Abstract
Biological scientists are eagerly confronting the challenge of understanding the regulatory mechanisms that control the cell division cycle in eukaryotes. New information will have major implications for the treatment of growth-related diseases and cancer in animals. In plants, cell division has a key role in root and shoot growth as well as in the development of vegetative storage organs and reproductive tissues such as flowers and seeds. Many of the strategies for crop improvement, especially those aimed at increasing yield, involve the manipulation of cell division. This review describes, in some detail, the current status of our understanding of the regulation of cell division in eukaryotes and especially in plants. It also features an outline of some preliminary attempts to exploit transgenesis for manipulation of plant cell division.
Similar content being viewed by others
References
Howard, A. and Pelc, S. R. (1953) Synthesis of deoxyribonucleic acid in normal and irradiated cells and its relation to chromosome breakage.Heredity 6(Suppl.), 261–273.
Muller, R., Mumberg, D., and Lucibello, F. C. (1993) Signals and genes in the control of cell-cycle progression.Biochim. Biophys. Acta 1155, 151–179.
Pardee, A. B. (1989) G1 events and regulation of cell proliferation.Science 246, 603–608.
Wick, M., Burger, C., Brusselbach, S., Lucibello, F. C., and Muller, R. (1994) Identification of serum-inducible genes: different patterns of gene regulation during G0-S and G1-S progression.J. Cell Sci. 107, 227–239.
Burger, C., Wick, M., Brusselbach, S., and Muller, R. (1994) Differential induction of “metabolic genes” after mitogen stimulation and during normal cell cycle progression.J. Cell Sci. 107, 241–252.
Drewinko, B., Yang, L. Y., Barlogie, B., and Trujillo, J. M. (1984) Cultured human tumour cells may be arrested in all stages of the cycle during stationary phase: demonstration of quiescent cells in G1, S and G2 phase.Cell Tissue Kinet. 17, 453–463.
Ferreira, P., Hemerly, A., Van Montagu, M., and Inze, D. (1994) Control of cell proliferation during plant development.Plant Mol. Biol. 26, 1289–1303.
Hutchison, C. and Glover, D. M. (1995)Cell Cycle Control, OUP, Oxford, UK.
Van't Hof, J. (1973) The regulation of cell division in higher plants.Brookhaven Sympo 25, 125–165.
Hanks, S. K., Quinn, A. M., and Hunter, T. (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domain.Science 241, 42–52.
Nurse, P., and Bissett, Y. (1981) Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast.Nature 292, 558–560.
Lorincz, A. T. and Reed, S. I. (1984) Primary structure homology between the product of a yeast cell division control geneCDC28 and vertebrate oncogenes.Nature 307, 183–185.
Reed, S. I. (1995) START and the G1-S phase transition in budding yeast, inCell Cycle Control (Hutchison, C. and Glover, D. M., eds.) OUP, Oxford, UK, pp. 40–62.
Lee, M. G., and Nurse, P. (1987) Complementation used to clone a human homologue of the fission yeast cell cycle control genecdc2.Nature 327, 31–35.
Ellidge, S. J. and Spottswood, M. R. (1991) A new human p34 protein kinase, CDK2, identified by complementation of acdc28 mutation inSaccharomyces cerevisiae, is a homolog ofXenopus Eg1.EMBO J. 10, 2653–2659.
Tsai, L.-H., Harlow, E., and Meyerson, M. (1991) Isolation of the humancdk2 gene that encodes the cyclin A- and adenovirus E1A-associated p33 kinase.Nature 353, 174–177.
Fang, F. and Newport, J. W. (1991) Evidence that the G1-S and G2-M transition are controlled by different cdc2 proteins in higher eukaryotes.Cell 66, 731–742.
Rosenblatt, J., Gu, Y., and Morgan, D. O. (1992) Human cyclin-dependent kinase 2 is activated during the S and G2 phases of the cell cycle and associates with cyclin A.Proc. Natl. Acad. Sci. USA 89, 2824–2828.
Elledge, S. J., Richman, R., Hall, F. L., Williams, R. T., Lodgson, N., and Wade-Harper, J. (1992)CDK2 encodes a 33-kDa cyclin A-associated protein kinase and is expressed beforeCDC2 in the cell cycle.Proc. Natl. Acad. Sci. USA 89, 2907–2911.
Tsai, L.-H., Lees, E., Faha, B., Harlow, E., and Riabowol, K. (1993) The cdk2 kinase is required for the G1-to-S transition in mammalian cells.Oncogene 8, 1593–1602.
Pagano, M., Pepperkok, R., Lukas, J., Baldin, V., Ansorge, W., Bartek, J., and Draetta, G. (1993) Regulation of the cell cycle by the cdk2 protein kinase in cultured human fibroblasts.J. Cell Biol. 121, 101–111.
Meyerson, M., Enders, G. H., Wu, C.-L., Su, L.-K., Gorka, C., Nelson, C., Harlow, E., and Tsai, L.-H. (1992) A family of human cdc2-related protein kinases.EMBO J. 11, 2909–2917.
Hofmann, F. and Livingston, D. M. (1996) Differential effects of cdk2 and cdk3 on the control of pRb and E2F function during G1 exit.Genes Dev. 10, 851–861.
Matsushime, H., Ewen, M. E., Strom, D. K., Kato, J.-Y., Hanks, S. K., Roussel, M. F., and Sherr, C. J. (1992) Identification and properties of an atypical catalytic subunit (p34PSK-J3/cdk4) for mammalian D type G1 cyclins.Cell 71,,323–334.
Xiong, Y., Zhang, H., and Beach, D. (1992) D type cyclins associate with multiple protein kinases and the DNA replication and repair factor PCNA.Cell 71, 505–514.
Hellmich, M. R., Pant, H. C., Wada, E., and Battey, J. F. (1992) Neuronal cdc2-like kinase: a cdc2-related protein kinase with predominantly neuronal expression.Proc. Natl. Acad. Sci. USA 89, 10,867–10,871.
Meyerson, M. and Harlow, E. (1994) Identification of G1 kinase activity for cdk6, a novel cyclin D partner.Mol. Cell. Biol. 14, 2077–2086.
Bates, S., Bonetta, L., MacAllan, D., Parry, D., Holder, A., Dickson, C., and Peters, G. (1994) CDK6 (PLSTIRE) and CDK4 (PSK-J3) are a distinct subset of the cyclin-dependent kinases that associate with cyclin D1.Oncogene 9, 71–79.
Shuttleworth, J., Godfrey, R., and Coleman, A. (1990) p40MO15, a cdc2-related protein kinase involved in negative regulation of meiotic maturation of Xenopus oocytes.EMBO J. 9, 3233–3240.
Solomon, M. J., Harper, J. W., and Shuttleworth, J. (1993) CAK, the p34cdc2 activating kinase, contains a protein identical or closely related to p40MO15.EMBO J. 12, 3133–3142.
Poon, R. Y. C., Yamashita, K., Adamczewski, J. P., Hunt, T., and Shuttleworth, J. (1993) The cdc2-related protein p40MO15 is the catalytic subunit of a protein kinase that can activate p33cdk2 and p34cdc2.EMBO J. 12, 3123–3132.
Fesquet, D., Labbe, J.-C., Derancourt, J., Capony, J.-P., Galas, S., Girard, F., Lorca, T., Shuttleworth, J., Doree, M., and Cavadore, J.-C. (1993) TheMO15 gene encodes the catalytic subunit of a protein kinase that activates cdc2 and other cyclin-dependent kinases (CDKs) through phosphorylation of Thr161 and its homologues.EMBO J. 12, 3111–3121.
Wu, L., Yee, A., Liu, L., Carbonaro-Hall, D., Venkatesan, N., Tolo, V. T., and Hall, F. L. (1994) Molecular cloning of the human CAK1 gene encoding a cyclin-dependent kinase-activating kinase.Oncogene 9, 2089–2096.
Tassan, J.-P., Jaquenoud, M., Leopold, P., Schultz, S. J., and Nigg, E. A. (1995) Identification of human CDK8, a protein kinase partner for cyclin C and potential homolog of yeast SRB10.Proc. Natl. Acad. Sci. USA 92, 8871–8875.
Leclerc, V., Tassan, J.-P., O'Farrell, P. H., Nigg, E. A., and Leopold, P. (1996) Drosophila cdk8, a kinase partner of cyclin C that interacts with the large subunit of RNA polymerase II.Mol. Biol. Cell 7, 505–513.
Rickert, P., Seghezzi, W., Shanahan, F., Cho, H., and Less, E. (1996) Cyclin C/CDK8 is a novel CTD kinase associated with RNA polymerase II.Oncogene 12, 2631–2640.
Guadagno, T. M. and Newport, J. W. (1996) Cdk2 kinase is required for entry into mitosis as a positive regulator of Cdc2-cyclin B kinase activity.Cell 84, 73–82.
