The Arabidopsis cyclin-dependent kinase-activating kinase CDKF;1 is a major regulator of cell proliferation and cell expansion but is dispensable for CDKA activation

Plant Journal

Volumn 59, Issue 3, 2009, Pages 475-487

  Takatsuka, Hirotomo ^a   Ohno, Ryoko ^b   Umeda, Masaaki ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b Research Institute for Biological Science OKAYAMA   (Japan)

Author keywords

CDK activating kinase; Cell cycle; Cyclin dependent kinase; Protein phosphorylation; Protein stability; Transcription

Indexed keywords

ARABIDOPSIS PROTEIN; CAK1AT PROTEIN, ARABIDOPSIS; CDKA1 PROTEIN, ARABIDOPSIS; CDKD;2 PROTEIN, ARABIDOPSIS; CYCLIN DEPENDENT KINASE; PLANT RNA; PROTEIN SERINE THREONINE KINASE;

ARABIDOPSIS; ARTICLE; CELL DIVISION; CELL ENLARGEMENT; CELL PROLIFERATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOSPHORYLATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DIVISION; CELL ENLARGEMENT; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASES; GENE EXPRESSION REGULATION, PLANT; GENE KNOCKOUT TECHNIQUES; MUTAGENESIS, INSERTIONAL; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA, PLANT;

ARABIDOPSIS; VERTEBRATA;

EID: 67651230832     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.03884.x     Document Type: Article

References (65)

