Plant Molecular Biology

, Volume 43, Issue 5–6, pp 677–690 | Cite as

Factors controlling cyclin B expression

  • Masaki Ito
Article

Abstract

Cyclins control the transition between the phases of the eukaryotic cell cycle as regulatory subunits of the cyclin-dependent kinases (CDKs). Phase-specific activation of the CDK is in part regulated by phase-specific expression of their cyclin component. In most eukaryotic cells including higher plant, B-type cyclin genes are expressed specifically at G2/M phase during the cell cycle. Promoters from yeast, plant and animal B-type cyclin genes are all activated in a cell cycle-regulated manner. In yeast, a transcription factor, Mcm1, in cooperation with an uncloned factor SFF, regulates the cell cycle-dependent promoter activation of mitotic B-type cyclin genes, CLB1 and CLB2. Activity of the human cyclin B1 promoter is regulated by a complex mechanism involving multiple cis-acting elements, none of which are sufficient for G2/M-specific promoter activation. In contrast, plants employ a simple mechanism for cell cycle-regulated promoter activation of B-type cyclin genes. Plant B-type cyclin gene promoters contain a common cis-acting element, called the MSA element, which is necessary and sufficient for the phase-specific promoter activation. MSA-like sequences are also found in the promoters of G2/M-specific genes encoding kinesin-like proteins, suggesting that a defined set of G2/M-specific genes are co-regulated by a common MSA-mediated mechanism in plants. Thus, the molecular mechanisms regulating B-type cyclin gene expression are evolutionarily divergent, and the MSA-mediated mechanism seems to be specific to plants. The consensus sequence of the MSA element resembles the binding sites of animal Myb transcription factors. A set of our data suggest the possibility that plant Myb may have unexpected roles in G2/M by inducing B-type cyclin genes, together with other cell cycle-related genes in plants.

B-type cyclin cell cycle cis-element promoter trans-acting factor transcriptional regulation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Althoefer, H., Schkeiffer, A., Wassmann, K., Nordheim, A. and Ammerer, G. 1995. Mcm1 is required to coordinate G2-specific transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 15: 5917–5928.PubMedGoogle Scholar
  2. Amon, A., Tyers, M., Futcher, B. and Nasmyth, K. 1993. Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins. Cell 74: 993–1007.PubMedGoogle Scholar
  3. Andrews, B. and Measday, V. 1998. The cyclin family of budding yeast: abundant use of a good idea. Trends Genet. 14: 66–72.PubMedGoogle Scholar
  4. Bai, C., Richman, R. and Elledge, S.J. 1994. Human cyclin F. EMBO J. 13: 6087–6098.PubMedGoogle Scholar
  5. Bender, A. and Sprague, G. 1987. MAT?1 protein, a yeast transcription activator, binds synergistically with a second protein to a set of cell-type-specific genes. Cell 50: 681–691.PubMedGoogle Scholar
  6. Brandt, T.L., Fraser, D.J., Leal, S., Halandras, P.M., Kroll, A.R. and Kroll, D.J. 1997. c-Myb trans-activates the human DNA topoisomerase II? gene promoter. J. Biol. Chem. 272: 6287–6284.Google Scholar
  7. Buckley, M.F., Sweeney, K.J., Hamilton, J.A., Sini, R.L., Manning, D.L., Nicholson, R.I., deFazio, A., Watts, C.K., Musgrove, E.A. and Sutherland, R.L. 1993. Expression and amplification of cyclin genes in human breast cancer. Oncogene 8: 2127–2133.PubMedGoogle Scholar
