Plant Molecular Biology

, Volume 43, Issue 5–6, pp 621–633 | Cite as

The role and regulation of D-type cyclins in the plant cell cycle

  • Marcel Meijer
  • James A.H. Murray


The G1 phase of the cell cycle represents a period of commitment to cell division, both for cells stimulated to resume division from a resting or quiescent state, and for cells involved in repeated cell cycles. During this period, various signals that affect the cells' ability to divide must be assessed and integrated. G1 culminates in the entry of cells into S phase, when DNA replication occurs. In addition, it is likely that several types of differentiation decision may be taken by cells in the G1 phase. In both animals and plants, it appears that D-type cyclins play an important role in the cell cycle responses to external signals, by forming the regulatory subunit of cyclin-dependent kinase complexes. The phosphorylation targets of D-cyclin kinases in mammalian cells are the retinoblastoma (Rb) protein and close relatives. Unphosphorylated Rb can associate with E2F transcription factors, preventing transcription of genes under E2F control until the G1/S boundary is reached. The conservation of Rb and E2F proteins in plants suggests that this pathway is therefore conserved in all higher eukaryotes, although it is absent in fungi and yeasts. Here we review the current understanding of the roles and regulations of D-type (CycD) cyclins in plants.

D-type cyclins differentiation G1/S control plant cell cycle proliferation retinoblastoma protein 


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  1. Ach, R.A., Durfee T., Miller, A.B., Taranto, P., Hanley-Bowdoin, L., Zambryski, P.C. and Gruissem. W. 1997a. RRB1 and RRB2 encode maize retinoblastoma-related proteins that interact with a plant D-type cyclin and geminivirus replication protein. Mol. Cell. Biol. 17: 5077–5086.PubMedGoogle Scholar
  2. Ach, R.A., Taranto, P. and Gruissem, W. 1997b. A conserved family of WD-40 proteins bind to the retinoblastoma protein in both plants and animals. Plant Cell 9: 1595–1606.PubMedGoogle Scholar
  3. Ajchenbaum, F., Ando, K., DeCaprio, J.A. and Griffin, J.D. 1993. Independent regulation of human D-type cyclin gene expression during G1 phase in primary human T-lymphocytes. J. Biol. Chem. 268: 4113–4119.PubMedGoogle Scholar
  4. Ando, K., Ajchenbaum-Cymbalista, F. and Griffin, J.D. 1993. Regulation of G1/S transition by cyclins D2 and D3 in hematopoietic cells. Proc. Natl. Acad. Sci. USA 90: 9571–9575.PubMedGoogle Scholar
  5. Baldin, V., Lukas, J., Marcote, M.J., Pagano, P. and Draetta, G. 1993. Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev. 7: 812–821.PubMedGoogle Scholar
  6. Bartkova, J., Rajpert-De Meyts, E., Skakkebaek, N.E. and Bartek, J. 1999. D-type cyclins in adult human testis and testicular cancer: relation to cell type, proliferation, differentiation, and malignancy. J. Path. 187: 573–581.PubMedGoogle Scholar
  7. Bayliss, M.W. 1985. Regulation of the cell division cycle in cultivated plant cells. In: J.A. Bryant and D. Francis (Eds.) The Cell Division Cycle in Plants, Cambridge University Press, Cambridge, UK, pp. 157–177.Google Scholar
  8. Brehm, A. and Kouzarides, T. 1999. Retinoblastoma protein meets chromatin. Trends Biochem. Sci. 24: 142–145.PubMedGoogle Scholar
  9. 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 gene cycMs4 complements G1 cyclin-deficient yeast and is induced in the G1 phase of the cell cycle. Plant Cell 7: 1847–1857.CrossRefPubMedGoogle Scholar
  10. De Veylder, L., Segers, G., Glab, N., Van Montagu, M. and Inzé, D. 1997. Identification of proteins interacting with the Arabidopsis Cdc2aAt protein. J. Exp. Bot. 48: 2113–2114.Google Scholar
