The C. elegans Tousled-like Kinase (TLK-1) Has an Essential Role in Transcription

Current Biology

Volumn 13, Issue 22, 2003, Pages 1921-1929

  Han, Zhenbo ^a   Saam, Jennifer R ^b   Adams, Henry P ^a   Mango, Susan E ^b   Schumacher, Jill M ^a,c  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; CAENORHABDITIS; CAENORHABDITIS ELEGANS; EUKARYOTA; INVERTEBRATA; METAZOA; SACCHAROMYCETALES;

EID: 0242540366     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2003.10.035     Document Type: Article

References (49)

1. Komarnitsky, P., Cho, E.J., and Buratowski, S. (2000). Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14, 2452-2460.
2. Kobor, M.S., and Greenblatt, J. (2002). Regulation of transcription elongation by phosphorylation. Biochim. Biophys. Acta 1577, 261-275.
3. McCracken, S., Fong, N., Rosonina, E., Yankulov, K., Brothers, G., Siderovski, D., Hessel, A., Foster, S., Shuman, S., and Bentley, D.L. (1997). 5′-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev. 11, 3306-3318.
4. Licatalosi, D.D., Geiger, G., Minet, M., Schroeder, S., Cilli, K., McNeil, J.B., and Bentley, D.L. (2002). Functional interaction of yeast pre-mRNA 3′ end processing factors with RNA polymerase II. Mol. Cell 9, 1101-1111.
5. Oelgeschlager, T. (2002). Regulation of RNA polymerase II activity by CTD phosphorylation and cell cycle control. J. Cell. Physiol. 190, 160-169.
6. Nigg, E.A. (1996). Cyclin-dependent kinase 7: at the cross-roads of transcription, DNA repair and cell cycle control? Curr. Opin. Cell Biol. 8, 312-317.
7. Larochelle, S., Chen, J., Knights, R., Pandur, J., Morcillo, P., Erdjument-Bromage, H., Tempst, P., Suter, B., and Fisher, R.P. (2001). T-loop phosphorylation stabilizes the CDK7-cyclin H-MAT1 complex in vivo and regulates its CTD kinase activity. EMBO J. 20, 3749-3759.
8. Wallenfang, M.R., and 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.
9. Price, D.H. (2000). P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase II. Mol. Cell. Biol. 20, 2629-2634.
10. Shim, E.Y., Walker, A.K., Shi, Y., and Blackwell, T.K. (2002). CDK-9/cyclin T (P-TEFb) is required in two postinitiation pathways for transcription in the C. elegans embryo. Genes Dev. 16, 2135-2146.
11. Seydoux, G., and Dunn, M.A. (1997). Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster. Development 124, 2191-2201.
12. Roe, J.L., Rivin, C.J., Sessions, R.A., Feldmann, K.A., and Zambryski, P.C. (1993). The Tousled gene in A. thaliana encodes a protein kinase homolog that is required for leaf and flower development. Cell 75, 939-950.
13. Sillje, H.H., Takahashi, K., Tanaka, K., Van Houwe, G., and Nigg, E.A. (1999). Mammalian homologues of the plant Tousled gene code for cell-cycle-regulated kinases with maximal activities linked to ongoing DNA replication. EMBO J. 18, 5691-5702.
14. Sillje, H.H., and Nigg, E.A. (2001). Identification of human Asf1 chromatin assembly factors as substrates of Tousled-like kinases. Curr. Biol. 11, 1068-1073.
15. Li, Y., DeFatta, R., Anthony, C., Sunavala, G., and De Benedetti, A. (2001). A translationally regulated Tousled kinase phosphorylates histone H3 and confers radioresistance when overexpressed. Oncogene 20, 726-738.
16. Groth, A., Lukas, J., Nigg, E.A., Sillje, H.H., Wernstedt, C., Bartek, J., and Hansen, K. (2003). Human Tousled like kinases are targeted by an ATM-and Chk1-dependent DNA damage checkpoint. EMBO J. 22, 1676-1687.
17. Krause, M., and Hirsh, D. (1987). A trans-spliced leader sequence on actin mRNA in C. elegans. Cell 49, 753-761.
18. Hsu, J.Y., Sun, Z.W., Li, X., Reuben, M., Tatchell, K., Bishop, D.K., Grushcow, J.M., Brame, C.J., Caldwell, J.A., Hunt, D.F., et al. (2000). Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102, 279-291.
19. Giet, R., and Glover, D.M. (2001). Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol. 152, 669-682.
20. Murnion, M.E., Adams, R.R., Callister, D.M., Allis, C.D., Earnshaw, W.C., and Swedlow, J.R. (2001). Chromatin-associated protein phosphatase 1 regulates aurora-B and histone H3 phosphorylation. J. Biol. Chem. 276, 26656-26665.
21. Crosio, C., Fimia, G.M., Loury, R., Kimura, M., Okano, Y., Zhou, H., Sen, S., Allis, C.D., and Sassone-Corsi, P. (2002). Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol. Cell. Biol. 22, 874-885.
22. Hayes, J.J., and Lee, K.M. (1997). In vitro reconstitution and analysis of mononucleosomes containing defined DNAs and proteins. Methods 12, 2-9.
23. Luger, K., Rechsteiner, T.J., and Richmond, T.J. (1999). Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 304, 3-19.
24. Timmons, L., and Fire, A. (1998). Specific interference by ingested dsRNA. Nature 395, 854.
25. Newman-Smith, E.D., and Rothman, J.H. (1998). The maternal-to-zygotic transition in embryonic patterning of Caenorhabditis elegans. Curr. Opin. Genet. Dev. 8, 472-480.
