UBF activates RNA polymerase I transcription by stimulating promoter escape

EMBO Journal

Volumn 25, Issue 14, 2006, Pages 3310-3322

  Panov, Kostya I ^a   Friedrich, J Karsten ^a,b   Russell, Jackie ^a   Zomerdijk, Joost C B M ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Promoter escape; Recruitment; RNA polymerase I; Transcription activation; UBF

Indexed keywords

DNA DIRECTED RNA POLYMERASE; PHOSPHORUS 32; RIBOSOME DNA; RIBOSOME RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR UBF; UNCLASSIFIED DRUG; URIDINE TRIPHOSPHATE;

ARTICLE; GENETIC TRANSCRIPTION; HUMAN; ISOTOPE LABELING; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PURIFICATION; RNA SYNTHESIS; TRANSCRIPTION INITIATION;

BASE SEQUENCE; DNA, RIBOSOMAL; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; POL1 TRANSCRIPTION INITIATION COMPLEX PROTEINS; PROMOTER REGIONS (GENETICS); RNA POLYMERASE I; TRANS-ACTIVATION (GENETICS);

EID: 33746517313     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601221     Document Type: Article

References (81)

1. Bachvarov D, Moss T (1991) The RNA polymerase I transcription factor xUBF contains 5 tandemly repeated HMG homology boxes. Nucleic Acids Res 19: 2331-2335
2. Bazett Jones DP, Leblanc B, Herfort M, Moss T (1994) Short-range DNA looping by the Xenopus HMG-box transcription factor, xUBF. Science 264: 1134-1137
3. Beckmann H, Chen JL, O'Brien T, Tjian R (1995) Coactivator and promoter-selective properties of RNA polymerase I TAFs. Science 270: 1506-1509
4. Bell SP, Learned RM, Jantzen HM, Tjian R (1988) Functional cooperativity between transcription factors UBF1 and SL1 mediates human ribosomal RNA synthesis. Science 241: 1192-1197
5. Bodeker M, Cairns C, McStay B (1996) Upstream binding factor stabilizes Rib 1, the TATA-binding-protein-containing Xenopus laevis RNA polymerase I transcription factor, by multiple protein interactions in a DNA-independent manner. Mol Cell Biol 16: 5572-5578
6. Bodem J, Dobreva G, Hoffmann-Rohrer U, Iben S, Zentgrafl H, Deliusl H, Vingron M, Grummt I (2000) TIF-IA, the factor mediating growth-dependent control of ribosomal RNA synthesis, is the mammalian homolog of yeast Rrn3p. EMBO Rep 1: 171-175
7. Bowser CA, Hanna MM (1991) Sigma subunit of Escherichia coli RNA polymerase loses contacts with the 3′ end of the nascent RNA after synthesis of a tetranucleotide. J Mol Biol 220: 227-239
8. Brou C, Kuhn A, Staub A, Chaudhary S, Grummt I, Davidson I, Tora L (1993) Sequence-specific transactivators counteract topoisomerase II-mediated inhibition of in vitro transcription by RNA polymerases I and II. Nucleic Acids Res 21: 4011-4018
9. Brun RP, Ryan K, Sollner-Webb B (1994) Factor C*, the specific initiation component of the mouse RNA polymerase I holoenzyme, is inactivated early in the transcription process. Mol Cell Biol 14: 5010-5021
10. Carpousis AJ, Gralla JD (1980) Cycling of ribonucleic acid polymerase to produce oligonucleotides during initiation in vitro at the lac UV5 promoter. Biochemistry 19: 3245-3253
11. Cavanaugh AH, Hempel WM, Taylor LJ, Rogalsky V, Todorov G, Rothblum LI (1995) Activity of RNA polymerase I transcription factor UBF blocked by Rb gene product. Nature 374: 177-180
12. Cheetham GM, Steitz TA (1999) Structure of a transcribing T7 RNA polymerase initiation complex. Science 286: 2305-2309
13. Cheetham GM, Steitz TA (2000) Insights into transcription: structure and function of single-subunit DNA-dependent RNA polymerases. Curr Opin Struct Biol 10: 117-123
14. Comai L (2004) Mechanism of RNA polymerase I transcription. Adv Protein Chem 67: 123-155
15. Comai L, Tanese N, Tjian R (1992) The TATA-binding protein and associated factors are integral components of the RNA polymerase I transcription factor, SL1. Cell 68: 965-976