Marcote, M. J., Knoghton, D. R., Basi, G., Sowadski, J. M., Brambilla, P., Draetta, G., and Taylor, S. S. (1993) A three-dimensional model of the cdc2 protein kinase: localisation of cyclin- and suc1-binding regions and phosphorylation sites.Mol. Cell. Biol. 13, 5122–5131.
DeBondt, H. L., Rosenblatt, J., Jancarik, J., Jones, H. D., Morgan, D. O., and Kim, S-H. (1993) Crystal structure of cyclin-dependent kinases 2.Nature 363, 595–602.
Pines, J. (1996) Cyclin from sea urchins to HeLas: making the human cell cycle.Biochem. Soc. Trans. 24, 15–33.
Morla, A. O., Draetta, G., Beach, D., and Wang, J. Y. J. (1989) Reversible tyrosine phosphorylation of cdc2: dephosphorylation accompanies activation during entry into mitosis.Cell 58, 193–203.
Krek, W. and Nigg, E. A. (1991) Differential phosphorylation of vertebrate p34cdc2 kinase at the G1/S and G2/M transitions of the cell cycle: identification of major phosphorylation sites.EMBO J. 10, 305–316.
Krek, W., and Nigg, E. A. (1991) Mutations of p34cdc2 phosphorylation sites induce premature mitotic events in HeLa cells: evidence for a double block to p34cdc2 kinase activation in vertebrates.EMBO J. 10, 3331–3341.
Norbury, C., Blow, J. J., and Nurse, P. (1991) Regulatory phosphorylation of the p34cdc2 protein kinase in vertebrates.EMBO J. 10, 3321–3329.
Atherton-Fessler, S., Parker, L. L., Geahlen, R. L., and Piwnica-Worms, H. (1993) Mechanisms of p34cdc2 regulation.Mol. Cell. Biol. 13, 1675–1685.
MacNeill, S. A. and Fantes, P. A. (1995) Controlling entry into mitosis in fission yeast, inCell Cycle Control (Hutchison, C. and Glover, D. M., eds.), OUP, Oxford, UK, pp. 63–105.
Koff, A., Cross, F., Fisher, A., Schumacher, J., Legullec, K., Philippe, M., and Roberts, J. M. (1991) Human cyclin E, a new cyclin that interacts with two members of theCDC2 gene family.Cell 66, 1217–1228.
Koff, A., Giordano, A., Desai, D., Yamashita, K., Harper, J. W., Elledge, S., Nishimoto, T., Morgan, D. O., Franza, B. R., and Roberts, J. M. (1992) Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle.Science 257, 1689–1693.
Tamura, K., Kanaoka, Y., Jinno, S., Nagata, A., Ogiso, Y., Shimizu, K., Hayakawa, T., Nojima, H., and Okayama, H. (1993) Cyclin-G—a new mammalian cyclin with homology to fission yeast Cig1.Oncogene 8, 2113–2118.
Bates, S., Rowan, S., and Vousden, K. H. (1996) Characterisation of human cyclin G1 and G2: DNA damage inducible genes.Oncogene 13, 1103–1109.
Horne, M. C., Goolsby, G. L., Donaldson, K. L., Tran, D., Neubauer, M., and Wahl, A. F. (1996) Cyclin G1 and cyclin G2 comprise a new family of cyclins with contrasting tissue-specific and cell cycle-regulated expression.J. Biol. Chem. 271, 6050–6061.
Fisher, R. P. and Morgan, D. O. (1994) A novel cyclin associates with MO15/cdk7 to form the CDK-activating kinase.Cell 78, 713–724.
Makela, T. P., Tassan, J. P., Nigg, E. A., Frutiger, S., Hughes, G. J., and Weinberg, R. A. (1994) A cyclin associated with the CDK-activating kinase MO15.Nature 371, 254–257.
Tassan, J. P., Schultz, S. J., Bartek, J., and Nigg, E. A. (1994) Cell cycle analysis of the activity, subcellular localisation and subunit composition of human CAK (CDK-activating kinase).J. Cell Biol. 127, 467–478.
Lew, J. and Wang, J. H. (1995) Neuronal cdc2-like kinase.TIBS 20, 33–37.
Higashi, H., Suzuki-Takahashi, I., Saitoh, S., Segawa, K., Taya, Y., Okuyama, A., Nishimura, S., and Kitagawa, M. (1996) Cyclin-dependent kinase-2 (Cdk2) forms an inactive complex with cyclin D1 since Cdk2 associated with cyclin D1 is not phosphorylated by Cdk7-cyclin H.Eur. J. Biochem. 237, 460–467.
Kobayashi, H., Stewart, E., Poon, R., Adamczewski, J. P., Gannon, J., and Hunt, T. (1992) Identification of the domains in cyclin-A required for binding to, and activation of p34 (cdc2) and p32 (cdk2) protein-kinase subunits.Mol. Biol. Cell 3, 1279–1294.
Lees, E. and Harlow, E. (1993) Sequences within the conserved cyclin box of human cyclin A are sufficient for binding to and activation of cdc2 kinase.Mol. Cell. Biol. 13, 1194–1201.
Peeper, D. S., Parker, L.L., Ewen, M. E., Toebes, M., Hall, F. L., Xu, M., Zantema, A., van der Eb, A. J., and Piwnica-Worms, H. (1993) A- and B-type cyclin differnetially modulate substrate specificity of cyclin-cdk complexes.EMBO J. 12, 1947–1954.
Pines, J. and Hunter, T. (1989) Isolation of a human cyclin cDNA—evidence for cyclin messenger-RNA and protein-regulation in the cell-cycle and for interaction with p34cdc2.Cell 58, 833–846.
Pines, J. and Hunter, T. (1990) Human cyclin-A is adenovirus E1A-associated protein p60 and behaves differnetly from cyclin-B.Nature 346, 760–763.
Hunt, T. (1991) Destruction's our delight.Nature 349, 100,101.
Glotzer, M., Murray, A. W., and Kirscner, M. W. (1991) Cyclin is degraded by the ubiquitin pathway.Nature 349, 132–138.
Hershko, A., Ganoth, D., Pehrson, J., Palazzo, R. E., and Cohen, L. H. (1991) Methylated ubiquitin inhibits cyclin degradation in clam embryo extracts.J. Biol. Chem. 266, 16,376–16,379.
Luca, F. C. and Ruderman, J. V. (1989) Control of programmed cyclin destruction in a cell-free system.J. Cell Biol. 109, 1895–1909.
Minshull, J., Golsteyn, R., Hill, C. S., and Hunt, T. (1990) The A- and B-type cyclin associated kinases inXenopus turn on and off at different times in the cell cycle.EMBO J. 8, 2865–2875.
Whitfield, W. G. F., Gonzalez, C., Maldon-do-Codina, G., and Glover, D. M. (1990) The A- and B-type cyclins ofDrosophila are accumulated and destroyed in temporally distinct events that define separable phases of the G2-M transition.EMBO J. 9, 2563–2572.
Hunt, T., Luca, F. C., and Ruderman, J. V. (1992) The requirements for protein synthesis and degradation, and the control of destruction of cyclins A and B in the meiotic and mitotic cell cycles of the clam embryo.J. Cell Biol. 116, 707–724.
Rogers, S., Wells, R., and Rechsteiner, M. (1986) Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis.Science 234, 364–368.
Jeffrey, P. D., Russo, A. A., Polyak, K., Gibbs, E., Hurwitz, J., Massague, J., and Pavletich, N. P. (1995) Mechanism of CDK activation revealed by the structure of a cyclin A-CDK2 complex.Nature 376, 313–320.
Nigg, E. A. (1996) Cyclin-dependent kinase 7: at the crossroads of transcription, DNA repair and cell cycle control?Curr. Opin. Cell Biol. 8, 312–317.
Basi, G., and Draetta, G. (1995) The cdc2 kinase: structure, activation, and its role at mitosis in vertebrate cells, inCell Cycle Control (Hutchison, C., and Glover, D. M., eds) OUP, Oxford, UK, pp. 106–143.
Russo, A. A., Jeffrey, P. D., and Paveltich, N. P. (1996) Structural basis of cyclin-dependent kinase activation by phosphorylation.Nature Structural Biol. 3, 696–700.
Solomon, M. (1994) The function(s) of CAK, the p34cdc2-activating kinase.TIBS 19, 496–500.
Tassan, J. P., Jaquenoud, M., Fry, A. M., Frutiger, S., Hughes, G. J., and Nigg, E. A. (1995) In vitro assembly of a functional human CDK7-cyclin H complex requires MAT1, a novel 36kDa RING finger protein.EMBO J. 14, 5608–5617.
Yee, A., Nichols, M. A., Wu, L., Hall, F. L., Kobayashi, R., and Xiong, Y. (1995) Molecular cloning of CDK7-associated human MAT1, a cyclin-dependent kinase-activating kinase (CAK) assembly factor.Cancer Res. 55, 6058–6062.
Shuttleworth, J. (1995) The regulation and functions of cdk7.Prog. Cell Cycle Res. 1, 229–240.
Hata, S. (1991) cDNA cloning of a novel cdc2+/ CDC28-related protein kinase from rice.FEBS Lett. 279, 149–152.