1. Aleem, E., Kiyokawa, H. Kaldis, P. (2005) Cdc2-cyclin E complexes regulate the G1/S phase transition. Nat. Cell Biol., 7, 831 836.
2. Andersen, S.U., Buechel, S., Zhao, Z., Ljung, K., Novák, O., Busch, W., Schuster, C. Lohmann, J.U. (2008) Requirement of B2-type cyclin-dependent kinases for meristem integrity in Arabidopsis thaliana. Plant Cell, 20, 88 100.
3. Boudolf, V., Barrôco, R., de Almeida Engler, J., Verkest, A., Beeckman, T., Naudt, M., Inzé, D. De Veylder, L. (2004a) B1-type cyclin-dependent kinases are essential for the formation of stomatal complexes in Arabidopsis thaliana. Plant Cell, 16, 945 955.
4. Boudolf, V., Vlieghe, K., Beemster, G.T., Magyar, Z., Torres Acosta, J.A., Maes, S., Van Der Schueren, E., Inzé, D. De Veylder, L. (2004b) The plant-specific cyclin-dependent kinase CDKB1;1 and transcription factor E2FA-DPA control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. Plant Cell, 16, 2683 2692.
5. Buck, V., Russell, P. Millar, J.B. (1995) Identification of a cdk-activating kinase in fission yeast. EMBO J., 14, 6173 6183.
6. Chao, W.S., Serpe, M.D., Jia, Y., Shelver, W.L., Anderson, J.V. Umeda, M. (2007) Potential roles for autophosphorylation, kinase activity, and abundance of a CDK-activating kinase (Ee;CDKF;1) during growth in leafy spurge. Plant Mol. Biol., 63, 365 379.
7. Ciemerych, M., Kenney, A., Sicinska, E., Kalaszczynska, I., Bronson, R., Rowitch, D., Gardner, H. Sicinski, P. (2002) Development of mice expressing a single D-type cyclin. Genes Dev., 16, 3277 3289.
8. Cismowski, M.J., Laff, G.M., Solomon, M.J. Reed, S.I. (1995) KIN28 encodes a C-terminal domain kinase that controls mRNA transcription in Saccharomyces cerevisiae but lacks Cyclin-dependent kinase-activating kinase (CAK) activity. Mol. Cell. Biol., 15, 2983 2992.
9. Cui, X., Fan, B., Scholz, J. Chen, Z. (2007) Roles of Arabidopsis cyclin-dependent kinase C complexes in cauliflower mosaic virus infection, plant growth and development. Plant Cell, 19, 1388 1402.
10. Damagnez, V., Mäkelä, T.P. Cottarel, G. (1995) Schizosaccharomyces pombe Mop1-Mcs2 is related to mammalian CAK. EMBO J., 14, 6164 6172.
11. De Schutter, K., Joubès, J., Cools, T. et al. (2007) Arabidopsis WEE1 kinase controls cell cycle arrest in response to activation of the DNA integrity checkpoint. Plant Cell, 19, 211 225.
12. De Veylder, L., Beeckman, T., Beemster, G.T., Krols, L., Terras, F., Landrieu, I., van der Schueren, E., Maes, S., Naudts, M. Inzé, D. (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell, 13, 1653 1668.
13. Devault, A., Martinez, A.M., Fesquet, D., Labbe, J.C., Morin, N., Tassan, J.P., Nigg, E.A., Cavadore, J.C. Doree, M. (1995) MAT1 ('menage a trois') a new RING finger protein subunit stabilizing cyclin H-cdk7 complexes in starfish and Xenopus CAK. EMBO J., 14, 5027 5036.
14. Di Laurenzio, L., Wysockadiller, J., Malamy, J.E., Pysh, L., Helariutta, Y., Freshour, G., Hahn, M.G., Feldmann, K.A. Benfey, P.N. (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell, 86, 423 433.
15. Dissmeyer, N., Nowack, M.K., Pusch, S., Stals, H., Inzé, D., Grini, P.E. Schnittger, A. (2007) T-loop phosphorylation of Arabidopsis CDKA;1 is required for its function and can be partially substituted by an aspartate residue. Plant Cell, 19, 972 985.
16. Espinoza, F.H., Farrell, A., Erdjument-Bromage, H., Tempst, P. Morgan, D.O. (1996) A cyclin-dependent kinase-activating kinase (CAK) in budding yeast unrelated to vertebrate CAK. Science, 273, 1714 1717.
17. Espinoza, F.H., Farrell, A., Nourse, J.L., Chamberlin, H.M., Gileadi, O. Morgan, D.O. (1998) Cak1 is required for Kin28 phosphorylation and activation in vivo. Mol. Cell. Biol., 18, 6365 6373.
18. wee1 mitotic inhibitor is a tyrosine/serine kinase. Nature, 349, 808 811.
19. Fisher, R.P. Morgan, D.O. (1994) A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase. Cell, 78, 713 724.
20. Fisher, R.P., Jin, P., Chamberlin, H.M. Morgan, D.O. (1995) Alternative mechanisms of CAK assembly require an assembly factor or an activating kinase. Cell, 83, 47 57.
21. Fülöp, K., Pettkó-Szandtner, A., Magyar, Z., Miskolczi, P., Kondorosi, E., Dudits, D. Bakó, L. (2005) The Medicago CDKC;1-CYCLINT;1 kinase complex phosphorylates the carboxy-terminal domain of RNA polymerase II and promotes transcription. Plant J., 42, 810 820.