  11. De Veylder, L., Van Montagu, M. and Inzé, D. 1998. Cell cycle control in Arabidopsis. In: D. Francis, D. Dudits and D. Inzé (Eds.) Plant Cell Division, Portland Press, London, pp. 1–20.Google Scholar
  12. De Veylder, L., de Almeida Engler, J., Burssens, S., Manevski, A., Lescure, B., Van Montague, 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.Google Scholar
  13. DeCaprio, J.A., Furukawa, Y., Ajchenbaum, F., Griffin, J.D. and Livingston, D.M. 1992. The retinoblastoma-susceptibility gene product becomes phosphorylated in multiple stages during cell cycle entry and progression. Proc. Natl. Acad. Sci. USA 89: 1795–1798.PubMedGoogle Scholar
  14. Doerner, P. 1999. Shoot meristem: intercellular signals keep the balance. Curr. Biol. 9: R377–R380.PubMedGoogle Scholar
  15. Doerner, P., Jorgensen, J.E., You, R., Steppuhn, J. and Lamb, C. 1996. Root growth and cyclin control. Trends Plant Sci. 1: 211–212.Google Scholar
  16. Doonan, J.H. 1998. Cell division during floral development in Antirrhinum majus. In: D. Francis, D. Dudits and D. Inzé (Eds.) Plant Cell Division, Portland Press, London, pp. 207–222.Google Scholar
  17. 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.CrossRefPubMedGoogle Scholar
  18. Dyson, N. 1998. The regulation of E2F by pRb-family proteins. Genes Dev. 12: 2245–2262.PubMedGoogle Scholar
  19. Ewen, M.E., Sluss, H.K., Sherr, C.J., Matsushime, H., Kato, J. and Livingston, D.M. 1993. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell 73: 487–497.CrossRefPubMedGoogle Scholar
  20. Fountain, M.D., Murray, J.A.H. and Beck, E. 1999. Nucleotide sequence of a cDNA encoding a cyclin D3 protein (Accession No. AJ011776) from suspension cultured photoautotrophic Chenopodium rubrum L. cells. Plant Physiol. 119: 363.PubMedGoogle Scholar
  21. Francis, D. 1998. Cell size and organ development in higher plants. In: D. Francis, D. Dudits and D. Inzé (Eds.) Plant Cell Division, Portland Press, London, pp. 187–206.Google Scholar
  22. Fuerst, R.A.U., 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
  23. Gaudin, V., Fobert, P., Lunness, T., Riou-Khamlichi, C., Murray, J.A.H., Coen, E. and Doonan, J.H. 2000. CycD cyclins are expressed in distinct proliferative zones of Antirrhinum meristems. Plant Physiol., in press.Google Scholar
  24. Genschick, P., Criqui, M.C., Parmentier, Y., Derevier, A., and Fleck, J. 1998. Cell cycle-dependent proteolysis in plants: identification of the destruction box pathway and metaphase arrest produced by the proteasome inhibitor MG132. Plant Cell 10: 2063–2075.PubMedGoogle Scholar
  25. Glotzer, M., Murray, A.W. and Kirschner, M.W. 1991. Cyclin is degraded by the ubiquitin pathway. Nature 349: 132–138.PubMedGoogle Scholar
  26. Grafi, G., Burnett, R.J., Helentjaris, T., Larkins, A.B., DeCaprio, J.A., Sellers, W.R. and Kaelin, W.G. Jr. 1996. Amaize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication. Proc. Natl. Acad. Sci. USA 93: 8962–8967.Google Scholar
  27. Gutierrez, C. 1998. The retinoblastoma pathway in plant cell cycle and development. Curr. Opin. Plant. Biol. 1: 492–497.PubMedGoogle Scholar
  28. Harper, J.W. and Elledge, S.J. 1996. Cdk inhibitors in development and cancer. Curr. Opin. Genet. Dev. 6: 56–64.PubMedGoogle Scholar
  29. Hartwell, L.H. and Weinert, T.A. 1989. Checkpoints: controls that ensure the order of cell cycle events. Science 246: 629–634.PubMedGoogle Scholar
  30. Hata, S. 1991. cDNA cloning of a novel cdc2+/cdc28-related protein kinase from rice. FEBS Lett. 279: 149–152.PubMedGoogle Scholar
  31. 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.Google Scholar
  32. Huntley, R., Healy, S., Freeman, D., Lavender, P., de Jager, S., Greenwood, J., Makker, J., Walker, E., Jackmann, M., Xie, Q., Bannister, A., Kouzarides, T., Gutierrez, C., Doonan, J.H. and Murray, J.A.H. 1998. The maize retinoblastoma protein homologue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins. Plant Mol. Biol. 37: 155–169.PubMedGoogle Scholar