Sauter, M. (1997) Differential expression of a CAK (cdc2-activating kinase)-like protein kinase, cyclins andcdc2 genes from rice during the cell cycle and in response to gibberellin.Plant J. 11, 181–190.
Devault, A., Martinez, A. M., Fesquet, D., Labbe, J. C., Tassan, J. P., Nigg, E. A., Cavadore, J. C., and Doree, M. (1995) MAT1, a new RING-finger protein subunit stabilizing cyclin H-cdk7 complexes in starfish andXenopus CAK.EMBO J. 14, 5027–5036.
Fisher, R. P., Jin, P., Chamberlin, H. M., and Morgan, D. O. (1995) Alternative mechanisms of CAK assembly require an assembly factor or an activating kinase.Cell 83, 47–57.
Matsuoka, M., Kato, J. Y., Fisher, R. P., Morgan, D. O., and Sherr, C. J. (1994) Activation of cyclin-dependent kinase 4 (cdk4) by mouse MO15-associated kinase.Mol. Cell. Biol. 14, 7265–7275.
Kato, J.-Y., Matsuoka, M., Strom, D. K., and Sherr, C. J. (1994) Regulation of cyclin D-dependent kinase 4 (cdk4) by cdk4-activating kinase.Mol. Cell. Biol. 14, 2713–2721.
Roy, R., Adamczewski, J. P., Seroz, T., Vermeulen, W., Tassan, J. P., Schaeffer, L., Nigg, E. A., Hoejimakers, J. H. J., and Egly, J. M. (1994) The MO15 cell cycle kinase is associated with the TFHH transcription-DNA repair factor.Cell 79, 1093–1101.
Serizawa, H., Makela, T. P., Conaway, J. W., Conaway, R. C., Weinberg, R. A., and Young, R. A. (1995) Association of cdk-activating kinase subunits with transcription factor TFIIH.Nature 374, 280–282.
Shiekhatter, R., Mermelstein, F., Fisher, R., Drapkin, R., Dynlacht, B., Wessling, H. C., Morgan, D. O., and Reinberg, D. (1995) Cdk-activating kinase complex is a component of human transcription factor TFIIH.Nature 374, 283–287.
Adamczewski, J. P., Rossignoi, M., Tassan, J. P., Nigg, E. A., Moncollin, V., and Egly, J. M. (1996) MATI, cdk7 and cyclin H form a kinase complex which is UV light sensitive upon association with IFIIH.EMBO J. 15, 1877–1884.
Simon, M., Seraphin, B., and Faye, G. (1986) KIN28, a yeast split gene coding for a putative protein kinase homologous to CDC28.EMBO J.,5, 2697–2701.
Valay, J. G., Simon, M., Dubois, M. F., Bensaude, O., Facca, C., and Faye, G. (1995) The KIN28 gene is required both for RNA polymerase II mediated transcription and phosphorylation of the CTD.J. Mol. Biol. 249, 535–544.
Feaver, W. J., Svejstrup, J. Q., Henry, N. L., and Kornberg, R. D. (1994) Relationship of CDK-activating kinase and RNA polymerase II CTD kinase TFIIH/TFIIK.Cell 79, 1103–1109.
Cismowski, M. J., Laff, G. M., Solomon, M. J., and Reed, S. I. (1995) KIN28 encodes a C-terminal domain kinase that controls mRNA transcription inSaccharomyces cerevisiae but lacks cyclin-dependent kinase-activating kinase (CAK) activity.Mol. Cell. Biol. 15, 2983–2992.
Buck, V., Russell, R., and Millar, J. B. A. (1995) Identification of a cdk-activating kinase in fission yeast.EMBO J. 14, 6173–6183.
Damagnez, V., Makela, T. P., and Cottarel, G. (1995)Schizosaccharomyces pombe Mopl-Mcs2 is related to mammalian CAK.EMBO J. 14, 6164–6172.
Liao, S.-M., Zhang, J., Jeffery, D. A., Koleske, A. J., Thompson, C. M., Chao, D. M., Viljeon, M., van Vuuren, H. J. J., and Young, R. A. (1995) A kinase cyclin pair in the RNA polymerase II holoenzyme.Nature 374, 193–196.
Espinoza, F. H., Farrell, A., Erdjument-Bromage, H., Tempest, P., and Morgan, D. O. (1996) A cyclindependent kinase-activating kinase (CAK) in budding yeast unrelated to vertebrate CAK.Science 273, 1714–1717.
Solomon, M. J., Lee, T., and Kirschner, M. W. (1992) The role of phosphorylation in p34cdc2 activation: identification of an activating kinase.Mol. Biol. Cell 3, 13–27.
Honda, R., Ohba, Y., and Yasuda, H. (1992) The cell cycle regulator, human p50weel, is a tyrosine kinase and not a serine/tyrosine kinase.Biochem. Biophys. Res. Commun. 186, 1333–1338.
Igarashi, M., Nagata, A., Jinno, S., Suto, K., and Okayama, H. (1991) Weel+-like gene in human cells.Nature 353, 80–83.
McGowan, C. H. and Russell, P. (1993) Human Weel kinase inhibits cell division by phosphorylating p34cdc2 exclusively on Tyr15.EMBO J. 12, 75–85.
McGowan, C. H. and Russell, P. (1995) Cell cycle regulation of human WEE1.EMBO J. 14, 2166–2175.
Parker, L. L. and Piwnica-Worms, H. (1992) Inactivation of the p34cdc2/cyclin B complex by the human WEE1 tyrosine kinase.Science 257, 1955–1957.
Parker, L. L., Sylvestre, P. J., Byrnes, M. J., Liu, F., and Piwnica-Worms, H. (1995) Identification of a 95-kDA WEE1-like tyrosine kinase in HeLa cells.Proc. Natl. Acad. Sci. USA92, 9638–9642.
Liu, F., Stanton, J. J., Wu, Z., and Piwnica-Worms, H. (1997) The human Mytl kinase preferentially phosphorylates Cdc2 on threonine 14 and localises to the endoplasmic reticulum and golgi complex.Mol. Cell. Biol. 17, 571–583.
Mueller, P. R., Coleman, T. R., Kumagai, A., and Dunphy, W. G. (1995) Mytl: a membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15.Science 270, 86–90.
Parker, L. L., Atherton-Fessler, S., and Pownica-Worms, H. (1992) p107weel is a dual-specificity kinase that phosphorylates p34cdc2 on tyrosine 15.Proc. Natl. Acad. Sci. USA 89, 2917–2921.
Atherton-Fessler, S., Hannig, G., and Piwnica-Worms, H. (1993) Reversible tyrosine phosphorylation and cell cycle control.Semin. Cell Biol. 4, 433–442.
Kornbluth, S., Sebastian, B., Hunter, T., and Newport, J., (1994) Membrane localization of the kinase which phosphorylates p34cdc2 on threonine 14.Mol. Biol. Cell 5, 273–282.
Baldin, V. and Ducommun, B. (1995) Subcellular localisation of human weel kinase is regulated during the cell cycle.J. Cell Sci. 108, 2425–2432.
Heald, R., McLoughlin, M., and McKeon, F. (1993) Human Weel maintains mitotic timing by protecting the nucleus from cytoplasmically activated Cdc2 kinase.Cell 74, 463–474.
Pines, J. and Hunter, T. (1994) The differential localisation of human cyclins A and B is due to a cytoplasmic retention signal in cyclin B.EMBO J. 13, 3772–3781.
Russell, P. and Nurse, P. (1987) The mitotic inducernim1 + functions in a regulatory network of protein kinase homologs controlling the initiation of mitosis.Cell 49, 569–576.
Young, P. G. and Fantes, P. (1987)Schizosaccharomyces pombe mutants affected in their division response to starvation.J. Cell Sci. 88, 295–304.
Belenguer, P., Pelloquin, L., Baldin, V., Oustrin, M.-L., and Ducommun, B. (1995) The fission yeast Nim1/Cdr1 kinase: a link between nutritional state and cell cycle control.Prog. Cell Cycle Res. 1, 207–214.
Russell, P. and Nurse, P. (1986) cdc25+ functions as an inducer in the mitotic control of fission yeast.Cell 45, 145–153.
Dunphy, W. G., and Kumagai, A. (1991) The cdc25 protein contains an intrinsic phosphatase activity.Cell 67, 189–196.
Millar, J. B. A., McGowan, C. H., Lenaers, G., Jones, R., and Russell, P. (1991) p80cdc25 mitotic inducer is the tyrosine phosphatase that activates cdc2 kinase in fission yeast.EMBO J. 10, 4301–4309.
Kumagai, A. and Dunphy, W. G. (1991) The cdc25 protein controls tyrosine dephosphorylation of the cdc2 protein in a cell-free system.Cell 64, 903–914.
Gautier, J., Solomon, M. J., Booher, R. N., Bazan, J. F., and Kirschner, M. W. (1991) cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2.Cell 67, 197–211.
