CDK8 is a positive regulator of transcriptional elongation within the serum response network

Nature Structural and Molecular Biology

Volumn 17, Issue 2, 2010, Pages 194-201

  Donner, Aaron J ^a   Ebmeier, Christopher C ^a   Taatjes, Dylan J ^a   Espinosa, Joaquín M ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 8; EARLY GROWTH RESPONSE FACTOR; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; RNA POLYMERASE II; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; SERUM RESPONSIVE ELEMENT; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE 8; GENE KNOCKDOWN TECHNIQUES; HUMANS; NUCLEAR PROTEINS; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RNA POLYMERASE II; SERUM RESPONSE ELEMENT; SERUM RESPONSE FACTOR; TRANS-ACTIVATORS; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 76349090199     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1752     Document Type: Article

References (60)

1. Taatjes, D.J., Marr, M.T. & Tjian, R. Regulatory diversity among metazoan co-activator complexes. Nat. Rev. Mol. Cell Biol. 5, 403-410 (2004).
2. Kim, Y.J., Bjorklund, S., Li, Y., Sayre, M.H. & Kornberg, R.D. A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II. Cell 77, 599-608 (1994).
3. Cantin, G.T., Stevens, J.L. & Berk, A.J. Activation domain-mediator interactions promote transcription preinitiation complex assembly on promoter DNA. Proc. Natl. Acad. Sci. USA 100, 12003-12008 (2003).
4. Li, X.Y., Virbasius, A., Zhu, X. & Green, M.R. Enhancement of TBP binding by activators and general transcription factors. Nature 399, 605-609 (1999).
5. Kuras, L. & Struhl, K. Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme. Nature 399, 609-613 (1999).
6. Guenther, M.G., Levine, S.S., Boyer, L.A., Jaenisch, R. & Young, R.A. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88 (2007).
7. O'Brien, T. & Lis, J.T. RNA polymerase II pauses at the 5′ end of the transcriptionally induced Drosophila hsp70 gene. Mol. Cell. Biol. 11, 5285-5290 (1991).
8. Espinosa, J.M., Verdun, R.E. & Emerson, B.M. p53 functions through stress-and promoter-specifc recruitment of transcription initiation components before and after DNA damage. Mol. Cell 12, 1015-1027 (2003).
9. Zeitlinger, J., et al. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat. Genet. 39, 1512-1516 (2007).
10. Chao, S.H. & Price, D.H. Flavopiridol inactivates P-TEFb and blocks most RNA polymerase II transcription in vivo. J. Biol. Chem. 276, 31793-31799 (2001).
11. Eberhardy, S.R. & Farnham, P.J. Myc recruits P-TEFb to mediate the fnal step in the transcriptional activation of the cad promoter. J. Biol. Chem. 277, 40156-40162 (2002).
12. Zhu, Y., et al. Transcription elongation factor P-TEFb is required for HIV-1 tat transactivation in vitro. Genes Dev. 11, 2622-2632 (1997).
13. Yang, Z., et al. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol. Cell 19, 535-545 (2005).
14. Kim, Y.K., Bourgeois, C.F., Isel, C., Churcher, M.J. & Karn, J. Phosphorylation of the RNA polymerase II carboxyl-terminal domain by CDK9 is directly responsible for human immunodefciency virus type 1 Tat-activated transcriptional elongation. Mol. Cell. Biol. 22, 4622-4637 (2002).
15. Marshall, N.F., Peng, J., Xie, Z. & Price, D.H. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J. Biol. Chem. 271, 27176-27183 (1996).
16. Cho, E.J., Kobor, M.S., Kim, M., Greenblatt, J. & Buratowski, S. Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser 2 of the RNA polymerase II C-terminal domain. Genes Dev. 15, 3319-3329 (2001).
17. Price, D.H. P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase II. Mol. Cell. Biol. 20, 2629-2634 (2000).
18. Komarnitsky, P., Cho, E.J. & Buratowski, S. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14, 2452-2460 (2000).
19. Kim, M., Ahn, S.H., Krogan, N.J., Greenblatt, J.F. & Buratowski, S. Transitions in RNA polymerase II elongation complexes at the 3′ ends of genes. EMBO J. 23, 354-364 (2004).
20. Ahn, S.H., Kim, M. & Buratowski, S. Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3′ end processing. Mol. Cell 13, 67-76 (2004).
21. McCracken, S., et al. 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 (1997).
22. Ho, C.K. & Shuman, S. Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian mRNA capping enzyme. Mol. Cell 3, 405-411 (1999).
23. Rickert, P., Corden, J.L. & Lees, E. Cyclin C/CDK8 and cyclin H/CDK7/p36 are biochemically distinct CTD kinases. Oncogene 18, 1093-1102 (1999).
24. Akhtar, M.S., et al. TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II. Mol. Cell 34, 387-393 (2009).
25. Ramanathan, Y., et al. Three RNA polymerase II carboxyl-terminal domain kinases display distinct substrate preferences. J. Biol. Chem. 276, 10913-10920 (2001).
26. Wang, G., et al. Mediator requirement for both recruitment and postrecruitment steps in transcription initiation. Mol. Cell 17, 683-694 (2005).
27. Donner, A.J., Szostek, S., Hoover, J.M. & Espinosa, J.M. CDK8 is a stimulus-specifc positive coregulator of p53 target genes. Mol. Cell 27, 121-133 (2007).