  33. Inzé, D., Guterriez, C. and Chua, N.-H. 1999. Trends in plant cell cycle research. Plant Cell 11: 991–994.PubMedGoogle Scholar
  34. Jacobs, T.W. 1995. Cell cycle control. Annu. Rev. Plant Physiol. Plant Mol Biol. 46: 317–339.Google Scholar
  35. 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.PubMedGoogle Scholar
  36. John, P.C.L., Zhang, K., Dong, C., Diederich, L. and Wightman, F. 1993. p34cdc2 related proteins in control of cell cycle progression, the switch between division and differentiation in tissue development, and stimulation of division by auxin and cytokinin. Aust. J. Plant Physiol. 20: 503–526.Google Scholar
  37. Johnson, D.G. and Walker, C.L. 1999. Cyclins and cell cycle checkpoints. Annu. Rev. Pharmacol. Toxicol. 39: 295–312.PubMedGoogle Scholar
  38. Jyung, J.-C. and Sheen, J. 1997. Sugar sensing in higher plants. Trends Plant Sci. 2: 208–214.Google Scholar
  39. Kato, J., 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.PubMedGoogle Scholar
  40. 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: 11513–11517.PubMedGoogle Scholar
  41. Kitagawa, M., Higashi, H., Jung, H.K., Susuki-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: 7060–7096.PubMedGoogle Scholar
  42. Koch, K.E. 1996. Carbohydrate modulated gene expression in plants. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 47: 509–540.PubMedGoogle Scholar
  43. Laufs, P., Grandjean, O., Jonak, C., Kieu, K. and Traas, J. 1998. Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell 10: 1375–1389.PubMedGoogle Scholar
  44. Lees, E.M. 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.PubMedGoogle Scholar
  45. Lees, E. 1995. Cyclin dependent kinase regulation. Curr. Opin. Cell Biol. 7: 773–780.PubMedGoogle Scholar
  46. Lenhard, M. and Laux, T. 1999. Shoot meristem formation and maintenance. Curr. Opin. Plant. Biol. 2: 44–50.PubMedGoogle Scholar
  47. Loeffler, M. and Potten, C.S. 1996. Stem cells and cellular pedigrees. In: C.S. Potten (Ed.) Stem Cells, Academic Press, London, pp. 1–27.Google Scholar
  48. Long, J.A., Moan, E.I., Medford, J.I. and Barton, M.K. 1996. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66–69.PubMedGoogle Scholar
  49. Ludlow, J.W., Glendening, C.L., Livingston, D.M. and De-Caprio, J.A. 1993. Specific enzymatic dephosphorylation of the retinoblastoma protein. Mol. Cell. Biol. 13: 367–372.PubMedGoogle Scholar
  50. Lyndon, R.F. 1994. Control of organogenesis at the shoot apex. New Phytol. 128: 1–18.Google Scholar
  51. Lyndon, R.F. 1998. The Shoot Apical Meristem, Cambridge University Press, Cambridge, UK.Google Scholar
  52. Mateyak, M.K., Obaya, A.J. and Sedivy, J.M. 1999. c-Myc regulates cyclin D-CDK4 and-CDK6 activity but affects cell cycle progression at multiple independent points. Mol. Cell. Biol. 19: 4672–4683.PubMedGoogle Scholar
  53. Matsushime, H., Roussel, M.F., Ashmun, R.A. and Sherr, C.J. 1991. Colony-stimulated factor 1 regulates novel cyclins during the G1 phase of the cell cycle. Cell 65: 701–713.CrossRefPubMedGoogle Scholar
  54. Miao, G.-H., Hong, Z. and Verma, D.P.S. 1993. Two functional soybean genes encoding p34cdc2 protein kinases are regulated by different developmental pathways. Proc. Natl. Acad. Sci. USA 90: 943–947.PubMedGoogle Scholar
  55. Mironov, V., De Veylder, L., Van Montague, M. and Inzé, D. 1999. Cyclin-dependent kinases and cell division in plants: the nexus. Plant Cell 11: 509–521.PubMedGoogle Scholar
  56. Mittnacht, S. 1998. Control of pRB phosphorylation. Curr. Opin. Genet. Dev. 8: 21–27.PubMedGoogle Scholar
  57. Morgan, D.O. 1997. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13: 261–291.PubMedGoogle Scholar