  8. Cogswell, J.P., Godlevski, M.M., Bonham, M., Bisi, J. and Babiss, L. 1995. Upstream stimulatory factor regulates expression of the cell cycle-dependent cyclin B1 gene promoter. Mol. Cell. Biol. 15: 2782–2790.PubMedGoogle Scholar
  9. Dahl, M., Meskiene, I., Bogre, L., Cam Ha, D.T, Swoboda, I., Hubmann, R., Hirt, H. and Heberle-Bors, E. 1955. The Dtype alfalfa cyclin gene cycMs4 complements G1 cyclin-deficient yeast and is induced in the G1 phase of the cell cycle. Plant Cell 7: 1847–1857.Google Scholar
  10. DeGregori, J., Kowalik, T. and Nevins, J.R. 1995. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis and G1/S-regulatory genes. Mol. Cell. Biol. 15: 5846–5847.Google Scholar
  11. De Veylder, L., de Almeida Engler, J., Burssens, S., Manevski, A., Lescure, B., Van Montagu, M., Engler, G. and Inzé, D. 1999. A new D-type cyclin of Arabidopsis thaliana expressed during lateral root primordia formation. Planta 208: 453–462.PubMedGoogle Scholar
  12. Desdouets, C., Matesic, G., Molina, C.A., Foulkes, N.S., Sassone-Corsi, P., Brechot, C. and Sobczak-Thepot, J. 1995. Cell cycle regulation of cyclin A gene expression by the cyclic AMPresponsive transcription factors CREB and CREM. Mol. Cell. Biol. 15: 3301–3309.PubMedGoogle Scholar
  13. 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.PubMedGoogle Scholar
  14. Dohrmann, P.R., Butler, G., Tamai, K., Dorland, S., Green, J.R., Thiele, D.J. and Stillman, D.J. 1992. Parallel pathways of gene regulation: homologous regulators SWI5 and ACE2 differentially control transcription of HO and chitinase. Genes Dev. 6: 93–104.PubMedGoogle Scholar
  15. Doonan, J. and Fobert, P. 1997. Conserved and novel regulators of the plant cell cycle. Curr. Opin. Cell Biol. 9: 824–830.PubMedGoogle Scholar
  16. 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.PubMedGoogle Scholar
  17. Farina, A., Gaetano, C., Crescenzi, M., Puccini, F., Manni, I., Sacchi, A. and Piaggio, G. 1996. The inhibition of cyclin B1 gene transcription in quiescent NIH3T3 cells is mediated by an E-box. Oncogene 13: 1287–1296.PubMedGoogle Scholar
  18. 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.PubMedGoogle Scholar
  19. Ferreira, P.C.G., Hemerly, A.S., de Almeida Engler, J., Bergounioux, C., Burssens, S., Van Montagu, M., Engler, G. and Inzé, D. 1994a. Three discrete classes of Arabidopsis cyclins are expressed during different intervals of the cell cycle. Proc. Natl. Acad. Sci. USA 91: 11313–11317.PubMedGoogle Scholar
  20. Ferreira, P.C.G., Hemerly, A.S., de Almeida Engler, J., Van Montagu, M., Engler, G. and Inzé, D. 1994b. Developmental expression of the Arabidopsis cyclin gene cyc1At. Plant Cell 6: 1763–1774.CrossRefPubMedGoogle Scholar
  21. Fitch, I., Dahmann, C., Surana, U., Amon, A., Nasmyth, K., Goetsch, L., Byers, B. and Futcher, B. 1992. Characterization of four B-type cyclin genes of the budding yeast Saccharomyces cerevisiae. Mol. Biol. Cell 3: 805–818.PubMedGoogle Scholar
  22. Fobert, P., 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.PubMedGoogle Scholar
  23. Fuerst, R.A.U.A., Soni, R., Murray, J.A.H. and Lindsey, K. 1996. Modulation of cyclin transcript levels in cultured cells of Arabidopsis thaliana. Plant Physiol. 112: 1023–1033.PubMedGoogle Scholar
  24. Futcher, B. 1996. Cyclins and wiring of the yeast cell cycle. Yeast 12: 1635–1646.PubMedGoogle Scholar
