The plant cyclin-dependent kinase inhibitor ICK1 has distinct functional domains for in vivo kinase inhibition, protein instability and nuclear localization

Plant Journal

Volumn 35, Issue 4, 2003, Pages 476-489

  Zhou, Yongming ^a   Li, Genyi ^a   Brandizzi, Federica ^b   Fowke, Larry C ^a   Wang, Hong ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

Author keywords

Arabidopsis thaliana; CDK inhibitor; Cell cycle; Inhibition domain; Protein localization; Protein stability

Indexed keywords

CELLS; FLUORESCENCE; PROTEINS;

CELL DIVISION;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CELL CYCLE PROTEINS; CYCLIN-DEPENDENT KINASE INHIBITOR PROTEINS; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; PHENOTYPE; PLANTS, GENETICALLY MODIFIED; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; STRUCTURE-ACTIVITY RELATIONSHIP;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 0042352313     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01821.x     Document Type: Article

References (62)

1. Kip1 synthesis by platelet-derived growth factor in BALB/c 3T3 cells. Mol. Cell Biol. 16, 4327-4336.
2. Bechtold, N., Ellis, J. and Pelletier, G. (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C. R. Acad. Sci. Paris Sci. la Vie/Life Sci. 316, 1194-1199.
3. Bogre, L., Zwerger, K., Meskiene, I., Binarova, P., Csizmadia, V., Planck, C., Wagner, E., Hirt, H. and Heberle-Bors, E. (1997) The cdc2Ms kinase is differently regulated in the cytoplasm and in the nucleus. Plant Physiol. 113, 841-852.
4. Carrano, A.C., Eytan, E., Hershko, A. and Pagano, M. (1999) SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat. Cell Biol. 1, 193-199.
5. Kip1 CDK 'inhibitors' are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J. 18, 1571-1583.
6. Cleary, A.L., Fowke, L.C., Wang, H. and John, P.C.L. (2002) The effect of ICK1, a plant cyclin-dependent kinase inhibitor, on mitosis in living plant cells. Plant Cell Rep. 20, 814-820.
7. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
8. cdc2 homolog of maize in root tip and stomatal complex cells: association with predicted division sites. Plant Cell, 5, 1101-1111.
9. Criqui, M.C., Parmentier, Y., Derevier, A., Shen, W.H., Dong, A. and Genschik, P. (2000) Cell cycle-dependent proteolysis and ectopic overexpression of cyclin B1 in tobacco BY2 cells. Plant J. 24, 763-773.
10. Davis, S.J. and Vierstra, R.D. (1998) Soluble, highly fluorescent variants of green fluorescent protein (GFP) for use in higher plants. Plant Mol. Biol. 36, 521-528.
11. De Veylder, L., Segers, G., Glab, N., Casteels, P., Van Montagu, M. and Inzé, D. (1997) The Arabidopsis Cks1At protein binds the cyclin-dependent kinases Cdc2aAt and Cdc2bAt. FEBS Lett. 412, 446-452.
12. De Veylder, L., Beeckman, T., Beemster, G.T., Krols, L., Terras, F., Landrieu, I., Van Der Schueren, E., Maes, S., Naudts, M. and Inzé, D. (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell, 13, 1653-1668.
13. 1 cyclin-dependent kinases in the mammalian cell cycle. Curr. Opin. Cell Biol. 12, 676-684.
14. cdc2 protein kinase. Plant Cell, 3, 531-540.
15. Fountain, M.D., Renz, A. and Beck, E. (1999) Isolation of a cDNA encoding a G1-cyclin-dependent kinase inhibitor (ICDK) from suspension cultured photoautotrophic Chenopodium rubrum L. cells. Plant Physiol. 120, 339.
16. Genschik, 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, 2063-2076.
17. 1 transition mediated by a Skp2-independent ubiquitination pathway. J. Biol. Chem. 276, 48937-48943.