22. Hemerly, A.S., Ferreira, P., de Almeida Engler, J., Van Montagu, M., Engler, G. Inzé, D. (1993) cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell, 5, 1711 1723.
23. Hemerly, A.S., de Almeida Engler, J., Bergounioux, C., Van Montagu, M., Engler, G., Inzé, D. Ferreira, P. (1995) Dominant negative mutants of the Cdc2 kinase uncouple cell division from iterative plant development. EMBO J., 14, 3925 3936.
24. Hemerly, A.S., Ferreira, P.C.G., Van Montagu, M., Engler, G. Inzé, D. (2000) Cell division events are essential for embryo patterning and morphogenesis: studies on dominant-negative cdc2aAt mutants of Arabidopsis. Plant J., 23, 123 130.
25. Hermand, D., Pihlak, A., Westerling, T., Damagnez, V., Vandenhaute, J., Cottarel, G. Mäkelä, T.P. (1998) Fission yeast Csk1 is a CAK-activating kinase (CAKAK). EMBO J., 17, 7230 7238.
26. Hermand, D., Westerling, T., Pihlak, A., Thuret, J.-Y., Vallenius, T., Tiainen, M., Vandenhaute, J., Cottarel, G., Mann, C. Mäkelä, T.P. (2001) Specificity of Cdk activation in vivo by the two Caks Mcs6 and Csk1 in fission yeast. EMBO J., 20, 82 90.
27. Iwakawa, H., Shinmyo, A. Sekine, M. (2006) Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J., 45, 819 831.
28. Joubès, J., Lemaire-Chamley, M., Delmas, F., Walter, J., Hernould, M., Mouras, A., Raymond, P. Chevalier, C. (2001) A new C-type cyclin-dependent kinase from tomato expressed in dividing tissues does not interact with mitotic and G1 cyclins. Plant Physiol., 126, 1403 1415.
29. Kaldis, P., Sutton, A. Solomon, M.J. (1996) The Cdk-activating kinase (CAK) from budding yeast. Cell, 86, 553 564.
30. Kimmelman, J., Kaldis, P., Hengartner, C.J., Laff, G.M., Koh, S.S., Young, R.A. Solomon, M.J. (1999) Activating phosphorylation of the Kin28p subunit of yeast TFIIH by Cak1p. Mol. Cell. Biol., 19, 4774 4787.
31. Koncz, C., Mayerhofer, R., Koncz-Kalman, Z., Nawrath, C., Reiss, B., Redei, G.P. Schell, J. (1990) Isolation of a gene encoding a novel chloroplast protein by T-DNA tagging in Arabidopsis thaliana. EMBO J., 9, 1337 1346.
32. Kono, A., Umeda-Hara, C., Lee, J., Ito, M., Uchimiya, H. Umeda, M. (2003) Arabidopsis D-type cyclin CYCD4;1 is a novel cyclin partner of B2-type cyclin-dependent kinase. Plant Physiol., 132, 1315 1321.
33. Kono, A., Ohno, R., Umeda-Hara, C., Uchimiya, H. Umeda, M. (2006) A distinct type of cyclin D, CYCD4;2, involved in the activation of cell division in Arabidopsis. Plant Cell Rep., 25, 540 545.
34. Labbé, J.C., Martinez, A.M., Fesquet, D., Capony, J.P., Darbon, J.M., Derancourt, J., Devault, A., Morin, N., Cavadore, J.C. Dorée, M. (1994) p40MO15 associates with a p36 subunit and requires both nuclear translocation and Thr176 phosphorylation to generate cdk-activating kinase activity in Xenopus oocytes. EMBO J., 13, 5155 5164.
35. Larochelle, S., Pandur, J., Fisher, R., Salz, H. Suter, B. (1998) Cdk7 is essential for mitosis and for in vivo Cdk-activating kinase activity. Genes Dev., 12, 370 381.
36. Leclerc, V., Raisin, S. Léopold, P. (2000) Dominant-negative mutants reveal a role for the Cdk7 kinase at the mid-blastula transition in Drosophila embryos. EMBO J., 19, 1567 1575.
37. Magyar, Z., Mészáros, T., Miskolczi, P. et al. (1997) Cell cycle phase specificity of putative cyclin-dependent kinase variants in synchronized alfalfa cells. Plant Cell, 9, 223 235.
38. Mäkelä, T.P., Tassan, J.P., Nigg, E.A., Frutiger, S., Hughes, G.J. Weinberg, R.A. (1994) A cyclin associated with the CDK-activating kinase MO15. Nature, 371, 254 257.
39. Malamy, J.E. Benfey, P.N. (1997) Analysis of SCARECROW expression using a rapid system for assessing transgene expression in Arabidopsis roots. Plant J., 12, 957 963.
40. Menges, M. Murray, J.A. (2002) Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J., 30, 203 212.
41. Menges, M., de Jager, S.M., Gruissem, W. Murray, J.A. (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J., 41, 546 566.
42. Mészáros, T., Miskolczi, P., Ayaydin, F., Pettkó-Szandtner, A., Peres, A., Magyar, Z., Horváth, G.V., Bakó, L., Fehér, A. Dudits, D. (2000) Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells. Plant Mol. Biol., 43, 595 605.
43. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T. Kimura, T. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng., 104, 34 41.