Belle, R., Ollivier, E., and Guerrucci, M.-A. (1992) Higher eukaryotic cdc25 proteins are structurally related to phosphoseryl/threonyl protein phosphatases.Biol. Cell 75, 139–143.
Millar, J. B. A. and Russell, P. (1992) The cdc25 M-phase inducer: an unconventional protein phosphatase.Cell 68, 407–410.
Honda, R., Ohba, Y., Nagata, A., Okayama, H., and Yasuda, H. (1993) Dephosphorylation of human p34 (cdc2) kinase on both Thr-14 and Tyr-15 by human cdc25B phosphatase.FEBS Lett. 318, 331–334.
Jessus, C. and Ozon, R. (1995) Function and regulation of cdc25 protein phosphatase through mitosis and meiosis.Prog. Cell Cycle Res. 1, 215–228.
Galactionov, K. and Beach, D. (1991) Specific activation of cdc25 tyrosine phosphatase by B-type cyclins: evidence for multiple roles of mitotic cyclins.Cell 67, 1181–1194.
Nagata, A., Igarashi, M., Jinno, S., Suto, K., and Okayama, H. (1991) An additional homolog of the fission yeastcdc25 gene occurs in humans and is highly expressed in some cancer cells.New Biol. 3, 959–968.
Sadhu, K., Reed, S. I., Richardson, H., and Russell, P. (1990) Human homolog of fission yeastcdc25 is predominantly expressed in G1.Proc. Natl. Acad. Sci. USA 87, 5139–5143.
Sebastian, B., Kakizuka, A., and Hunter, T. (1993). Cdc25M2 activation of cyclin-dependent kinases by dephosphorylation of threonine-14 and tyrosine-15.Proc. Natl. Acad. Sci. USA 90, 3521–3524.
Hoffmann, I., Clarke, P., Draetta, G. and Karsenti, E. (1993) Regulation of cyclin-dependent kinases and tyrosine phosphatases during the cell cycle.Eur. J. Cell Biol. 61(Suppl 38), 6–12.
Kakizuka, A., Sebastian, B., Borgmeyer, U., Hermans-Borgmeyer, I., Bolado, J., Hunter, T., Hoekstra, M. F., and Evans, R. M. (1992) A mouse cdc25 homolog is differentially and developmentally expressed.Genes Dev. 6, 578–590.
Hoffmann, I., Clarke, P. R., Marcote, M. J., Karsenti, E., and Draetta, G. (1993) Phosphorylation and activation of cdc25-C by cdc2-cyclin B and its involvement in the self-amplification of MPF at mitosis.EMBO J. 12, 53–63.
Strausfeld, U., Fernandez, A., Capony, J.-P., Girard, F., Lautredou, N., Derancourt, J., Labbe, J.-C., and Lamb, N. J. C. (1994) Activation of p34cdc2 kinase by microinjection of human cdc25C into mammalian cells.J. Biol. Chem. 269, 5989–6000.
Jinno, S., Suto, K., Nagata, A., Igarishi, M., Kanaoka, Y., Nojima, H., and Okayama, H. (1994) Cdc25A is a novel phosphatase functioning early in the cell cycle.EMBO J. 13, 1549–1556.
Hoffmann, I., Draetta, G., and Karsenti, E. (1994) Activation of the phosphatase activity of human cdc25A by a cdk2-cyclin E dependent phosphorylation at the G1/S transition.EMBO J. 13, 4302–4310.
Millar, J. B., Blevitt, J., Gerace, L., Sadhu, K., Featherstone, C., and Russell, P. (1991) p55CDC25 is a nuclear protein required for the initiation of mitosis in human cells.Proc. Natl. Acad. Sci. USA 88, 10,500–10,504.
Zheng, X.-F. and Ruderman, J. V. (1993) Functional analysis of the P box, a domain required for the activation of cdc25.Cell 75 155–164.
Izumi, T. and Maller, J. L. (1993) Elimination of cdc2 phosphorylation sites in the cdc25 phosphatase blocks initiation of M-phase.Mol. Biol. Cell 4, 1337–1350.
Walker, D. H., and Maller, J. L. (1991) Role for cyclin-A in the dependence of mitosis on completion of DNA-replication.Nature 354, 314–317.
Clarke, P. R., Leiss, D., Pagano, M., and Karsenti, E. (1992) Cyclin A-dependent and cyclin B-dependent protein kinases are regulated by different mechanisms inXenopus egg extracts.The EMBO J. 11, 1751–1761.
Devault, A., Fesquet, D., Cavadore, J. C., Garrigues, A. M., Labbe, J. C., Lorca, T., Picard, A., Philippe, M., and Doree, M. (1992) Cyclin A potentiates maturation promoting factor activation in the earlyXenopus embryo via inhibition of the tyrosine kinase that phosphorylates cdc2.J. Cell Biol. 118, 1109–1120.
Izumi, T., Walker, D. H., and Maller, J. L. (1992) Periodic changes in phosphorylation of theXenopus cdc25 phosphatase regulate its activity.Mol. Biol. Cell 3, 927–939.
Yeudall, W. A. and Jakus, J. (1995) Cyclin kinase inhibitors add a new dimension to cell cycle control.Oral Oncol. Eur. J. Cancer 31, 291–298.
Peter, M. and Herslowitz, I. (1994) Joining the complex:cyclin-dependent kinase inhibitory proteins and the cell cycle.Cell 79, 181–184.
Ellidge, S. J., Winston, J., and Harper, J. W. (1996) A question of balance: the role of cyclin-kinase inhibitors in development and tumorigenesis.Trends Cell Biol. 6, 388–392.
Hunter, T. and Pines, J. (1994) Cyclins and cancer II: cyclin D and CDK inhibitors come of age.Cell 79, 573–582.
Gallant, P. and Nigg, E. A. (1994) Identification of a novel vertebrate cyclin: cyclin B3 shares properties with both A- and B-type cyclins.EMBO J. 13, 595–605.
McGowan, C. H., Russell, P., and Reed, S. I. (1990) Periodic biosynthesis of the human M-phase promoting factor catalytic subunit p34 during the cell-cycle.Mol. Cell. Biol. 10, 3847–3851.
Dalton, S. (1992) Cell cycle regulation of the humancdc2 gene.EMBO J. 11, 1797–1804.
Welch, P. J. and Wang, J. Y. J. (1992) Coordinated synthesis and degradation of cdc2 in the mammalian cell cycle.Proc. Natl. Acad. Sci. USA 89, 3093–3097.
Gautier, J., Norbury, C., Lohka, M., Nurse, P., and Maller, J. (1988) Purified maturation-promoting factor contains the product of a Xenopus homolog of the fission yeast cell cycle control genecdc2 2+.Cell 54, 433–439.
Arion, D., Meijer, L., Brizuela, L., and Beach, D. (1988)cdc2 is a component of the M phase-specific histone H1 kinase: evidence for identity with MPF.Cell 55, 371–378.
Meijer, L., Arion, D., Golsteyn, R., Pines, J., Brizuela, L., Hunt, T., and Beach, D. (1989) Cyclin is a component of the sea urchin egg M-phase specific histone H1 kinase.EMBO J. 8, 2275–2282.
Labbe, J. C., Picard, A., Peaucellier, G., Cavadore, J. C., Nurse, P., and Doree, M. (1989) Purification of MPF from starfish: identification as the histone H1 kinase p34cdc2 and a possible mechanism for its periodic action.Cell 57, 253–263.
Draetta, G., Luca, F., Westendorf, J., Brizuela, L., Ruderman, J., and Beach, D. (1989) cdc2 protein kinase is complexed with both cyclin A and B: evidence for proteolytic inactivation of MPF.Cell 56, 829–836.
Buendia, B., Draetta, G., and Karsenti, E. (1992) Regulation of the microtubule nucleating activity of centrosomes inXenopus egg extracts: role of cyclin A-associated protein kinase.J. Cell Biol. 116, 1431–1442.
Bailly, E., Pines, J., Hunter, T., and Bornens, M. (1992) Cytoplasmic accumulation of cyclin-B1 in human cells—association with a detergent-resistant compartment and with the centrosome.J. Cell Sci. 101, 529–545.
Maldonado, G. and Glover, D. M. (1992) Cyclin-A and cyclin-B associate with chromatin and the polar-regions of spindles, respectively, and do not undergo complete degradation at anaphase in syncytialDrosophila embryos.J. Cell Biol 116, 967–976.
Verde, F., Dogterom, M., Stelzer, E., Karsenti, E., and Leibler, S. (1992) Control of microtubule dynamics and length by cyclin A-dependent and cyclin B-dependent kinases inXenopus egg extracts.J. Cell Biol. 118, 1097–1108.
Pines, J. and Hunter, T. (1991) Human cyclin-A and cyclin-B are differentially located in the cell and undergo cell-cycle dependent nuclear transport.J. Cell Biol. 115, 1–17.