  25. Ghiara, J.B., Richardson, H.E., Sugimoto, K., Henze, M., Lew, D.J., Wittenberg, C. and Reed, S.I. 1991. A cyclin B homolog in S. cerevisiae: chronic activation of the Cdc28 protein kinase by cyclin prevents exit from mitosis. Cell 65: 163–174.PubMedGoogle Scholar
  26. Glotzer, M., Murray, A.W. and Kirshener, M.W. 1991. Cyclin is degraded by the ubiquitin pathway. Nature 349: 132–138.PubMedGoogle Scholar
  27. Gong, J., Ardelt, B., Traganos, F. and Darzynkiewicz, Z. 1994. Unscheduled expression of cyclin B1 and cyclin E in several leukemic and solid tumor lines. Cancer Res. 54: 4285–4288.PubMedGoogle Scholar
  28. Grotewold, E., Drummond, B.J., Bowen, B. and Peterson, T. 1994. The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76: 543–553.CrossRefPubMedGoogle Scholar
  29. Gregor, P.D., Sawadogo, M. and Roeder, R.G. 1990. The adenovirus major late transcription factor USF is a member of the helixloop-helix group of regulatory proteins and binds to DNA as a dimer. Genes Dev. 4: 1730–1740.PubMedGoogle Scholar
  30. Hata, S., Kouchi, H., Suzuka, I. and Ishii, T. 1991. Isolation and characterization of cDNA clones for plant cyclins. EMBO J. 10: 2681–2688.PubMedGoogle Scholar
  31. Hemerly, A., Bergounioux, C., Van Montagu, M., Inzé, D. and Ferreira, P. 1992. Genes regulating the plant cell cycle: isolation of a mitotic-like cyclin from Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 89: 3295–3299.PubMedGoogle Scholar
  32. Hirayama, T. and Shinozaki, K. 1996. A cdc5C homolog of a higher plant, Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 93: 13371–13376.PubMedGoogle Scholar
  33. Hirt, H., Mink, M., Pfosser, M., Bogre, L., Gyorgyey, 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.Google Scholar
  34. Howe, K.M. and Watson, R.J. 1991. Nucleotide preference in sequence-specific recognition of DNA by c-myb protein. Nucl. Acids Res. 19: 3913–3919.PubMedGoogle Scholar
  35. Hwang, A., Maity, A., McKenna, W.G. and Muschel, R.J. 1995. Cell cycle-dependent regulation of the cyclin B1 promoter. J. Biol. Chem. 270: 28419–28424.PubMedGoogle Scholar
  36. Hwang, A., McKenna, W.G. and Muschel, R.J. 1998. Cell cycle dependent usage of transcriptional start sites: a novel mechanism for regulation of cyclin B1. J. Biol. Chem. 273: 31505–31509.PubMedGoogle Scholar
  37. Ito, M. 1998. Cell cycle dependent gene expression. In: D. Francis, D. Dudits and D. Inzé (Eds.) Plant Cell Division, Portland Press, London/Miami, pp. 165–186.Google Scholar
  38. Ito, M., Criqui, M.-C., Sakabe, M., Ohno, T., Hata, S., Kouchi, H., Hashimoto, J., Fukuda, H., Komamine, A. and Watanabe, A. 1997. Cell-cycle-regulated transcription of A-and B-type plant cyclin genes in synchronous cultures. Plant J. 11: 983–992.PubMedGoogle Scholar
  39. Ito, M., Iwase, M., Kodama, H., Lavisse, P., Komamine, A., Nishihama, R., Machida, Y. and Watanabe, A. 1998. A novel cis-acting element in promoters of plant B-type cyclin genes activates M phase-specific transcription. Plant Cell 10: 331–341.PubMedGoogle Scholar
  40. Johnston, L.H., White, J.H.M., Johnson, A.L., Lucchini, G. and Plevani, P. 1987. The yeast DNA polymerase I transcripts is regulated in both the mitotic cell cycle and in meiosis and is also induced after DNA damage. Nucl. Acids Res. 15: 5017–5030.PubMedGoogle Scholar
  41. Katula, K.S., Wright, K.L., Paul, H., Surman, D.R., Nuckolls, F.J., Smith, J.W., Ting, J.P.-Y., Yates, J. and Cogswell, J.P. 1997. Cyclin-dependent kinase activation and S-phase induction of the cyclin B1 gene are linked through the CCAAT elements. Cell Growth Differ. 8: 811–820.PubMedGoogle Scholar