44. Nowack, M.K., Grini, P.E., Jakoby, M.J., Lafos, M., Koncz, C. Schnittger, A. (2006) A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat. Genet., 38, 63 67.
45. Ostapenko, D. Solomon, M.J. (2005) Phosphorylation by Cak1 regulates the C-terminal domain kinase Ctk1 in Saccharomyces cerevisiae. Mol. Cell. Biol., 25, 3906 3913.
46. Parker, L.L. Piwnica-Worms, H. (1992) Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science, 257, 1955 1957.
47. Porceddu, A., Stals, H., Reichheld, J.P., Segers, G., De Veylder, L., De Pinho Barrôco, R., Casteels, P., Van Montagu, M., Inzé, D. Mironov, V. (2001) A plant-specific cyclin-dependent kinase is involved in the control of G2/M progression in plants. J. Biol. Chem., 276, 36354 36360.
48. Rossi, D.J., Londesborough, A., Korsisaari, N., Pihlak, A., Lehtonen, E., Henkemeyer, M. Mäkelä, T.P. (2001) Inability to enter S phase and defective RNA polymerase II CTD phosphorylation in mice lacking Mat1. EMBO J., 20, 2844 2856.
49. Saiz, J.E. Fisher, R.P. (2002) A CDK-activating kinase network is required in cell cycle control and transcription in fission yeast. Curr. Biol., 12, 1100 1105.
50. Serizawa, H., Mäkelä, T.P., Conaway, J.W., Conaway, R.C., Weinberg, R.A. Young, R.A. (1995) Association of Cdk-activating kinase subunits with transcription factor TFIIH. Nature, 374, 280 282.
51. Shiekhattar, R., Mermelstein, F., Fisher, R.P., Drapkin, R., Dynlacht, B., Wessling, H.C., Morgan, D.O. Reinberg, D. (1995) Cdk-activating kinase complex is a component of human transcription factor TFIIH. Nature, 374, 283 287.
52. Shimotohno, A., Matsubayashi, S., Yamaguchi, M., Uchimiya, H. Umeda, M. (2003) Differential phosphorylation activities of CDK-activating kinases in Arabidopsis thaliana. FEBS Lett., 534, 69 74.
53. Shimotohno, A., Umeda-Hara, C., Bisova, K., Uchimiya, H. Umeda, M. (2004) The plant-specific kinase CDKF;1 is involved in activating phosphorylation of cyclin-dependent kinase-activating kinases in Arabidopsis. Plant Cell, 16, 2954 2966.
54. Shimotohno, A., Ohno, R., Bisova, K., Sakaguchi, N., Huang, J., Koncz, C., Uchimiya, H. Umeda, M. (2006) Diverse phosphoregulatory mechanisms controlling cyclin-dependent kinase-activating kinases in Arabidopsis. Plant J., 47, 701 710.
55. Tassan, J.P., Jaquenoud, M., Fry, A.M., Frutiger, S., Hughes, G.J. Nigg, E.A. (1995) In vitro assembly of a functional human CDK7-cyclin H complex requires MAT1, a novel 36 kDa RING finger protein. EMBO J., 14, 5608 5617.
56. Thuret, J.-Y., Valay, J.-G., Faye, G. Mann, C. (1996) Civ1 (CAK in vivo), a novel Cdk-activating kinase. Cell, 86, 565 576.
57. Umeda, M., Bhalerao, R.P., Schell, J., Uchimiya, H. Koncz, C. (1998) A distinct cyclin-dependent kinase-activating kinase of Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 95, 5021 5026.
58. Umeda, M., Umeda-Hara, C. Uchimiya, H. (2000) A cyclin-dependent kinase-activating kinase regulates differentiation of root initial cells in Arabidopsis. Proc. Natl Acad. Sci. USA, 97, 13396 13400.
59. Umeda, M., Shimotohno, A. Yamaguchi, M. (2005) Control of cell division and transcription by cyclin-dependent kinase-activating kinases in plants. Plant Cell Physiol, 46, 1437 1442.
60. Valay, J.G., Simon, M., Dubois, M.F., Bensaude, O., Facca, C. Faye, G. (1995) The KIN28 gene is required both for RNA polymerase II mediated transcription and phosphorylation of the Rpb1p CTD. J. Mol. Biol., 249, 535 544.
61. Vandepoele, K., Raes, J., De Veylder, L., Rouzé, P., Rombauts, S. Inzé, D. (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell, 14, 903 916.
62. Wallenfang, M.R. Seydoux, G. (2002) cdk-7 Is required for mRNA transcription and cell cycle progression in Caenorhabditis elegans embryos. Proc. Natl Acad. Sci. USA, 99, 5527 5532.
63. Wang, W. Chen, X. (2004) HUA ENHANCER3 reveals a role for a cyclin-dependent protein kinase in the specification of floral organ identity in Arabidopsis. Development 131, 3147 3156.
64. Yamaguchi, M., Umeda, M. Uchimiya, H. (1998) A rice homolog of Cdk7/MO15 phosphorylates both cyclin-dependent protein kinases and the carboxy-terminal domain of RNA polymerase II. Plant J., 16, 613 619.
65. Yao, S. Prelich, G. (2002) Activation of the bur1-bur2 cyclin-dependent kinase complex by cak1. Mol. Cell. Biol., 22, 6750 6758.