Dr1 (NC2) is present at tRNA genes and represses their transcription in human cells

Nucleic Acids Research

Volumn 38, Issue 4, 2009, Pages 1228-1239

  Kantidakis, Theodoros ^a,b   White, Robert J ^a,b  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOWN REGULATOR OF TRANSCRIPTION 1; DOWN REGULATOR OF TRANSCRIPTION 1 ASSOCIATED PROTEIN 1; NEGATIVE COFACTOR 2BETA; PROTEIN BRF1; REPRESSOR PROTEIN; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSFER RNA; UNCLASSIFIED DRUG; DNA DIRECTED RNA POLYMERASE III; DOWN-REGULATOR OF TRANSCRIPTION 1; DRAP1 PROTEIN, HUMAN; PHOSPHOPROTEIN; TRANSCRIPTION FACTOR IIIB;

ARTICLE; CELL STRAIN HEK293; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CROSS LINKING; DIMERIZATION; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN INDUCTION; PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CELL LINE; CHO CELL; CRICETULUS; DRUG ANTAGONISM; GENE EXPRESSION REGULATION; GENETICS; HAMSTER; METABOLISM;

ANIMALS; CELL LINE; CHO CELLS; CRICETINAE; CRICETULUS; GENE EXPRESSION REGULATION; HUMANS; PHOSPHOPROTEINS; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA POLYMERASE III; RNA, TRANSFER; TRANSCRIPTION FACTOR TFIIIB; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 77950365283     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1102     Document Type: Article

References (50)