  42. Keleher, C.A., Goutte, C. and Johnston, A.D. 1988. The yeast cell-type-specific repressor ?2 acts cooperatively with a non-cell type-specific protein. Cell 53: 927–936.PubMedGoogle Scholar
  43. Kitada, K., Johnson, A.T., Johnson, L.H. and Sugino, A. 1993. A multicopy suppressor gene of Saccharomyces cerevisiae G1 cell cycle mutant gene dbf4 encodes a protein kinase and is identified as CDC5. Mol. Cell. Biol. 13: 4445–4457.PubMedGoogle Scholar
  44. 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, p34cdc2 and p32cdk2 protein kinase subunits. Mol. Biol. Cell 3: 1279–1294.PubMedGoogle Scholar
  45. Koch, C. and Nasmyth, K. 1994. Cell cycle regulated transcription in yeast. Curr. Opin. Cell Biol. 6: 451–459.CrossRefPubMedGoogle Scholar
  46. 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.PubMedGoogle Scholar
  47. Kranz, H.D., Denekamp, M., Greco, R., Jin, H., Leyva, A., Meissner, R.C., Petroni, K., Urzainqui, A., Bevan, M., Martin, C., Smeekens, S., Tonelli, C., Paz-Ares, J. and Weisshaar, B. 1998. Towards functional characterization of the member of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J. 16: 263–276.PubMedGoogle Scholar
  48. Ku, D.H., Wen, S.C., Engelhard, A., Nicolaides, N.C., Lipson, K.E., Marino, T.A. and Calabretta, B. 1993. c-myb transactivates cdc2 expression via Myb binding sites in the 50-flanking region of the human cdc2 gene. J. Biol. Chem. 268: 2255–2259.PubMedGoogle Scholar
  49. Kuo, M.-H. and Grayhack, E. 1994. A library of yeast genomic MCM1 binding sites contains genes involved in cell cycle control, cell wall and membrane structure, and metabolism. Mol. Cell. Biol. 14: 348–359.PubMedGoogle Scholar
  50. Lees, E.M. and Harlow, E.D. 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.PubMedGoogle Scholar
  51. Lew, D.J., Dulic, V. and Reed, S.I. 1991. Isolation of three novel human cyclins by rescue of G1 cyclin (Clb) function in yeast. Cell 66: 1197–1206.CrossRefPubMedGoogle Scholar
  52. Loy, C.J., Lydall, D. and Surana, U. 1999. NDD1, a high-dosage suppressor of cdc28-1N, is essential for expression of a subset of late-S-phase-specific genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 3312–3327.PubMedGoogle Scholar
  53. Lydall, D., Ammerer, G. and Nasmyth, K. 1991. A new role for MCM1 in yeast: cell cycle regulation of SWI5 transcription. Genes Dev. 5: 2405–2419.PubMedGoogle Scholar
  54. Machida, Y., Nakashima, M., Morikiyo, K., Banno, H., Ishikawa, M., Soyano, T. and Nishihama, R. 1998. MAPKKK-related protein kinase NPK1: regulation of the M phase of the plant cell cycle. J. Plant Res. 111: 243–246.Google Scholar
  55. Maher, M., Cong, F., Kindelberger, D., Nasmyth, K. and Dalton, S. 1995. Cell cycle-regulated transcription of the CLB2 gene is dependent of Mcm1 and Ternary complex factor. Mol. Cell. Biol. 15: 3129–3137.PubMedGoogle Scholar
  56. Maity, A., McKenna, W.G. and Muschel, R.J. 1995. Evidence for post-transcriptional regulation of cyclin B1 mRNA in the cell cycle and following irradiation in HeLa cells. EMBO J. 14: 603-609.PubMedGoogle Scholar
  57. Martin, C. and Paz-Ares, J. 1997. MYB transcription factors in plants. Trends Genet. 13: 67–73.PubMedGoogle Scholar
  58. McInerny, C.J., Partridge, J.F., Mikesell, G.E., Creemer, D.P. and Breeden, L.L. 1997. A novel Mcm1-dependent element in the SWI4, CLN3, CDC6, and CDC47 promoters activates M/G1-specific transcription. Genes Dev. 11: 1277–1288.PubMedGoogle Scholar