Gallant, P. and Nigg, E. A. (1992) Cyclin-B2 undergoes cell cycle-dependent nuclear translocation and, when expressed as a non-destructable mutant, causes mitotic arrest in HeLa cells.J. Cell Biol. 117, 213–224.
Jackman, M., Firth, M., and Pines, J. (1995) Human cyclins B1 and B2 are localized to strikingly different structures: B1 to microtubules, B2 primarily to the Golgi apparatus.EMBO J. 14, 1646–1654.
Peter, M., Nakagawa, J., Doree, M., Labbe, J.-C., and Nigg, E. A. (1990)In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase.Cell 61, 591–602.
Ward, G. E. and Kirschner, M. W. (1990) Identification of cell cycle-regulated phosphorylation sites on nuclear lamin C.Cell 61, 561–577.
Dessev, G., Iovcheva-Dessev, C., Bischoff, J. R., Beach, D., and Goldman, R. (1991) a complex containing p34cdc2 and cyclin B phosphorylates the nuclear lamina and disassembles nuclei of clamin vitro.J. Cell Biol. 112, 523–533.
Peter, M., Heitlinger, E., Haener, M., Aebi, U., and Nigg, E. A. (1991) Disassembly ofin vitro formed lamin head-to-tail polymers by cdc2 kinase.EMBO J. 10, 1535–1544.
Heald, R. and McKeon, F. (1990) Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis.Cell 61, 579–589.
Chou, Y.-H., Bischoff, J. R., Beach, D., and Goldman, R. (1990) Intermediate filament reorganisation during mitosis is mediated by p34cdc2 phosphorylation of vimentin.Cell 62, 1063–1071.
Shiina, N., Moriguchi, T., Ohta, K., Gotoh, Y., and Nishida, E. (1992) Regulation of a major microtubule associated protein by MPF and MAP kinase.EMBO J 11, 3977–3988.
Satterwhite, L. L., Lohka, M. J., Wilson, K. L., Scherson, T. Y., Cisek, L. J., Corden, J. L., and Pollard, T. D. (1992) Phosphorylation of myosin-II regulatory light chain by cyclin-p34cdc2: a mechanism for the timing of cytokinesis.J. Cell Biol. 118, 595–605.
Shenoy, S., Choi, J., Bagrodia, S., Copeland, T. D., Maller, J. L., and Shalloway, D. (1989) Purified maturation promoting factor phosphorylates pp60c-src at the sites phosphorylated during fibroblast mitosis.Cell 57, 763–774.
Morgan, D. O., Kaplan, J. M., Bishop, J. M., and Varmus, H. E. (1989) Mitosis-specific phosphorylation of p60c-src by p34cdc2-associated protein kinase.Cell 57, 775–786.
Shenoy, S., Chackalaparampil, I., Bagrodia, S., Lin, P.-H., and Shalloway, D. (1992) Role of p34cdc2 mediated phosphorylations in two step activation of p60c-src during mitosis.Proc. Natl. Acad. Sci. USA 89, 7237–7241.
Kipreos, E. T. and Wang, J. Y. (1990) Differential phosphorylation of c-Abl in cell cycle determined by cdc2 kinase and phosphatase activity.Science 248, 217–220.
Kipreos, E. t. and Wang, J. Y. (1992) Cell cycle regulated binding of c-abl tyrosine kinase to DNA.Science 256, 382–385.
Litchfield, D. W., Lozeman, F. J., Cicirelli, M. F., Harrylock, M., Ericsson, L. H., Piening, C. J., and Krebs, E. G. (1991) Phosphorylation of the beta subunit of casein kinase II in human A431 cells. Identification of the autophosphorylation site and a site phosphorylated by p34cdc2.J. Biol. Chem. 266, 20,380–20,389.
Litchfield, D. W., Luescher, B., Lozeman, F. J., Eisenman, R. N., and Krebs, E. G. (1992) Phosphorylation of casein kinase IIin vitro and at mitosis.J. Biol. Chem. 267, 13,943–13,951.
Langan, T. A., Gautier, J., Lohka, M., Hollingsworth, R., Moreno, S., Nurse, P., Maller, J., and Sclafani, R. A. (1989) Mammalian growth-associated H1 histone kinase: a homolog ofcdc2 +/CDC28 protein kinase controlling mitotic entry in yeast and frog cells.Mol. Cell. Biol. 9, 3860–3868.
Meijer, L., Ostvold, A.-C., Walaas, S. I., Lund, T., and Laland, S. G. (1991) High mobility-group proteins P1, I, Y as substrates of the M-phase-specific p34cdc2/ cyclincdc13 kinase.Eur. J. Biochem. 196, 557–567.
Nissen, M. S., Langan, T. A., and Reeves, R. (1991). Phosphorylation by cdc2 kinase modulates DNA binding activity of high mobility group I nonhistone chromatin protein.J. Biol. Chem. 266, 19,945–19,952.
Belengeur, P., Caizergues-Ferrer, M., Labbe, J.-C., Doree, M., and Amalric, F. (1990) Mitosis specific phosphorylation of nucleolin by p34cdc2 kinase.Mol. Cell. Biol. 10, 3607–3618.
Luscher, B., and Eisenman, R. N. (1992) Mitosis-specific phosphorylation of the nuclear oncoproteins myc and myb.J. Cell. Biol. 118, 775–784.
Peter, M., Nakagawa, J., Doree, M., Labbe, J.-C., and Nigg, E. A. (1990) Identification of major nucleolar proteins as candidate mitotic substrates of cdc2 kinase.Cell 60, 791–801.
Gurley, L. R., Valdez, J. G., and Buchanan, J. S. (1995) Characterisation of the mitotic specific phosphorylation site of Histone H1.J. Biol. Chem. 270, 27,653–27,660.
Evans, T., Rosenthal, E. T., Youngblom, J., Distel, D., and Hunt, T. (1983) Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division.Cell 33, 389–396.
Cardoso, M. C., Leonhardt, H., and Nadal-Ginard, B. (1993) Reversal of terminal differentiation and control of DNA replication: cyclin A and cdk2 specifically localize at subnuclear sites of DNA replication.Cell 74, 979–992.
Girard, F., Strausfeld, U., Fernandez, A., and Lamb, N. J. C. (1991) Cyclin A is required for the onset of DNA replication in mammalian fibroblasts.Cell 67, 1169–1179.
Pagano, M., Pepperkok, R., Verde, F., Ansorge, W., and Draetta, G. (1992) Cyclin A is required at two points in the human cell cycle.EMBO J. 11, 961–971.
Lehner, C. F. and O'Farrell, P. H. (1989) Expression and function ofDrosophila cyclin A during embryogenic cell cycle progression.Cell 56, 957–968.
Zindy, F., Lamas, E., Chenivesse, X., Sobczak, J., Wang, J., Fesquet, D., Henglein, B., and Brechot, C. (1992) Cyclin A is required in S phase in normal epithelial cells.Biochem. Biophys. Res. Commun. 182, 1144–1154.
Sherr, C. J. (1993) Mammalian G1 cyclins.Cell 73, 1059–1065.
Sherr, C. J. (1995) D-type cyclins. TIBS20, 187–190.
Matsushime, H., Roussel, M. F., Ashmun, R. A., and Sherr, C. J. (1991) Colony-stimulating factor 1 regulates novel cyclins during the G1 phase of the cell cycle.Cell 65, 701–713.
Kato, J. Y., and Sherr, C. J. (1993) Inhibition of granulocyte differentiation by G1 cyclins D2 and D3 but not D1.Proc. Natl. Acad. Sci. USA 90, 11,513–11,517.
Sewing, A., Burger, C., Brusselbach, S., Schalk, C., Lucibello, F. C., and Muller, R. (1993) Human cyclin D1 encodes a labile nuclear protein whose synthesis is directly induced by growth factors and suppressed by cyclic AMP.J. Cell Sci. 104, 545–554.
Motokura, T., Bloom, T., Kim, H. G., Juppner, H., Ruderman, J. V., Kronenberg, H. M., and Arnold, A. (1991) A novel cyclin encoded by abcl-linked candi-date oncogene.Nature 350, 512–515.
Withers, D. A., Harvey, R. C., Faust, J. B., Melnyk, O., Carey, K., and Meeker, T. C. (1991) Characterisation of a candidatebcl-1 gene.Mol. Cell. Biol. 11, 4846–4853.
Hanna, Z., Jankowski, M., Tremblay, P., Jiang, X., Milatovich, A., Francke, U., and Jolicoeur, P. (1993) Thevin-1 gene, identified by provirus insertional mutagenesis, is the cyclin D2.Oncogene 8, 1661–1666.
Won, K. A., Xiong, Y., Beach, D., and Gilman, M. Z. (1992) Growth-regulated expression of D-type cyclin genes in human diploid fibroblasts.Proc. Natl. Acad. Sci. USA 89, 9910–9914.
Ajchenbaum, F., Ando, K., DeCaprio, J. A., and Griffen, J. D. (1993) Independent regulation of human D-type cyclin gene expression during the G1 phase in primary human t lymphocytes.J. Biol. Chem. 268, 4113–4119.