16. Comai L, Zomerdijk JCBM, Beckmann H, Zhou S, Admon A, Tjian R (1994) Reconstitution of transcription factor SL1: exclusive binding of TBP by SL1 or TFIID subunits. Science 266: 1966-1972
17. Copenhaver GP, Putnam CD, Denton ML, Pikaard CS (1994) The RNA polymerase I transcription factor UBF is a sequence-tolerant HMG-box protein that can recognize structured nucleic acids. Nucleic Acids Res 22: 2651-2657
18. De Carlo S, Carles C, Riva M, Schultz P (2003) Cryo-negative staining reveals conformational flexibility within yeast RNA polymerase I. J Mol Biol 329: 891-902
19. Drakas R, Tu X, Baserga R (2004) Control of cell size through phosphorylation of upstream binding factor 1 by nuclear phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 101: 9272-9276
20. Dvir A (2002) Promoter escape by RNA polymerase II. Biochim Biophys Acta 1577: 208-223
21. Friedrich JK, Panov KI, Cabart P, Russell J, Zomerdijk JCBM (2005) TBP-TAF complex SL1 directs RNA polymerase I pre-initiation complex formation and stabilizes upstream binding factor at the rDNA promoter. J Biol Chem 280: 29551-29558
22. Fukuda A, Nakadai T, Shimada M, Tsukui T, Matsumoto M, Nogi Y, Meisterernst M, Hisatake K (2004) Transcriptional coactivator PC4 stimulates promoter escape and facilitates transcriptional synergy by GAL4-VP16. Mol Cell Biol 24: 6525-6535
23. Gokal PK, Mahajan PB, Thompson EA (1990) Hormonal regulation of transcription of rDNA. Formation of initiated complexes by RNA polymerase I in vitro. J Biol Chem 265: 16234-16243
24. Grummt I (2003) Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 17: 1691-1702
25. Hanada K, Song CZ, Yamamoto K, Yano K, Maeda Y, Yamaguchi K, Muramatsu M (1996) RNA polymerase I associated factor 53 binds to the nucleolar transcription factor UBF and functions in specific rDNA transcription. EMBO J 15: 2217-2226
26. Hannan KM, Brandenburger Y, Jenkins A, Sharkey K, Cavanaugh A, Rothblum L, Moss T, Poortinga G, McArthur GA, Pearson RB, Hannan RD (2003) mTOR-dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF. Mol Cell Biol 23: 8862-8877
27. Hannan KM, Hannan RD, Rothblum LI (1998) Transcription by RNA polymerase I. Front Biosci 3: d376-d398
28. Hannan KM, Hannan RD, Smith SD, Jefferson LS, Lun M, Rothblum LI (2000) Rb and p130 regulate RNA polymerase I transcription: Rb disrupts the interaction between UBF and SL-1. Oncogene 19: 4988-4999
29. Hannan RD, Cavanaugh A, Hempel WM, Moss T, Rothblum L (1999) Identification of a mammalian RNA polymerase I holoenzyme containing components of the DNA repair/replication system. Nucleic Acids Res 27: 3720-3727
30. Hempel WM, Cavanaugh AH, Hannan RD, Taylor L, Rothblum LI (1996) The species-specific RNA polymerase I transcription factor SL-1 binds to upstream binding factor. Mol Cell Biol 16: 557-563
31. Hirschler-Laszkiewicz I, Cavanaugh AH, Mirza A, Lun M, Hu Q, Smink T, Rothblum LI (2003) Rrn3 becomes inactivated in the process of ribosomal DNA transcription. J Biol Chem 278: 18953-18959
32. Hu CH, McStay B, Jeong SW, Reeder RH (1994) xUBF, an RNA polymerase I transcription factor, binds crossover DNA with low sequence specificity. Mol Cell Biol 14: 2871-2882
33. Jantzen HM, Admon A, Bell SP, Tjian R (1990) Nucleolar transcription factor hUBF contains a DNA-binding motif with homology to HMG proteins. Nature 344: 830-836
34. Jantzen HM, Chow AM, King DS, Tjian R (1992) Multiple domains of the RNA polymerase I activator hUBF interact with the TATA-binding protein complex hSL1 to mediate transcription. Genes Dev 6: 1950-1963
35. Kihm AJ, Hershey JC, Haystead TA, Madsen CS, Owens GK (1998) Phosphorylation of the rRNA transcription factor upstream binding factor promotes its association with TATA binding protein. Proc Natl Acad Sci USA 95: 14816-14820
36. Kingston RE, Green MR (1994) Modeling eukaryotic transcriptional activation. Curr Biol 4: 325-332
