C. (1991). Cyclical Changes in the Subcellular Distribution of Proteins Essential for Mitosis during Embryogenesis in Drosophila. Cold Spring Harb Symp Quant Biol 56: 709-717 [Abstract]  
• Standart, N, Dale, M, Stewart, E, Hunt, T (1990). Maternal mRNA from clam oocytes can be specifically unmasked in vitro by antisense RNA complementary to the 3'-untranslated region.. Genes Dev. 4: 2157-2168 [Abstract]  
• Richardson, H E, Stueland, C S, Thomas, J, Russell, P, Reed, S I (1990). Human cDNAs encoding homologs of the small p34Cdc28/Cdc2-associated protein of Saccharomyces cerevisiae and Schizosaccharomyces pombe.. Genes Dev. 4: 1332-1344 [Abstract]  
• Pondaven, P, Meijer, L, Beach, D (1990). Activation of M-phase-specific histone H1 kinase by modification of the phosphorylation of its p34cdc2 and cyclin components.. Genes Dev. 4: 9-17 [Abstract]  
• Murray, A., Kirschner, M. (1989). Dominoes and clocks: the union of two views of the cell cycle. Science 246: 614-621 [Abstract]  
• O'Farrell, P., Edgar, B., Lakich, D, Lehner, C. (1989). Directing cell division during development. Science 246: 635-640 [Abstract]  

Home | Help | Feedback | Subscriptions | Archive | Search | Table of Contents