26. Powell-Coffman, J.A., Knight, J., and Wood, W.B. (1996). Onset of C. elegans gastrulation is blocked by inhibition of embryonic transcription with an RNA polymerase antisense RNA. Dev. Biol. 178, 472-483.
27. Bird, D.M., and Riddle, D.L. (1989). Molecular cloning and sequencing of ama-1, the gene encoding the largest subunit of Caenorhabditis elegans RNA polymerase II. Mol. Cell. Biol. 9, 4119-4130.
28. Maduro, M.F., Meneghini, M.D., Bowerman, B., Broitman-Maduro, G., and Rothman, J.H. (2001). Restriction of mesendoderm to a single blastomere by the combined action of SKN-1 and a GSK-3beta homolog is mediated by MED-1 and -2 in C. elegans. Mol. Cell 7, 475-485.
29. Maduro, M.F., Lin, R., and Rothman, J.H. (2002). Dynamics of a developmental switch: recursive intracellular and intranuclear redistribution of Caenorhabditis elegans POP-1 parallels Wnt-inhibited transcriptional repression. Dev. Biol. 248, 128-142.
30. Fukushige, T., Hendzel, M.J., Bazett-Jones, D.P., and McGhee, J.D. (1999). Direct visualization of the elt-2 gut-specific GATA factor binding to a target promoter inside the living Caenorhabditis elegans embryo. Proc. Natl. Acad. Sci. USA 96, 11883-11888.
31. Schumacher, J.M., Ashcroft, N., Donovan, P.J., and Golden, A. (1998). A highly conserved centrosomal kinase, AIR-1, is required for accurate cell cycle progression and segregation of developmental factors in Caenorhabditis elegans embryos. Development 125, 4391-4402.
32. Lachner, M., and Jenuwein, T. (2002). The many faces of histone lysine methylation. Curr. Opin. Cell Biol. 14, 286-298.
33. Bernstein, B.E., Humphrey, E.L., Erlich, R.L., Schneider, R., Bouman, P., Liu, J.S., Kouzarides, T., and Schreiber, S.L. (2002). Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl. Acad. Sci. USA 99, 8695-8700.
34. Santos-Rosa, H., Schneider, R., Bannister, A.J., Sherriff, J., Bernstein, B.E., Emre, N.C., Schreiber, S.L., Mellor, J., and Kouzarides, T. (2002). Active genes are tri-methylated at K4 of histone H3. Nature 419, 407-411.
35. Nakayama, J., Rice, J.C., Strahl, B.D., Allis, C.D., and Grewal, S.I. (2001). Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292, 110-113.
36. Schreiber, S.L., and Bernstein, B.E. (2002). Signaling network model of chromatin. Cell 111, 771-778.
37. Li, B., Howe, L., Anderson, S., Yates, J.R., 3rd, and Workman, J.L. (2003). The Set2 Histone Methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 278, 8897-8903.
38. Li, J., Moazed, D., and Gygi, S.P. (2002). Association of the histone methyltransferase Set2 with RNA polymerase II plays a role in transcription elongation. J. Biol. Chem. 277, 49383-49388.
39. Krogan, N.J., Kim, M., Tong, A., Golshani, A., Cagney, G., Canadien, V., Richards, D.P., Beattie, B.K., Emili, A., Boone, C., et al. (2003). Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 23, 4207-4218.
40. Fong, N., and Bentley, D.L. (2001). Capping, splicing, and 3′ processing are independently stimulated by RNA polymerase II: different functions for different segments of the CTD. Genes Dev. 15, 1783-1795.
41. Orphanides, G., and Reinberg, D. (2002). A unified theory of gene expression. Cell 108, 439-451.
42. Marshall, N.F., Peng, J., Xie, Z., and Price, D.H. (1996). Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J. Biol. Chem. 271, 27176-27183.
43. Kobor, M.S., Archambault, J., Lester, W., Holstege, F.C., Gileadi, O., Jansma, D.B., Jennings, E.G., Kouyoumdjian, F., Davidson, A.R., Young, R.A., et al. (1999). An unusual eukaryotic protein phosphatase required for transcription by RNA polymerase II and CTD dephosphorylation in S. cerevisiae. Mol. Cell 4, 55-62.
44. Xiao, T., Hall, H., Kizer, K.O., Shibata, Y., Hall, M.C., Borchers, C.H., and Strahl, B.D. (2003). Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev. 17, 654-663.
45. Tyler, J.K., Adams, C.R., Chen, S.R., Kobayashi, R., Kamakaka, R.T., and Kadonaga, J.T. (1999). The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402, 555-560.
46. Tyler, J.K., Collins, K.A., Prasad-Sinha, J., Amiott, E., Bulger, M., Harte, P.J., Kobayashi, R., and Kadonaga, J.T. (2001). Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol. Cell. Biol. 21, 6574-6584.
47. Mello, J.A., Sillje, H.H., Roche, D.M., Kirschner, D.B., Nigg, E.A., and Almouzni, G. (2002). Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep. 3, 329-334.
48. Sutton, A., Bucaria, J., Osley, M.A., and Sternglanz, R. (2001). Yeast ASF1 protein is required for cell cycle regulation of histone gene transcription. Genetics 158, 587-596.
49. Saunders, A., Werner, J., Andrulis, E.D., Nakayama, T., Hirose, S., Reinberg, D., and Lis, J.T. (2003). Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 301, 1094-1096.