  59. McKinney, J.D. and Heintz, N. 1991. Transcriptional regulation in the eukaryotic cell cycle. Trends Biochem. Sci. 16: 430–435.PubMedGoogle Scholar
  60. Measday, V., Moore, L., Retnakaran, R., Lee, J., Donoviel, M., Neiman, A.M. and Andrews, B. 1997. A family of cyclin-like proteins that interact with the Pho85 cyclin-dependent kinase. Mol. Cell. Biol. 17: 1212–1223.PubMedGoogle Scholar
  61. Meskiene, I., Bogre, L., Dahl, M., Pirck, M., Ha, D.T.C., Swoboda, 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.CrossRefPubMedGoogle Scholar
  62. Minshull, J., Pines, J., Golstyen, R., Standart, N., Mackie, S., Colman, A., Blow, J., Ruderman, J., Wu, M. and Hunt, T. 1989. The role of cyclin synthesis, modification and destruction in the control of cell division. J. Cell Sci. 12: 77–97.Google Scholar
  63. Mironov, V., Van Montagu, M. and Inzé, D. 1997. Regulation of cell division in plants: an Arabidopsis perspective. Prog. Cell Cycle Res. 3: 29–41.PubMedGoogle Scholar
  64. Müller, R. 1995. Transcriptional regulation during the mammalian cell cycle. Trends Genet. 11: 173–178.PubMedGoogle Scholar
  65. Nagata, T., Nemoto, Y. and Hasezawa, S. 1992. Tobacco BY2 cell line as the ‘HeLa’ cell in cell biology of higher plants. Int. Rev. Cytol. 132: 1–30.Google Scholar
  66. Nasmyth, K. 1993. Control of the yeast cell cycle by the Cdc28 protein kinase. Curr. Opin. Cell Biol. 5: 166–179.PubMedGoogle Scholar
  67. Nigg, E.A. 1993. Cellular substrates of p34cdc2 and its companion cyclin-dependent kinases. Trends Cell Biol. 3: 296–301.PubMedGoogle Scholar
  68. Nigg, E.A. 1995. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays 17: 471–480.PubMedGoogle Scholar
  69. Norbury, C. and Nurse, P. 1992. Animal cell cycles and their control. Annu. Rev. Biochem. 61: 441–470.PubMedGoogle Scholar
  70. Ogas, J., Andrews, B.J. and Herskowitz, I. 1991. Transcriptional activation of CLN1 and CLN2, and a putative G1 cyclin (HCS26) by SWI4, a positive regulator of G1-specific transcription. Cell 66: 1015–1026.PubMedGoogle Scholar
  71. Ohi, R., Feoktistova, A., McCann, S., Valentine, V., Look, A.T., Lipsick, J.S. and Gould, K.L. 1998. Myb-related Schizosaccharomyces pombe cdc5p is structurally and functionally conserved in eukaryotes. Mol. Cell. Biol. 18: 4097–4108.PubMedGoogle Scholar
  72. Ohi, R., McCollum, D., Hirani, B., Den Haese, G.J., Zhang, X., Burke, J.D., Turner, K. and Gould, K.L. 1994. The Schizosaccharomyces pombe cdc5C gene encodes an essential protein with homology to c-Myb. EMBO J. 13: 471–483.PubMedGoogle Scholar
  73. 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: 12146–12150.PubMedGoogle Scholar
  74. Park, H., Francesconi, S. and Wang, T.S.-F. 1993. Cell cycle expression of two replicative DNA polymerase ? and ? from Schizosaccharomyces pombe. Mol. Biol. Cell 4: 145–157.PubMedGoogle Scholar
  75. Piaggio, G., Farina, A., Perrotti, D., Manni, I., Fuschi, P., Sacchi, A. and Gaetano, C. 1995. Structure and growth-dependent regulation of the human cyclin B1 promoter. Exp. Cell Res. 216: 396–402.PubMedGoogle Scholar
  76. Pines, J. and Hunter, T. 1989. Isolation of a human cyclin cDNA: evidence for cyclin mRNA and protein regulation in the cell cycle and for interaction with p34cdc2. Cell 58: 833–846.CrossRefPubMedGoogle Scholar