Lukas, J., Bartkova, J., and Bartek, J. (1996) Convergence of mitogenic signalling cascades from diverse classes of receptors at the cyclin D-cyclin-dependent kinase-pRb-controlled G1 checkpoint.Mol. Cell. Biol. 16, 6917–6925.
Quelle, D. E., Ashmun, R. A., Shurtleff, S. A., Kato, J.-Y., Bar-Sagi, D., Roussel, M. F., and Sherr, C. J. (1993) Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts.Genes Dev. 7, 1559–1571.
Resnitzky, D., Gossen, M., Bujard, H., and Reed, S. I. (1994) Acceleration of the G1/S phase transition by expression of cyclins D1 and E with an inducible system.Mol. Cell. Biol. 14, 1669–1679.
Resnitzky, D. and Reed, S. I. (1995) Different roles for cyclins D1 and E in regulation of the G1-to-S transition.Mol. Cell. Biol. 15, 3463–3469.
Baldin, V., Lukas, J., Marcote, M. J., Pagano, M., and Draetta, G. (1993) Cyclin D1 is a nuclear protein required for cell cycle progression in G1.Genes Dev. 7, 812–821.
Sewing, A., Ronicke, V., Burger, C., Funk, M., and Muller, R. (1994) Alternative splicing of human cyclin E.J. Cell Sci. 107, 581–588.
Ohtsubo, M., Theodoras, A. M., Schumacher, J., Roberts, J. M., and Pagano, M. (1995) Human cyclin E, a nuclear protein essential for the G1-to-S phase transition.Mol. Cell. Biol. 15, 2612–2624.
D'Urso, G., Marraccino, R., Marshak, D., and Roberts, J. (1990) Cell cycle control of DNA replication by a homologue from human cells of the p34cdc2 protein kinase.Science 250, 786–791.
Dulic, V., Lees, E., and Reed, S. I. (1992) Association of human cyclin E with a periodic G1-S phase protein kinase.Science 257, 1958–1961.
Dulic, V., Drullinger, L., Lees, E., Reed, S., and Stein, G. (1993) Altered regulation of G1 cyclins in senescent human diploid fibroblasts: accumulation of inactive cyclin E-Cdk2 and cyclin D1-Cdk2 complexes.Proc. Natl. Acad. Sci. USA 90, 11,034–11,038.
Ohtsubo, M., Theodoras, A. M., Schumacher, J., Roberts, J. M., and Pagano, M. (1995) Human cyclin E, a nuclear protein essential for the G1-to-S phase transition.Mol. Cell. Biol. 15, 2612–2624.
Won, K.-A. and Reed, S. I. (1996) Activation of cyclin E/CDK2 is coupled to site-specific autophosphorylation and ubiquitin-dependent degradation of cyclin E.EMBO J. 15, 4182–4193.
Knoblich, J. A., Sauer, K., Jones, L., Richardson, H., Saint, R., and Lehner, C. F. (1994) Cyclin E controls S phase progression and its down-regulation during Drosophila embryogenesis is required for the arrest of cell proliferation.Cell 77, 107–120.
Wimmel, A., Lucibello, F. C., Sewing, A., Adolph, S., and Muller, R. (1994) Inducible acceleration of G1 progression through tetracyclin regulated expression of human cyclin E.Oncogene 9, 995–997.
Ohtsubo, M. and Roberts, J. (1993) Cyclin-dependent regulation of G1 in mammalian fibroblasts.Science 259, 1908–1912.
Mudryi, M., Devoto, S. H., Hiebert, S. W., Hunter, T., Pines, J., and Nevins, J. R. (1991) Cell cycle regulation of the E2F transcription factor involves an interaction with cyclin A.Cell 65, 1243–1253.
Devoto, S. H., Mudryi, M., Pines, J., Hunter, T., and Nevins, J. R. (1992) A cyclin A-protein kinase complex possesses sequence-specific DNA binding activity: p33cdk2 is a component of the E2F-cyclin A complex.Cell 68, 167–176.
Shirodkar, S., Ewen, M., DeCaprio, J. A., Morgan, J., Livingston, D. M., and Chittenden, T. (1992) The transcription factor E2F interacts with the retinoblastoma gene product and a p107-cyclin A complex in a cell cycle- regulated manner.Cell 68, 157–166.
Kato, J-Y., Matsushime, H., Hiebert, S. W., Ewen, M. E., and Sherr, C. J. (1993) Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4.Genes Dev. 7, 331–342.
Ewen, M. E., Sluss, H. K., Sherr, C. J., Matsushime, H., Kato, J.-Y., and Livingston, D. M. (1993) Functional interactions of the retinoblastoma protein with mammalian D-type cyclins.Cell 73, 487–497.
Dowdy, S. F., Hinds, P. W., Louie, K., Reed, S. I., Arnold, A., and Weinberg, R. A. (1993) Physical interaction of the retinoblastoma protein with human D cyclins.Cell 73, 499–511.
Lukas, J., Bartkova, J., Rohde, M., Strauss, M., and Bartek, J. (1995) Cyclin D1 is dispensable for G1 control in retinoblastoma gene-deficient cells independently of cdk4 activity.Mol. Cell. Biol. 15, 2600–2611.
Krek, W., Xu, G., and Livingston, D. M. (1995) Cyclin A-kinase regulation of E2F-1 DNA binding function underlies suppression of an S phase checkpoint.Cell 83, 1149–1158.
DeGregori, J., Leone, G., Ohtani, K., Miron, A., and Nevins, J. R. (1995) E2F-1 accumulation bypasses a G1 arrest resulting from the inhibition of G1 cyclin-dependent kinase activity.Genes Dev. 9, 2873–2887.
Hatakeyama, M. and Weinberg, R. A. (1995) The role of RB in cell cycle control.Prog. Cell Cycle Res. 1, 9–19.
Cobrinik, D. (1995) Regulatory interactions among E2Fs and cell cycle control proteins.Curr. Top. Microbiol. and Immunol. 208, 32–61.
Xiao, Z.-X., Ginsberg, D., Ewen, M., and Livingston, D. M. (1996) Regulation of the retinoblastoma protein-related protein p107 by G1 cyclin-associated kinases.Proc. Natl. Acad. Sci. USA 93, 4633–4637.
Duronio, R. J., Brook, A., Dyson, N., and O'Farrell, P. H. (1996) E2F-induced S phase requirescyclin E.Genes Dev. 10, 2505–2513.
Hofmann, F. and Livingston, D. M. (1996) Differential effects of cdk2 and cdk3 on the control of pRb and E2F function during G1 exit.Genes Dev. 10, 851–861.
Zwicker, J. and Muller, R. (1995) Cell cycle regulated transcription in mammalian cells.Progr. Cell Cycle Res. 1, 91–99.
Kitagawa, M., Higashi, H., Jung, H.-K., Suzuki-Takahashi, I., Ikeda, M., Tamai, K., Kato, J.-Y., Segawa, K., Yoshida, E., Nishimura, S., and Taya, Y. (1996) The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2.EMBO J. 15, 7060–7069.
Schwarz, J. K., Devoto, S. H., Smith, E. J., Chellapan, S. P., Jakoi, L., and Nevins, J. R. (1993) Interaction of the p107 and Rb proteins with E2F during the cell proliferation response.EMBO J. 12, 1013–1020.
Johnson, D. G., Ohtani, K., and Nevins, J. R. (1994) Autoregulatory control of E2F-1 expression in response to positive and negative regulators of cell cycle progression.Genes Dev. 7, 331–342.
Dynlacht, B. D., Flores, O., Less, J. A., and Harlow, E. (1994) Differential regulation of E2Ftrans-activation by cyclin/cdk2 complexes.Genes Dev. 8, 1772–1786.
Krek, W., Ewen, M. E., Shirodkar, S., Arany, Z., Kaelin, W. G., and Livingston, D. M. (1994) Negative regulation of the growth-promoting transcription factor E2F-1 by a stably bound cyclin A-dependent protein kinase.Cell 78, 161–172.
Xu, M., Sheppard, K.-A., Peng, C.-Y., Yee, A. S., and Piwnica-Worms, H. (1994) Cyclin A/CDK2 binds directly to E2F-1 and inhibits the DNA-binding activity of E2F-1/DP-1 by phosphorylation.Mol. Biol. Cell 14, 8420–8431.
Ohtani, K., DeGregori, J., and Nevins, J. R. (1995) Regulation of the cyclin E gene by transcription factor E2F1.Proc. Natl. Acad. Sci. USA 92, 12,146–12,150.
Geng, Y., Eaton, E. N., Picon, M., Roberts, J. M., Lundberg, A. S., Gifford, A., Sardet, C., and Weinberg, R. A. (1996) Regulation of cyclin E transcription by E2Fs and retinoblastoma protein.Oncogene 12, 1173–1180.
Bunnell, B. A., Heath, L. S. Adams, D. E., Lahti, J. M., and Kidd, V. J. (1990) Increased expression of a 58-kDa protein kinase leads to changes in the CHO cell cycle.Proc. Natl. Acad. Sci. USA 87, 7467–7471.