18. Healy, J.M., Menges, M., Doonan, J.H. and Murray, J.A. (2001) The Arabidopsis D-type cyclins CycD2 and CycD3 both interact in vivo with the PSTAIRE cyclin-dependent kinase Cdc2a but are differentially controlled. J. Biol. Chem. 276, 7041-7047.
19. Kip1 accumulation during the cell cycle. Science, 271, 1861-1864.
20. Himanen, K., Boucheron, E., Vanneste, S., De Almeida Engler, J., Inzé, D. and Beeckman, T. (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell, 14, 2339-2351.
21. Hirayama, T., Imajuku, Y., Anai, T., Matsui, M. and Oka, A. (1991) Identification of two cell-cycle-controlling cdc2 gene homologs in Arabidopsis thaliana. Gene, 105, 159-165.
22. cdc2. Proc. Natl. Acad. Sci. USA, 88, 1636-1640.
23. Huntley, R.P. and Murray, J.A. (1999) The plant cell cycle. Curr. Opin. Plant Biol. 2, 440-446.
24. Jasinski, S., Perennes, C., Bergounioux, C. and Glab, N. (2002a) Comparative molecular and functional analyses of the tobacco cyclin-dependent kinase inhibitor NtKIS1a and its spliced variant NtKIS1b1. Plant Physiol. 130, 1871-1882.
25. Jasinski, S., Riou-Khamlichi, C., Roche, O., Perennes, C., Bergounioux, C. and Glab, N. (2002b) The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3;1-overexpressing plants. J. Cell Sci. 115, 973-982.
26. John, P.C., Sek, F.J. and Lee, M.G. (1989) A homolog of the cell cycle control protein p34cdc2 participates in the division cycle of Chlamydomonas, and a similar protein is detectable in higher plants and remote taxa, Plant Cell, 1, 1185-1193.
27. Joubes, J., Chevalier, C., Dudits, D., Heberle-Bors, E., Inzé, D., Umeda, M. and Renaudi, J.P. (2000) CDK-related protein kinases in plants. Plant Mol. Biol. 43, 607-620.
28. King, R.W., Deshaies, R.J., Peters, J.M. and Kirschner, M.W. (1996) How proteolysis drives the cell cycle. Science, 274, 1652-1659.
29. LaBaer, J., Garrett, M.D., Stevenson, L.F., Slingerland, J.M., Sandhu, C., Chou, H.S., Fattaey, A. and Harlow, E. (1997) New functional activities for the p21 family of CDK inhibitors. Genes Dev, 11, 847-862.
30. Liu, B. and Lee, Y.R.J. (2001) Kinesin-related proteins in plant cytokinesis. J. Plant Growth Regul. 20, 141-150,
31. Lui, H., Wang, H., DeLong, C., Fowke, L.C., Crosby, W.L. and Fobert, P.R. (2000) The Arabidopsis Cdc2a-interacting protein ICK2 is structurally related to ICK1 and is a potent inhibitor of cyclin-dependent kinase activity in vitro. Plant J. 21, 379-385.
32. Kip1 in G1 and S phase. Nature, 413, 323-327.
33. Meijer, M. and Murray, J.A. (2001) Cell cycle controls and the development of plant form. Curr. Opin. Plant Biol. 4, 44-49.
34. Menges, M. and Murray, J.A. (2002) Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J. 30, 203-212.
35. Mews, M., Baluska, B. and Volkmann, D. (1996) Tissue- and development-specific distribution of PSTAIRE-proteins in cells of control and wounded maize root apices. J. Exp. Bot. 47, 819-829.
36. Mews, M., Sek, F.J., Moore, R., Volkmann, D., Gunning, B.E.S. and John, P.C.L. (1997) Mitotic cyclin distribution during maize cell division: implications for the sequence diversity and function of cyclins in plants. Protoplasm, 200, 128-145.
37. Mews, M., Sek, F.J., Volkmann, D. and John, P.C.L. (2000) Immunodetection of four mitotic cyclins and the Cdc2a protein kinase in the maize root: their distribution in cell development and dedifferentiation. Protoplasm, 212, 236-249.
38. Kip1 mRNA is a mechanism contributing to accumulation during growth arrest. J. Biol. Chem. 272, 7093-7098.