  58. Motokura, T., Bloom, T., Kim, H.G., Juppner, H., Ruderman, J.V., Kronenberg, H.M. and Arnold, A. 1991. A novel cyclin encoded by a bcl1-linked candidate oncogene. Nature 350: 512–515.CrossRefPubMedGoogle Scholar
  59. Murashige, T. and Skoog, F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15: 473–497.Google Scholar
  60. Murray, J.A.H. 1994. The beginning of START. Plant Mol. Biol. 26: 1–3.PubMedGoogle Scholar
  61. Murray, J.A.H., Freeman, D., Greenwood, J., Huntley, R., Makkerh, J., Riou-Khamlichi, C., Sorrell, D.A., Cockcroft, C., Carmichael, J.P., Soni, R. and Shah, Z.H. 1998. Plant D cyclins and retinoblastoma (Rb) plant homologues. In: D. Francis, D. Dudits and D. Inzé (Eds.) Plant Cell Division, Portland Press, London, pp. 99–128.Google Scholar
  62. Nagata, T., Nemoto, Y. and Hasewaza, S. 1992. Tobacco BY-2 cell line as the ‘HeLa’ cell in the cell biology of higher plants. Int. Rev. Cytol. 132: 1–30.Google Scholar
  63. Nakagami, H., Sekine, M., Muraki, H. and Shinmyo, A. 1999. Tobacco retinoblastoma-related protein phosphorylated by a distinct cyclin-dependent kinase complex with Cdc2/ cyclin D in vitro. Plant J. 18: 243–252.PubMedGoogle Scholar
  64. Nasmyth, K. 1996. At the heart of the budding yeast cell cycle. Trends Genet. 12: 405–411.PubMedGoogle Scholar
  65. Nigg, E.A. 1993. Targets of cyclin-dependent protein kinases. Curr. Opin. Cell Biol. 5: 187–193.PubMedGoogle Scholar
  66. Norbury, C. and Nurse, P. 1992. Animal cell cycles and their control. Annu. Rev. Biochem. 61: 441–470.PubMedGoogle Scholar
  67. Pardee, A.B. 1989. G1 events and regulation of cell proliferation. Science 246: 603–608.PubMedGoogle Scholar
  68. Pavletich, N.P. 1999. Mechanisms of cyclin-dependent kinase regulation: structures of CDKs, their cyclin activators, and Cip and INK4 inhibitors. J. Mol. Biol. 287: 821–828.PubMedGoogle Scholar
  69. Pennell, R.I. and Lamb, C. 1997. Programmed cell death in plants. Plant Cell 9: 1157–1168.PubMedGoogle Scholar
  70. Pines, J. 1995a. Cyclins and cyclin-dependent kinases: a biochemical view. Biochem. J. 308: 697–711.PubMedGoogle Scholar
  71. Pines, J. 1995b. Cyclins and cyclin-dependent kinases: theme and variations. Adv. Cancer Res. 66: 181–212.PubMedGoogle Scholar
  72. Rechsteiner, M. and Rogers, S.W. 1996. PEST sequences and regulation by proteolysis. Trends Biochem. Sci 21: 267–271.PubMedGoogle Scholar
  73. 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 organisation. Plant Mol. Biol. 32: 1003–1018.PubMedGoogle Scholar
  74. Renaudin, J.P., Savoure, A., Philippe, H., Van Montague, M., Inzé, D. and Rouze, P. 1998. Characterisation and classification of plant cyclin sequences related to A-and B-type cyclins. In: D. Francis, D. Dudits, and D. Inzé (Eds.) Plant Cell Division, Portland Press, London, pp. 67–98.Google Scholar
  75. Renz, A., Fountain, M.D. and Beck, E. 1997. Nucleotide sequence of a cDNA encoding a D-type cyclin (accession no. Y10162) from a photoautotrophic cell suspension culture of Chenopodium rubrum (L.). Plant Physiol. 113: 1004.Google Scholar
  76. Riou-Khamlichi, C., Huntley, R., Jacqmard, A. and Murray, J.A.H. 1999. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541–1544.PubMedGoogle Scholar
  77. Rogers, S.W., Wells, R. and Rechsteiner, M. 1996. Amino acid sequences common to rapidly degrading proteins: the PEST hypothesis. Science 234: 364–368.Google Scholar
  78. Sekine, M., Ito, M., Uemukai, K., Maeda, Y., Nakagami, H. and Shinmyo, A. 1999. Isolation and characterization of the E2F-like gene in plants. FEBS Lett. 460: 117–122.PubMedGoogle Scholar
  79. Sewing, A., Burger, C., Brusselbach, S., Schalk, C., Lubicello, 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: 545–555.PubMedGoogle Scholar
  80. Sherr, C.J. 1993. Mammalian G1 cyclins. Cell 73: 1059–1065.CrossRefPubMedGoogle Scholar