Okuda, T., Cleveland, J. L., and Downing, J. R. (1992)PCTAIRE-1 andPCTAIRE-3, two members of a novelcdc2/CDC28-related protein kinase gene family.Oncogene 7, 2249–2258.
Lapidot-Lifson, Y., Patinkin, D., Prody, C. A., Ehrlich, G., Seidman, S., Ben-Aziz, R., Benseller, F., Eckstein, F., Zakut, H., and Soreq, H. (1992) Cloning and oligodeoxynucleotide inhibition of a human homolog ofcdc2 required in hematopoiesis.Proc. Natl. Acad. Sci. USA 89, 579–583.
Li, H., Grenet, J., Valentine, M., Lahti, J. M., and Kidd, V. J. (1995) Structure and expression of chicken protein kinase PITSLRE-encoding genes.Gene 153, 237–242.
Lahti, J. M., Xiang, J., and Kidd, V. J. (1995) The PITSLRE protein family.Progr. Cell Cycle Res. 1, 329–338.
Grana, X., De Luca, A., Sang, N., Fu, Y., Claudio, P. P., Rosenblatt, J., Morgan, D. O., and Giordano, A. (1994) PITALRE, a nuclear CDC2-related protein kinase that phosphorylates the retinoblastoma proteinin vitro.Proc. Natl. Acad. Sci. USA 91, 3834–3838.
Brambilla, R. and Draetta, G. (1994) Molecular cloning of PISSLRE, a novel putative member of the cdk family of protein serine/threonine kinases.Oncogene 9, 3037–3041.
Grana, X., Claudio, P. P., De Luca, A., Sang, N., and Giordano, A. (1994) PISSLRE, a human novel CDC2-related protein kinase.Oncogene 9, 2097–2103
Daksis, J. I., Lu, R. Y., Facchini, L. M., Martin, M. W., and Penn, L. J. Z. (1994) Myc induces cyclin D1 expression in the absence ofde novo protein synthesis and links mitogen-stimulated signal transduction to the cell cycle.Oncogene 12, 3635–3645.
Jansen-Durr, P., Meichle, A., Steiner, P., Pagano, M., Finke, K., Botz, J., Wessbecher, J., Draetta, G., and Ellers, M. (1993) Differential modulation of cyclin gene expression byMYC.Proc. Natl. Acad. Sci. USA 90, 3685–3689.
Colasanti J., Cho, S.-O., Wick, S., and Sundaresan, V. (1993) Localization of the functional p34cdc2 homolog of maize in root tip and stomatal complex cells: association with predicted division sites.Plant Cell 5, 1101–1111.
Jacobs, T. W. (1995) Cell cycle control.Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 317–339.
Doerner, P. W. (1994) Cell cycle regulation in plants.Plant Physiol. 106, 823–827.
Francis, D. (1992) The cell cycle in plant development.New Phytol. 122, 1–20.
Hata, S., Kouchi, H., Suzuka, J., and Ishii, T. (1991) Isolation and characterization of cDNA clones for plant cyclins.EMBO J. 10, 2681–2688.
Hemerly, A., Bergounioux, C., Van Montagu, M., Inze, D., and Ferreira, P. (1992) Genes regulating the plant cell cycle: isolation of a mitotic-like cyclin fromArabidopsis thaliana.Proc. Natl. Acad. Sci. USA 89, 3295–3299.
Hirt, H., Mink, M., Pfosser, M., Bogre, L., Gyogyey, J., Jonak, C., Gartner, A., Dudits, D., and Heberle-Bors, E. (1992) Alfalfa cyclins: differential expression during the cell cycle and in plant organs.Plant Cell 4, 1531–1538.
Ferreira, P., Hemerly, A., de Almeida Engler, J., Bergounioux, C., Burssens, S., Van Montagu, M., Engler, G., and Inze, D. (1994) Three discrete classes ofArabidopsis cyclins are expressed during different intervals of the cell cycle.Proc. Natl Acad. Sci. USA 91, 11,313–11,317.
Ferreira, P. C. G., Hemerly, A. S., de Almeida Engler, J., Van Montagu, M., Engler, G., and Inze, D. (1994) Developmental expression of the Arabidopsis cyclin genecyc1At.Plant Cell 6, 1763–1774.
Day, I. S. and Reddy, A. S. N. (1994) Cloning of a family of cyclins from,Arabidopsis Thaliana.Biochim. Biophys. Acta 1218, 115–118.
Fobert, P. R., Coen, E. S., Murphy, G. J. P., and Doonan J. H. (1994) Patterns of cell division revealed by transcriptional regulation of genes during the cell cycle in plants.EMBO J. 13, 616–624.
Renaudin, J.-P., Colasanti, J., Rime, H., Yuan, Z., and Sundaresan, V. (1994) Cloning of four cyclins from maize indicates that higher plants have three structurally distinct groups of mitotic cyclins.Proc. Natl. Acad. Sci. USA 91, 7375–7379.
Dahl, M., Meskiene, I., Bogre, L., Ha, D. T. C., Swoboda, I., Hubmann, R., Hirt, H., and Heberle-Bors, E. (1995) The D-type alfalfa cyclin genecycMs4 complements G1 cyclin-deficient yeast and is, induced in the G1 phase of the cell cycle.Plant Cell 7, 1847–1857.
Soni R., Carmichael, J. P., Shah, Z. H., and Murray, J. A. H. (1995) A family of cyclin D homologs from plants differentially controlled by growth, regulators and containing the conserved retinoblastoma protein interaction motif.Plant Cell 7, 85–103.
Setiady, Y. Y., Sekine, M., Hariguchi, N., Yamamoto, T., Kouchi, H., and Shinmyo, A. (1995) Tobacco mitotic cyclins: cloning, characterisation, gene expression and functional assay.Plant J. 8, 949–957.
Savoure, A., Feher, A., Kalo, P., Petrovics, G., Csanadi, G., Szecsi, J., Kiss, G., Brown, S., Kondorosi, A., and Kondorosi, E. (1995) Isolation of a full length mitotic cyclin cloneCycIIIMs fromMedicago sativa: chromosomal mapping and expression.Plant Mol. Biol. 27, 1059–1070.
Kouchi, H., Sekine, M., and Hata, S. (1995) Distinct classes of mitotic cyclins are differentially expressed in the soybean shoot apex during the cell cycle.Plant Cell 7, 1143–1155.
Meskiene, I., Bogre, L., Dahl, M., Pirck, M., Ha, D. T. C., Swododa, I., Heberle-Bors, E., Ammerer, G., and Hirt, H. (1995)cycMs3, a novel B-type alfalfa cyclin gene, is induced in the G0-to-G1 transition of the cell cycle.Plant Cell 7, 759–771.
Szarka, S., Fitch, M., Schaerer, S., and Moloney, M. (1995) Classification and expression of a family of cyclin homologues inBrassica napus.Plant Mol. Biol. 27, 263–275.
Shaul, O., Mironov, V., Van Montagu, M., and Inze, D. (1996) TwoArabidopsis cyclin promoters mediate distinctive transcriptional oscillation in synchronized tobacco BY-2 cells.Proc. Natl. Acad. Sci. USA 93, 4868–4872.
Day, I. S., Reddy, A. S. N., and Golovkin, M. (1996) Isolation of a new mitotic cyclin from Arabidopsis: complementation of a yeast mutant with a plant cyclin.Plant Mol. Biol. 30, 565–575.
Fuerst, R. A. U. A., Soni, R., Murray, J. A. H., and Lindsay, K. (1996) Modulation of cyclin transcript levels in cultured cells ofArabidopsis thaliana.Plant Physiol. 112, 1023–1033.
Feiler, H. S. and Jacobs, T. W. (1990) Cell division in higher plants: acdc2 gene, its 34-kDa product and histone H1 kinase activity in pea.Proc. Natl. Acad. Sci. USA 87, 5397–5401.
Hirayama, T., Imajuku, Y., Matsui, M., and Oka, A. (1991) Identification of two cell-cycle-controllingcdc2 gene homologs inArabidopsis thaliana.Gene 105, 159–165.
Hata, S. (1991) cDNA cloning of a novel cdc2+/CDC28-related protein kinase from rice.FEBS Lett. 279, 149–152.
Hirt, H., Pay, A., Gyorgyey, J., Bako, L., Nemeth, K., Bogre, L., Schweyen, R. J., Heberle-Bors, E., and Dudits, D. (1991) Complementation of a yeast cell cycle mutant by an alfalfa cDNA encoding a protein kinase homologous to p34cdc2.Proc. Natl. Acad. Sci. USA 88, 1636–1640.
Colasanti, J., Tyers, M., and Sundaresan, V. (1991) Isolation and characterisation of cDNA clones encoding a functional p34cdc2 homologue fromZea mays.Proc. Natl. Acad. Sci. USA 88, 3377–3381.