  77. Pines, J. and Hunter, T. 1990. p34cdc2: the S and M kinase? New Biol. 2: 389–401.PubMedGoogle Scholar
  78. Poon, P.P. and Storms, R.K. 1991. The periodically expressed TMP1 gene of Saccharomyces cerevisiae is subject to STARTdependent and START-independent regulation. J. Biol. Chem. 266: 16808–16812.PubMedGoogle Scholar
  79. Qin, L.-X., Perennes, C., Richard, L., Bouvier-Durand, M., Tréhin, C., Inzé, D. and Bergounioux, C. 1996. G2-and early-M-specific expression of the NTCYC1 cyclin gene in Nicotiana tabacum cells. Plant Mol. Biol. 32: 1093–1101.PubMedGoogle Scholar
  80. Reichheld, J.-P., Chaubet, N., Shen, W.H., Renaudin, J.-P. and Gigot, C. 1996. Multiple A-type cyclins express sequentially during the cell cycle in Nicotiana tabacum BY2 cells. Proc. Natl. Acad. Sci. USA 93: 13819–13824.PubMedGoogle Scholar
  81. 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.PubMedGoogle Scholar
  82. Renaudin, J.-P., Doonan, J.H., Freeman, D., Hashimoto, J., Hirt, H., Inzé, 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 organization. Plant Mol. Biol. 32: 1003–1018.PubMedGoogle Scholar
  83. Richardson, H.E., Lew, D.J., Henze, M., Sugimoto, K. and Reed, S.I. 1992. Cyclin-B homologs in Saccharomyces cerevisiae function in S phase and in G2. Genes Dev. 6: 2021–2034.PubMedGoogle Scholar
  84. Romero, I., Fuertes, A., Benito, M.J., Malpica, J.M., Leyva, A. and Paz-Ares, J. 1998. More than 80 R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. Plant J. 14: 273–284.PubMedGoogle Scholar
  85. Sauter, M. 1997. Differential expression of CAK (cdc2-activating kinase)-like protein kinase, cyclins and cdc2 genes from rice during the cell cycle and in response to gibberellin. Plant J. 11: 181–190.PubMedGoogle Scholar
  86. Savouré, 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 cDNA clone CycIIIMs from Medicago sativa: chromosomal mapping and expression. Plant Mol. Biol. 27: 1059–1070.PubMedGoogle Scholar
  87. Schwob, E. and Nasmyth, K. 1993. CLB5 and CLB6, a new pair of B cyclin involved in S phase and mitotic spindle formation in Saccharomyces cerevisiae. Genes Dev. 7: 1160–1175.PubMedGoogle Scholar
  88. Segers, G., Gadisseur, I., Bergounioux, C., de Almeida Engler, J., Jacqmard, A., Van Montagu, M. and Inzé, D. 1996. The Arabidopsis cyclin-dependent kinase gene cdc2bAt is preferentially expressed during S and G2 phases of the cell cycle. Plant J. 10: 601–612.PubMedGoogle Scholar
  89. Setiady, Y.Y., Sekine, M., Hariguchi, N., Yamamoto, T., Kouchi, H. and Shinmyo, A. 1995. Tobacco mitotic cyclins: cloning, characterization, gene expression and functional assay. Plant J. 8: 949–957.PubMedGoogle Scholar
  90. Sewing, A., Bürger, C., Brüsselbach, S., Schalk, C., Lucibello, F.C. and Müller, R. 1993. Human cyclin D encodes a labile nuclear protein whose synthesis is directly induced by growth factors and suppressed by cyclic AMP. J. Cell Sci. 104: 545–554.PubMedGoogle Scholar
  91. Shaul, O., Mironov, V., Burssens, S., Van Montagu, M. and Inzé, D. 1996. Two Arabidopsis cyclin promoters mediate distinctive transcriptional oscillation in synchronized tobacco BY-2 cells. Proc. Natl. Acad. Sci. USA 93: 4868–4872.CrossRefPubMedGoogle Scholar
  92. Solomon, M.J., Glotzer, M., Lee, T.H., Philipe, M. and Kirschner, M.W. 1990. Cyclin activation of p34cdc2. Cell 63: 1013–1034.PubMedGoogle Scholar
  93. 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.CrossRefPubMedGoogle Scholar