39. Mironov, V., De Veylder, L., Van Montagu, M. and Inzé, D. (1999) Cyclin-dependent kinases and cell division in plants-the nexus. Plant Cell, 11, 509-522.
40. Nakagami, H., Sekine, M., Murakami, 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.
41. Nakayama, K.I., Hatakeyama, S. and Nakayama, K. (2001) Regulation of the cell cycle at the G1-Stransition by proteolysis of cyclin E and p27Kip1. Biochem. Biophys. Res. Commun. 282, 853-860.
42. Nath, U., Crawford, B.C., Carpenter, R. and Coen, E. (2003) Genetic control of surface curvature. Science, 299, 1404-1407.
43. Pines, J. (1996) Reaching for a role for the Cks proteins. Curr. Biol. 6, 1399-1402.
44. Pines, J. (1999) Four-dimensional control of the cell cycle. Nat. Cell Biol. 1, E73-E79.
45. Renaudin, J.P., Doonan, J.H., Freeman, D. et al. (1996) Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization. Plant Mol. Biol. 32, 1003-1018.
46. Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature, 382, 325-331.
47. Schnittger, A., Weinl, C., Bouyer, D., Schbobinger, U. and Hulskamp, M. (2003) Misexpression of the cyclin-dependent kinase inhibitor ICK1/KRP1 in single-celled Arabidopsis trichomes reduces endoreduplication and cell size and induces cell death. Plant Cell, 15, 303-315.
48. Kip1 expression by mitogenic and hypertrophic factors: involvement of transcriptional and post-transcriptional mechanisms. J. Cell Biol. 148, 543-556.
49. Sherr, C.J. and Roberts, J.M. (1995) Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9, 1149-1163.
50. Sherr, C.J. and Roberts, J.M. (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13, 1501-1512.
51. 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.
52. Stals, H., Bauwens, S., Traas, J., Van Montagu, M., Engler, G. and Inzé, D. (1997) Plant CDC2 is not only targeted to the pre-prophase band, but also co-localizes with the spindle, phragmoplast, and chromosomes. FEBS Lett. 418, 229-234.
53. Skp2 complex through phosphorylated Thr187 in p27. Curr. Biol. 9, 661-664.
54. Wang, H., Fowke, L.C, and Crosby, W.L. (1997) A plant cyclin-dependent kinase inhibitor gene. Nature, 386, 451-452.
55. 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.
56. Wang, H., Fowke, L.C. and Crosby, W.L. (1999) Cyclin-dependent kinase inhibitors as plant growth regulators. PCT patent application WO 99/64599.
57. Wang, H., Zhou, Y., Gilmer, S., Whitwill, S. and Fowke, L.C. (2000) Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology. Plant J. 24, 613-623.
58. Weingartner, M., Binarova, P., Drykova, D., Schweighofer, A., David, J.P., Heberle-Bors, E., Doonan, J. and Bogre, L. (2001) Dynamic recruitment of Cdc2 to specific microtubule structures during mitosis. Plant Cell, 13, 1929-1943.
59. Kip1, a cyclin-dependent kinase inhibitor. Biochem. Biophys. Res. Commun. 274, 37-42.
60. Zhou, Y., Fowke, L.C. and Wang, H. (2002a) Plant CDK inhibitors: studies of interactions with cell cycle regulators in the yeast two-hybrid system and functional comparisons in transgenic Arabidopsis plants. Plant Cell Rep. 20, 967-975.
61. Zhou, Y., Wang, H., Gilmer, S., Whitwill, S., Keller, W. and Fowke, L.C. (2002b) Control of petal and pollen development by the plant cyclin-dependent kinase inhibitor ICK1 in transgenic Brassica plants. Planta, 215, 248-257.
62. Zhou, Y., Wang, H., Gilmer, S., Whitwill, S. and Fowke, L.C. (2003) Effects of co-expressing the plant CDK inhibitor ICK1 and D-type cyclin genes on plant growth, cell size and ploidy in Arabidopsis thaliana. Planta, 216, 604-613.