1. Inostroza, J.A., Mermelstein, F.H., Ha, I., Lane, W.S. and Reinberg, D. (1992) Dr1, a TATA-binding protein-associated phosphoprotein and inhibitor of class II gene transcription. Cell, 70, 477-489.
2. Meisterernst, M. and Roeder, R.G. (1991) Family of proteins that interact with TFIID and regulate promoter activity. Cell, 67, 557-567.
3. Mermelstein, F., Yeung, K., Cao, J., Inostroza, J.A., Erdjument-Bromage, H., Eagelson, K., Landsman, D., Levitt, P., Tempst, P. and Reinberg, D. (1996) Requirement of a corepressor for Dr1-mediated repression of transcription. Genes Dev., 10, 1033-1048.
4. Goppelt, A. and Meisterernst, M. (1996) Characterization of the basal inhibitor of class II transcription NC2 from Saccharomyces cerevisiae. Nucleic Acids Res., 24, 4450-4455.
5. Kraus, V.B., Inostroza, J.A., Yeung, K., Reinberg, D. and Nevins, J.R. (1994) Interaction of the Dr1 inhibitory factor with the TATA binding protein is disrupted by adenovirus E1A. Proc. Natl Acad. Sci. USA, 91, 6279-6282.
6. Prelich, G. (1997) Saccharomyces cerevisiae BUR6 encodes a DRAP1/NC2alpha homolog that has both positive and negative roles in transcription in vivo. Mol. Cell Biol., 17, 2057-2065.
7. Kim, S., Na, J.G., Hampsey, M. and Reinberg, D. (1997) The Dr1/DRAP1 heterodimer is a global repressor of transcription in vivo. Proc. Natl Acad. Sci. USA, 94, 820-825.
8. Gadbois, E.L., Chao, D.M., Reese, J.C., Green, M.R. and Young, R.A. (1997) Functional antagonism between RNA polymerase II holoenzyme and global negative regulator NC2 in vivo. Proc. Natl Acad. Sci. USA, 94, 3145-3150.
9. Lemaire, M., Xie, J., Meisterernst, M. and Collart, M.A. (2000) The NC2 repressor is dispensable in yeast mutated for the Sin4p component of the holoenzyme and plays roles similar to Mot1p in vivo. Mol. Microbiol., 36, 163-173.
10. Yeung, K.C., Inostroza, J.A., Mermelstein, F.H., Kannabiran, C. and Reinberg, D. (1994) Structure-function analysis of the TBP-binding protein Dr1 reveals a mechanism for repression of class II gene transcription. Genes Dev., 8, 2097-2109.
11. Yeung, K., Kim, S. and Reinberg, D. (1997) Functional dissection of a human Dr1-DRAP1 repressor complex. Mol. Cell Biol., 17, 36-45.
12. Kamada, K., Shu, F., Chen, H., Malik, S., Stelzer, G., Roeder, R.G., Meisterernst, M. and Burley, S.K. (2001) Crystal structure of negative cofactor 2 recognizing the TBP-DNA transcription complex. Cell, 106, 71-81.
13. Schluesche, P., Stelzer, G., Piaia, E., Lamb, D.C. and Meisterernst, M. (2007) NC2 mobilizes TBP on core promoter TATA boxes. Nat. Struct. Mol. Biol., 14, 1196-1201.
14. Castano, E., Gross, P., Wang, Z., Roeder, R.G. and Oelgeschlager, T. (2000) The C-terminal domain-phosphorylated IIO form of RNA polymerase II is associated with the transcription repressor NC2 (Dr1/DRAP1) and is required for transcription activation in human nuclear extracts. Proc. Natl Acad. Sci. USA, 97, 7184-7189.
15. Geisberg, J.V., Holstege, F.C., Young, R.A. and Struhl, K. (2001) Yeast NC2 associates with the RNA polymerase II preinitiation complex and selectively affects transcription in vivo. Mol. Cell Biol., 21, 2736-2742.
16. Cang, Y. and Prelich, G. (2002) Direct stimulation of transcription by negative cofactor 2 (NC2) through TATA-binding protein (TBP). Proc. Natl Acad. Sci. USA, 99, 12727-12732.
17. Hsu, J.Y., Juven-Gershon, T., Marr, M.T. 2nd, Wright, K.J., Tjian, R. and Kadonaga, J.T. (2008) TBP, Mot1, and NC2 establish a regulatory circuit that controls DPE-dependent versus TATA-dependent transcription. Genes Dev., 22, 2353-2358.
18. Willy, P.J., Kobayashi, R. and Kadonaga, J.T. (2000) A basal transcription factor that activates or represses transcription. Science, 290, 982-985.
19. Deng, W., Malecova, B., Oelgeschlager, T. and Roberts, S.G. (2009) TFIIB recognition elements control the TFIIA-NC2 axis in transcriptional regulation. Mol. Cell Biol., 29, 1389-1400.
20. van Werven, F.J., van Bakel, H., van Teeffelen, H.A., Altelaar, A.F., Koerkamp, M.G., Heck, A.J., Holstege, F.C. and Timmers, H.T. (2008) Cooperative action of NC2 and Mot1p to regulate TATA-binding protein function across the genome. Genes Dev., 22, 2359-2369.
21. White, R.J., Khoo, B.C., Inostroza, J.A., Reinberg, D. and Jackson, S.P. (1994) Differential regulation of RNA polymerases I, II, and III by the TBP-binding repressor Dr1. Science, 266, 448-450.
22. Schramm, L. and Hernandez, N. (2002) Recruitment of RNA polymerase III to its target promoters. Genes Dev., 16, 2593-2620.
23. Marshall, L., Kenneth, N.S. and White, R.J. (2008) Elevated tRNA(iMet) synthesis can drive cell proliferation and oncogenic transformation. Cell, 133, 78-89.
24. Brummelkamp, T.R., Bernards, R. and Agami, R. (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science, 296, 550-553.
25. Larminie, C.G., Sutcliffe, J.E., Tosh, K., Winter, A.G., Felton-Edkins, Z.A. and White, R.J. (1999) Activation of RNA polymerase III transcription in cells transformed by simian virus 40. Mol. Cell Biol., 19, 4927-4934.