  94. Sorrell, D.A., Cambettes, B., Chaubet-Gigot, N., Gigot, C. and Murray, J.A.M. 1999. Distinct cyclin D show mitotic accumulation or constant levels of transcripts in tobacco Bright Yellow-2 cells. Plant Physiol. 119: 343–351.CrossRefPubMedGoogle Scholar
  95. Spellman, P.T., Sherlock, G., Zhang, M.Q., Iyer, V.R., Anders, K., Eisen, M.B., Brown, P.O., Botstein, D. and Futcher, B. 1998. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol. Biol. Cell 9: 3273–3297.PubMedGoogle Scholar
  96. Surana, U., Robitsch, H., Price, C., Schuster, T., Fitch, I., Futcher, B. and Nasmyth, K. 1991. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell 65: 145–161.PubMedGoogle Scholar
  97. Szarka, S., Fitch, M., Schaerer, S. and Moloney, M. 1995. Classifi-cation and expression of a family of cyclin gene homologues in Brassica napus. Plant Mol. Biol. 27: 263–275.PubMedGoogle Scholar
  98. Tassan, J.-P., Jaquenoud, M., Leopold, P., Schultz, S.J. and Nigg, E.A. 1995. Identification of human cyclin-dependent kinase 8, a putative protein kinase partner for cyclin C. Proc. Natl. Acad. Sci. USA 92: 8871–8875.PubMedGoogle Scholar
  99. Thompson, M.A. and Ramsay, R.G. 1995. Myb: an old oncoprotein with now roles. Bioessays 17: 341–350.PubMedGoogle Scholar
  100. Travali, S., Ferber, A., Reiss, K., Sell, C., Koniecki, J., Calabretta, B. and Baserga, R. 1991. Effect of the myb gene product on expression of the PCNA gene in fibroblasts. Oncogene 6: 887–894.PubMedGoogle Scholar
  101. Tréhin, C., Ahn, I.-O., Perennes, C., Couteau, F., Lalanne, E. and Bergounioux, C. 1997. Cloning of upstream sequences responsible for cell cycle regulation of the Nicotiana sylvestris Cyc1;1 gene. Plant Mol. Biol. 35: 667–672.PubMedGoogle Scholar
  102. Tréhin, C., Glab, N., Perennes, C., Planchais, S. and Bergounioux, C. 1999. M phase-specific activation of the Nicotiana sylvestris cyclin B1 promoter involves multiple regulatory elements. Plant J. 17: 263–273.Google Scholar
  103. Treisman, R. and Ammerer, G. 1992. The SRF and MCM1 transcription factors. Curr. Opin. Genet. Dev. 2: 221–226.PubMedGoogle Scholar
  104. Treisman, R. 1994. Ternary complex factors: growth factor regulated transcriptional activators. Curr. Opin. Genet. Dev. 4: 96–101.PubMedGoogle Scholar
  105. Venturelli, D., Travali, S. and Calabretta, B. 1990. Inhibition of T-cell proliferation by a MYB antisense oligomer is accompanied by selective down-regulation of DNA polymerase alpha expression. Proc. Natl. Acad. Sci. USA 87: 5963–5967.PubMedGoogle Scholar
  106. Weston, K. 1998. Myb proteins in life, death and differentiation. Curr. Opin. Genet. Dev. 8: 76–81.PubMedGoogle Scholar
  107. Yamamoto, M., Yoshida, M., Ono, K., Fujiata, T., Ohtani-Fujita, N., Sakai, T. and Nikaido, T. 1994. Effect of tumor suppressors on cell cycle-regulatory genes: RB suppresses p34cdc2 expression and normal p53 suppresses cyclin A expression. Exp. Cell Res. 210: 94–101.PubMedGoogle Scholar
  108. Zeng, X.-R., Hao, H., Jiang, Y. and Lee, M.Y.W.T. 1994. Regulation of human DNA polymerase ? during the cell cycle. J. Biol. Chem. 269: 24027–24033.PubMedGoogle Scholar
  109. Zheng, X.F. and Ruderman, J.V. 1993. Functional analysis of the P box, a domain in cyclin B required for the activation of Cdc25. Cell 75: 155–164.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Masaki Ito
    • 1
  1. 1.Department of Biological Sciences, Graduate School of ScienceUniversity of TokyoTokyoJapan

Personalised recommendations