Feiler, H. S. and Jacobs, T. W. (1991) Cloning of the peacdc2 homologue by efficient immunological screening of PCR products.Plant Mol. Biol. 17, 321–333.
Ferreira, P. C. G., Hemerly, A. S., Villarroel, R., Van Mantagu, M., and Inze, D. (1991) The Arabidopsis functional homolog of the p34cdc2 protein kinase.Plant Cell 3, 531–540.
Imajuku, Y., Hirayama, T., Endoh, H., and Oka, A. (1992) Exon-intron organisation of theArabidopsis thaliana protein kinase genes CDC2a and CDC2b.FEBS Lett. 304, 73–77.
Hashimoto, J., Hirabayashi, T., Hayano, Y., Hata, S., Ohashi, Y., Suzuka, I., Utsugi, T., Toh-E, A., and Kikuchi, Y. (1992) Isolation and characterisation of cDNA clones encodingcdc2 homologues fromOryza sativa: a functional homologue and cognate variants.Mol. Gen. Genetics 233, 10–16.
Martinez, M. C., Jorgensen, J.-E., Lawton, M. A., Lamb, C. J., and Doerner, P. W. (1992) Spatial pattern ofcdc2 expression in relation to meristem activity and cell proliferation during plant development.Proc. Natl. Acad. Sci. USA 89, 7360–7364.
Bergounioux, C., Perennes, C., Hemerly, A. S., Qin, L. X., Sarda, C., Inze, D., and Gadal, P. (1992) Acdc2 gene ofPetunia hybrida is differentially expressed in leaves, protoplasts and during various cell cycle phases.Plant Mol. Biol. 20, 1121–1130.
Magyar, Z., Bako, L., Bogre, L., Dedeoglu, D., Kapros, T., and Dudits, D. (1993) Activecdc2 genes and cell cycle phase-specific cdc2-related kinase complexes in hormone-stimulated alfalfa cells.Plant J. 4, 151–161.
Miao, G-H., Hong, Z., and Verma, D. P. S. (1993) Two functional soybean genes encoding p34cdc2 protein kinases are regulated by different plant developmental pathways.Proc. Natl. Acad. Sci. USA 90, 943–947.
Hirt, H., Pay, A., Bogre, L., Meskiene, I., and Heberle-Bors, E. (1993)cdc2MsB, a cognatecdc2 gene from alfalfa, complements the G1/S but not the G2/M transition of budding yeastcdc28 mutants.Plant J. 4, 61–69.
Hemerly, A. S., Ferreira, P., de Almeida Engler, J., Van Montagu, M., Engler, G., and Inze, D. (1993)cdc2a expression in Arabidopsis is linked with competence for cell division.Plant Cell 5, 1711–1723.
Russinova, E., Slater, A., Atanassov, A. I., and Elliott, M. C. (1995) Cloning novel alfalfa sequences—a RACE-PCR approach.Cell. Mol. Biol. 41, 703–714.
Qin, L.-X., Perennes, C., Richard, L., Bouvier-Durand, M., Trehin, C., Inze, D., and Bergounioux, C. (1996) G2- and early-M-specific expression of theNTCYC1 cyclin gene inNicotiana tabacum cells.Plant Mol. Biol. 32, 1093–1101.
Segers, G., Gadisseur, I., Bergounioux, C., de Almeida Engler, J., Jacqmard, A., Van Montagu, M., and Inze, D. (1996) TheArabidopsis cyclin-dependent kinase gene cdc2bAt is preferentially expressed during the S and G2 phases of the cell cycle.Plant J. 10, 601–612.
Fobert, P. R., Gaudin, V., Lunness, P., Coen, E. S., and Doonan, J. H. (1996) Distinct classes ofcdc2-related genes are differentially expressed during the cell division cycle in plants.Plant Cell 8, 1465–1476.
Magyar, Z., Meszaros, T., Miskolczi, P., Deak, M., Feher, A., Brown, S., Kondorosi, E., Athanasiadis, A., Pongor, S., Bilgin, M., Bako, L., Koncz, C., and Dudits, D. (1997) Cell cycle phase specificity of putative cyclin-dependent kinase varients in synchronised Alfalfa cells.Plant Cell 9, 223–235.
John, P. C. L., Sek, F. J., and Lee M. G. (1989) A homolog of the cell cycle control protein p34cde2 participates in the division cycle ofChlamydomonas, and a similar protein is detectable in higher plants and remote taxa.Plant Cell 1, 1185–1193.
John, P. C. L., Sek, F. J., Carmichael, J. P., and McCurdy, D. W. (1990) p34cdc2 homologue level, cell division, phytohormone responsiveness and cell differentiation in wheat leaves.J. Cell Sci. 97, 627–630.
Gorst, J. R., John, P. C. L., and Sek, F. J. (1991) Levels of p34cdc2-like protein in dividing, differentiating and dedifferentiating cells of carrot.Planta 185, 304–310.
Renaudin, J.-P., Doonan, J. H., Freeman, D., Hashimoto, J., Hirt, H., Inze, D., Jacobs, T., Kouchi, H., Rouze, P., Sauter, M., Savoure, A., Sorrell, D. A., Sundaresan, V., and Murray, J. A. H. (1996) Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organisation.Plant Mol. Biol.,32, 1003–1018.
Fowler, M. R., Kirby, M. J., Scott, N. W., Slater, A., and Elliott, M. C. (1996) Polyamine metabolism and gene-regulation during the transition of autonomous sugar-beet cells in suspension-culture from quiescence to division.Physiol. Plant 98, 439–446.
Doerner, P., Jorgensen, J.-E., You, R., Steppuhn, J. and Lamb, C. (1996) Control of root growth and development by cyclin expression.Nature 380, 520–523.
Chung, S. K. and Parish, R. W. (1995). Studies on the promoter of theArabidopsis thaliana cdc2a gene.FEBS Lett. 362, 215–219.
Bogre, L., Zwerger, K., Meskiene, I., Binarova, P., Csizadia, V., Planck, C., Wagner, E., Hirt, H., and Heberle-Bors, E. (1997) The cdc2Ms Kinase is differentially regulated in the cytoplasm and the nucleus.Plant Physiol. 113, 841–852.
Wang, H., Fowke, L. C., and Crosby, W. L. (1997) A plant cyclin-dependent kinase inhibitor gene.Nature 386, 451.
Grafi, G., and Larkins, B. A. (1995) Endoreduplication in maize endosperm: involvement of M phasepromoting factor inhibition and induction of S phase-related kinases.Science 269, 1262–1264.
Moran, T. V. and Walker, J. C. (1993) Molecular cloning of two novel protein kinase genes fromArabidopsis thaliana.Biochim. Biophys. Acta 1216, 9–14.
Elliott, M. C., Chen, D.-F., Fowler, M. L., Kirby, M. J., Kubalakova, M., Scott, N. W., and Slater, A. (1996) Transgenesis—A scheme for improving sugar-beet productivity.Russ. J. Plant Phys. 43, 544–551.
Fowler, M. R., Kirby, M. J., Scott, N. W., Slater, A., and Elliott, M. C. (1998) Induction of cell divisionrelated genes in quiescent (G0) sugar beet cells.Physiol. Plant. 102, 61–70.
Zhang, K., Letham, D. S., and John, P. C. L. (1996) Cytokinin controls the cell cycle at mitosis by stimulating the tyrosine dephosphorylation and activation of p34cdc2-like H1 histone kinase.Planta 200, 2–12.
Bell, M. H., Halford, N. G., Ormrod, J. C., and Francis, D. (1993). Tobacco plants transformed with cdc25, a mitotic inducer gene from fission yeast.Plant. Mol. Biol. 23, 445–451.
Minyuki, Y., Yamashita, M., and Nagahama, Y. (1991) p34cdc2 kinase homologue in the preprophase band.Protoplasma 162, 182–186.
Grafi, G., Burnett, R. J., Heleltjaris, T., Larkins, B. A., DeCaprio, J. A., Sellers, W. R., and Kaelin, W. G. (1996) A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication.Proc. Natl. Acad. Sci. USA 93, 8962–8967.
Xe, Q., Sanz-Burgos, P., Hannon, G. J., and Gutierrez, C. (1996) Plant cells contain a novel member of growth regulatory proteins.EMBO J. 15, 4900–4908.
Chiatante, D., and Bryant, J. A. (1994) Activity of DNA topoisomerase I and quiescence of embryo cells in seeds of Pisum sativum L.J. Exp. Bot. 45, 959–965.
Fowler, M. R. (1996) Gene expression during sugar beet cell division, PhD thesis, De Montfort University, Leicester, England.
Hemerly, A., de Almeida Engler, J., Bergounioux, C., Van Montagu, M., Engler, G., Inze, D. and Ferreira, P. (1995) Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative development.EMBO J. 14, 3925–3936.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Fowler, M.R., Eyre, S., Scott, N.W. et al. The plant cell cycle in context. Mol Biotechnol 10, 123–153 (1998). https://doi.org/10.1007/BF02760861
Issue Date:
DOI: https://doi.org/10.1007/BF02760861