  81. Sherr, C.J. 1994. G1 phase progression: cycling on cue. Cell 79: 551–555.CrossRefPubMedGoogle Scholar
  82. Sherr, C.J. 1996. Cancer cell cycles. Science 274: 1672–1677.CrossRefPubMedGoogle Scholar
  83. Shimizu, S. and Mori, H. 1998. Analysis of cycles of dormancy and growth in pea axillary buds based on mRNA accumulation patterns of cell cycle-related genes. Plant Cell Physiol. 39: 255–262.PubMedGoogle Scholar
  84. Sicinki, P., Donaher, J.D., Parker, S.B., Li, T., Fazelli, A., Gardner, H., Haslam, S.Z., Bronson, R.T., Elledge, S.J. and Weinberg, R.A. 1995. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82: 621–630.PubMedGoogle Scholar
  85. Simanis, V. and Nurse, P. 1986. The cell cycle control gene cdc2+ of fission yeast encodes a protein kinase potentially regulated by phosphorylation. Cell 45: 261–268.CrossRefPubMedGoogle Scholar
  86. Soni, R., Carmichael, J.P., Shah, Z.H. and Murray, J.A.H. 1995. A family of cyclin D homologues from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. Plant Cell 7: 85–103.CrossRefPubMedGoogle Scholar
  87. Sorrell, D.A., Combettes, B., Chaubet-Gigot, N., Gigot, C. and Murray, J.A.H. 1999. Distinct cyclin D genes show mitotic ac-cumulation or constant levels of transcripts in tobacco bright yellow-2 cells. Plant Physiol. 119: 343–351.CrossRefPubMedGoogle Scholar
  88. Taya, Y. 1997. Rb kinases and Rb-binding proteins: new points of view. Trends Biochem. Sci. 14–17.Google Scholar
  89. Traas, J., Hulskamp, M., Gendreau, E. and Hofte, H. 1998. Endoreduplication and development: rule without dividing? Curr. Opin. Plant Biol. 1: 498–503.PubMedGoogle Scholar
  90. Umeda, M., Bhalerao, R.P., Schell, J., Uchimiya, H. and Koncz, C. 1998. A distinct cyclin-dependent kinase-activating kinase of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 95: 5021–5026.PubMedGoogle Scholar
  91. Wang, H., Fowke, L.C. and Crosby, W.L. 1997. A plant cyclindependent kinase inhibitor gene. Nature 386: 451–452.CrossRefPubMedGoogle Scholar
  92. Wang, H, Qi, Q., Schorr, P., Cutler, A.J., Crosby, W.L. and Fowke, L.C. 1998. ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J. 15: 501–510.PubMedGoogle Scholar
  93. Weinberg, R.A. 1995. The retinoblastoma protein and cell cycle control. Cell 81: 323–330.CrossRefPubMedGoogle Scholar
  94. White-Cooper, H. and Glover, D.M. 1995. Regulation of the cell cycle during Drosophila development. In: C. Hutchsison and D.M. Glover (Eds.) Cell Cycle Control, IRL Press, Oxford, pp. 264–296.Google Scholar
  95. Xie, O., Suarez-Lopez, P. and Gutierrez, C. 1995. Identification and analysis of a retinoblastoma binding motif in the replication protein of a plant DNA virus: requirement for efficient viral DNA replication. EMBO J. 14: 4073–4082.PubMedGoogle Scholar
  96. Xie, O., Sanz-Burgos, A.P., Hannon, G.J. and Gutierrez, C. 1996. Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. EMBO J. 15: 4900–4908.PubMedGoogle Scholar
  97. Xiong, Y., Connolly, T., Futcher, B. and Beach, D. 1991. Human D-type cyclin. Cell 65: 691–699.CrossRefPubMedGoogle Scholar
  98. Zarkowska, T., Harlow, E. and Mittnacht, S. 1997. Monoclonal antibodies specific for underphosphorylated retinoblastoma protein identify a cell cycle regulated phosphorylation site targeted by CDKs. Oncogene 14: 249–254.PubMedGoogle Scholar
  99. Zwijssen, R.M.L., Klompmaker, R., Wientjens, E.B.H.G.M, Kristel, P.M.P., van der Burg, B. and Michalides, R.J.A.M. 1996. Cyclin D1 triggers autonomous growth of breast cancer cells by governing cell cycle exit. Mol. Cell. Biol. 16: 2554–2560.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Marcel Meijer
    • 1
  • James A.H. Murray
    • 1
  1. 1.Institute of BiotechnologyUniversity of CambridgeCambridgeUK

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