26. Winter, A.G., Sourvinos, G., Allison, S.J., Tosh, K., Scott, P.H., Spandidos, D.A. and White, R.J. (2000) RNA polymerase III transcription factor TFIIIC2 is overexpressed in ovarian tumors. Proc. Natl Acad. Sci. USA, 97, 12619-12624.
27. Daly, N.L., Arvanitis, D.A., Fairley, J.A., Gomez-Roman, N., Morton, J.P., Graham, S.V., Spandidos, D.A. and White, R.J. (2005) Deregulation of RNA polymerase III transcription in cervical epithelium in response to high-risk human papillomavirus. Oncogene, 24, 880-888.
28. Felton-Edkins, Z.A. and White, R.J. (2002) Multiple mechanisms contribute to the activation of RNA polymerase III transcription in cells transformed by papovaviruses. J. Biol. Chem., 277, 48182-48191.
29. Grandori, C., Gomez-Roman, N., Felton-Edkins, Z.A., Ngouenet, C., Galloway, D.A., Eisenman, R.N. and White, R.J. (2005) c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat. Cell Biol., 7, 311-318.
30. Innes, F., Ramsbottom, B. and White, R.J. (2006) A test of the model that RNA polymerase III transcription is regulated by selective induction of the 110 kDa subunit of TFIIIC. Nucleic Acids Res., 34, 3399-3407.
31. White, R.J., Gottlieb, T.M., Downes, C.S. and Jackson, S.P. (1995) Mitotic regulation of a TATA-binding-protein-containing complex. Mol. Cell Biol., 15, 1983-1992.
32. Gomez-Roman, N., Grandori, C., Eisenman, R.N. and White, R.J. (2003) Direct activation of RNA polymerase III transcription by c-Myc. Nature, 421, 290-294.
33. Pruzan, R., Chatterjee, P.K. and Flint, S.J. (1992) Specific transcription from the adenovirus E2E promoter by RNA polymerase III requires a subpopulation of TFIID. Nucleic Acids Res., 20, 5705-5712.
34. Cairns, C.A. and White, R.J. (1998) p53 is a general repressor of RNA polymerase III transcription. EMBO J., 17, 3112-3123.
35. Fairley, J.A., Scott, P.H. and White, R.J. (2003) TFIIIB is phosphorylated, disrupted and selectively released from tRNA promoters during mitosis in vivo. EMBO J., 22, 5841-5850.
36. Fairley, J.A., Kantidakis, T., Kenneth, N.S., Intine, R.V., Maraia, R.J. and White, R.J. (2005) Human La is found at RNA polymerase III-transcribed genes in vivo. Proc. Natl Acad. Sci. USA, 102, 18350-18355.
37. Goodfellow, S.J., Graham, E.L., Kantidakis, T., Marshall, L., Coppins, B.A., Oficjalska-Pham, D., Gerard, M., Lefebvre, O. and White, R.J. (2008) Regulation of RNA polymerase III transcription by Maf1 in mammalian cells. J. Mol. Biol., 378, 481-491.
38. Schramm, L., Pendergrast, P.S., Sun, Y. and Hernandez, N. (2000) Different human TFIIIB activities direct RNA polymerase III transcription from TATA-containing and TATA-less promoters. Genes Dev., 14, 2650-2663.
39. Yuan, C.C., Zhao, X., Florens, L., Swanson, S.K., Washburn, M.P. and Hernandez, N. (2007) CHD8 associates with human Staf and contributes to efficient U6 RNA polymerase III transcription. Mol. Cell Biol., 27, 8729-8738.
40. Malecova, B., Gross, P., Boyer-Guittaut, M., Yavuz, S. and Oelgeschlager, T. (2007) The initiator core promoter element antagonizes repression of TATA-directed transcription by negative cofactor NC2. J. Biol. Chem., 282, 24767-24776.
41. Creton, S., Svejstrup, J.Q. and Collart, M.A. (2002) The NC2 alpha and beta subunits play different roles in vivo. Genes Dev., 16, 3265-3276.
42. Masson, P., Leimgruber, E., Creton, S. and Collart, M.A. (2008) The dual control of TFIIB recruitment by NC2 is gene specific. Nucleic Acids Res., 36, 539-549.
43. Christova, R. and Oelgeschlager, T. (2002) Association of human TFIID-promoter complexes with silenced mitotic chromatin in vivo. Nat. Cell Biol., 4, 79-82.
44. Albert, T.K., Grote, K., Boeing, S., Stelzer, G., Schepers, A. and Meisterernst, M. (2007) Global distribution of negative cofactor 2 subunit-alpha on human promoters. Proc. Natl Acad. Sci. USA, 104, 10000-10005.
45. Kassavetis, G.A. and Geiduschek, E.P. (2006) Transcription factor TFIIIB and transcription by RNA polymerase III. Biochem. Soc. Trans., 34, 1082-1087.
46. Juo, Z.S., Kassavetis, G.A., Wang, J., Geiduschek, E.P. and Sigler, P.B. (2003) Crystal structure of a transcription factor IIIB core interface ternary complex. Nature, 422, 534-539.
47. Geisberg, J.V., Moqtaderi, Z., Kuras, L. and Struhl, K. (2002) Mot1 associates with transcriptionally active promoters and inhibits association of NC2 in Saccharomyces cerevisiae. Mol. Cell Biol., 22, 8122-8134.
48. Marshall, L. and White, R.J. (2008) Non-coding RNA production by RNA polymerase III is implicated in cancer. Nat. Rev. Cancer, 8, 911-914.
49. Johnson, D.L. and Johnson, S.A. (2008) Cell biology. RNA metabolism and oncogenesis. Science, 320, 461-462.
50. Di Pietro, C., Ragusa, M., Barbagallo, D., Duro, L.R., Guglielmino, M.R., Majorana, A., Giunta, V., Rapisarda, A., Tricarichi, E., Miceli, M. et al. (2008) Involvement of GTA protein NC2β in neuroblastoma pathogenesis suggests that it physiologically participates in the regulation of cell proliferation. Mol. Cancer, 7, 52.