28. Sato, S., et al. A set of consensus mammalian mediator subunits identifed by multidimensional protein identifcation technology. Mol. Cell 14, 685-691 (2004).
29. Knuesel, M.T., Meyer, K.D., Bernecky, C. & Taatjes, D.J. The human CDK8 subcomplex is a molecular switch that controls Mediator coactivator function. Genes Dev. 23, 439-451 (2009).
30. Elmlund, H., et al. The cyclin-dependent kinase 8 module sterically blocks Mediator interactions with RNA polymerase II. Proc. Natl. Acad. Sci. USA 103, 15788-15793 (2006).
31. Mo, X., Kowenz-Leutz, E., Xu, H. & Leutz, A. Ras induces mediator complex exchange on C/EBP beta. Mol. Cell 13, 241-250 (2004).
32. Pavri, R., et al. PARP-1 determines specifcity in a retinoid signaling pathway via direct modulation of mediator. Mol. Cell 18, 83-96 (2005).
33. Ding, N., et al. Mediator links epigenetic silencing of neuronal gene expression with x-linked mental retardation. Mol. Cell 31, 347-359 (2008).
34. Liu, Y., et al. Two cyclin-dependent kinases promote RNA polymerase II transcription and formation of the scaffold complex. Mol. Cell. Biol. 24, 1721-1735 (2004).
35. Firestein, R., et al. CDK8 is a colorectal cancer oncogene that regulates β-catenin activity. Nature 455, 547-551 (2008).
36. Meyer, K.D., et al. Cooperative activity of cdk8 and GCN5L within Mediator directs tandem phosphoacetylation of histone H3. EMBO J. 27, 1447-1457 (2008).
37. Morris, E.J., et al. E2F1 represses β-catenin transcription and is antagonized by both pRB and CDK8. Nature 455, 552-556 (2008).
38. Zippo, A., et al. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138, 1122-1136 (2009).
39. Davis, R.J. Transcriptional regulation by MAP kinases. Mol. Reprod. Dev. 42, 459-467 (1995).
40. Li, Q.-J. MAP kinase phosphorylation-dependent activation of Elk-1 leads to activation of the co-activator p300. EMBO J. 22, 281-291 (2003).
41. Stevens, J.L., et al. Transcription control by E1A and MAP kinase pathway via Sur2 mediator subunit. Science 296, 755-758 (2002).
42. Yamaguchi, Y., et al. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97, 41-51 (1999).
43. Wada, T., et al. DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev. 12, 343-356 (1998).
44. Bourgeois, C.F., Kim, Y.K., Churcher, M.J., West, M.J. & Karn, J. Spt5 cooperates with human immunodefciency virus type 1 Tat by preventing premature RNA release at terminator sequences. Mol. Cell. Biol. 22, 1079-1093 (2002).
45. Orphanides, G., Wu, W.H., Lane, W.S., Hampsey, M. & Reinberg, D. The chromatin-specifc transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400, 284-288 (1999).
46. Hargreaves, D.C., Horng, T. & Medzhitov, R. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 138, 129-145 (2009).
47. Houzelstein, D., et al. Growth and early postimplantation defects in mice defcient for the bromodomain-containing protein Brd4. Mol. Cell. Biol. 22, 3794-3802 (2002).
48. Wu, S.Y. & Chiang, C.M. The double bromodomain-containing chromatin adaptor Brd4 and transcriptional regulation. J. Biol. Chem. 282, 13141-13145 (2007).
49. Jang, M.K., et al. The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol. Cell 19, 523-534 (2005).
50. Esnault, C., et al. Mediator-dependent recruitment of TFIIH modules in preinitiation complex. Mol. Cell 31, 337-346 (2008).
51. Knuesel, M.T., Meyer, K.D., Donner, A.J., Espinosa, J.M. & Taatjes, D.J. The human CDK8 subcomplex is a histone kinase that requires Med12 for activity and can function independently of mediator. Mol. Cell. Biol. 29, 650-661 (2009).
52. Akoulitchev, S., Chuikov, S. & Reinberg, D. TFIIH is negatively regulated by cdk8-containing mediator complexes. Nature 407, 102-106 (2000).
53. Feaver, W.J., Svejstrup, J.Q., Henry, N.L. & Kornberg, R.D. Relationship of CDK-activating kinase and RNA polymerase II CTD kinase TFIIH/TFIIK. Cell 79, 1103-1109 (1994).
54. Kanin, E.I., et al. Chemical inhibition of the TFIIH-associated kinase Cdk7/Kin28 does not impair global mRNA synthesis. Proc. Natl. Acad. Sci. USA 104, 5812-5817 (2007).
55. Larochelle, S., et al. Requirements for Cdk7 in the assembly of Cdk1/cyclin B and activation of Cdk2 revealed by chemical genetics in human cells. Mol. Cell 25, 839-850 (2007).
56. Glover-Cutter, K., et al. TFIIH-associated Cdk7 kinase functions in phosphorylation of C-terminal domain Ser7 residues, promoter-proximal pausing, and termination by RNA polymerase II. Mol. Cell. Biol. 29, 5455-5464 (2009).
57. Jones, J.C., et al. C-terminal repeat domain kinase I phosphorylates Ser2 and Ser5 of RNA polymerase II C-terminal domain repeats. J. Biol. Chem. 279, 24957-24964 (2004).
58. Gomes, N.P., et al. Gene-specifc requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev. 20, 601-612 (2006).
59. Viladevall, L., et al. TFIIH and P-TEFb coordinate transcription with capping enzyme recruitment at specifc genes in fssion yeast. Mol. Cell 33, 738-751 (2009).
60. Barboric, M., Nissen, R.M., Kanazawa, S., Jabrane-Ferrat, N. & Peterlin, B.M. NF-κB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol. Cell 8, 327-337 (2001).