37. Klein J, Grummt I (1999) Cell cycle-dependent regulation of RNA polymerase I transcription: the nucleolar transcription factor UBF is inactive in mitosis and early G1. Proc Natl Acad Sci USA 96: 6096-6101
38. Kugel JF, Goodrich JA (1998) Promoter escape limits the rate of RNA polymerase II transcription and is enhanced by TFIIE, TFIIH, and ATP on negatively supercoiled DNA. Proc Natl Acad Sci USA 95: 9232-9237
39. Kugel JF, Goodrich JA (2002) Translocation after synthesis of a four-nucleotide RNA commits RNA polymerase II to promoter escape. Mol Cell Biol 22: 762-773
40. Kuhn A, Grummt I (1992) Dual role of the nucleolar transcription factor UBF: trans-activator and antirepressor. Proc Natl Acad Sci USA 89: 7340-7344
41. Kwon H, Green MR (1994) The RNA polymerase I transcription factor, upstream binding factor, interacts directly with the TATA box-binding protein. J Biol Chem 269: 30140-30146
42. Learned RM, Learned TK, Haltiner MM, Tjian RT (1986) Human rRNA transcription is modulated by the coordinate binding of two factors to an upstream control element. Cell 45: 847-857
43. Leblanc B, Read C, Moss T (1993) Recognition of the Xenopus ribosomal core promoter by the transcription factor xUBF involves multiple HMG box domains and leads to an xUBF interdomain interaction. EMBO J 12: 513-525
44. Liu J, Akoulitchev S, Weber A, Ge H, Chuikov S, Libutti D, Wang XW, Conaway JW, Harris CC, Conaway RC, Reinberg D, Levens D (2001) Defective interplay of activators and repressors with TFIH in xeroderma pigmentosum. Cell 104: 353-363
45. Mais C, Wright JE, Prieto JL, Raggett SL, McStay B (2005) UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery. Genes Dev 19: 50-64
46. McClure WR (1985) Mechanism and control of transcription initiation in prokaryotes. Annu Rev Biochem 54: 171-204
47. McStay B, Frazier MW, Reeder RH (1991) xUBF contains a novel dimerization domain essential for RNA polymerase I transcription. Genes Dev 5: 1957-1968
48. Meraner J, Lechner M, Loidl A, Goralik-Schramel M, Voit R, Grummt I, Loidl P (2006) Acetylation of UBF changes during the cell cycle and regulates the interaction of UBF with RNA polymerase I. Nucleic Acids Res 34: 1798-1806
49. Milkereit P, Tschochner H (1998) A specialized form of RNA polymerase I, essential for initiation and growth-dependent regulation of rRNA synthesis, is disrupted during transcription. EMBO J 17: 3692-3703
50. Miller G, Panov KI, Friedrich JK, Trinkle-Mulcahy L, Lamond AI, Zomerdijk JCBM (2001) hRRN3 is essential in the SL1-mediated recruitment of RNA polymerase I to rRNA gene promoters. EMBO J 20: 1373-1382
51. Moore PB, Steitz TA (2002) The involvement of RNA in ribosome function. Nature 418: 229-235
52. Moss T (2004) At the crossroads of growth control; making ribosomal RNA. Curr Opin Genet Dev 14: 210-217
53. Moss T, Stefanovsky VY (2002) At the center of eukaryotic life. Cell 109: 545-548
54. O'Mahony DJ, Smith SD, Xie W, Rothblum LI (1992a) Analysis of the phosphorylation, DNA-binding and dimerization properties of the RNA polymerase I transcription factors UBF1 and UBF2. Nucleic Acids Res 20: 1301-1308
55. O'Mahony DJ, Xie WQ, Smith SD, Singer HA, Rothblum LI (1992b) Differential phosphorylation and localization of the transcription factor UBF in vivo in response to serum deprivation. In vitro dephosphorylation of UBF reduces its transactivation properties. J Biol Chem 267: 35-38
56. O'Sullivan AC, Sullivan GJ, McStay B (2002) UBF binding in vivo is not restricted to regulatory sequences within the vertebrate ribosomal DNA repeat. Mol Cell Biol 22: 657-668
57. Panov KI, Friedrich JK, Zomerdijk JC (2001) A step subsequent to preinitiation complex assembly at the ribosomal RNA gene promoter is rate limiting for human RNA polymerase I-dependent transcription. Mol Cell Biol 21: 2641-2649
58. Panov KI, Panova TB, Gadal O, Nishiyama K, Saito T, Russell J, Zomerdijk JCBM (2006) RNA polymerase I-specific subunit CAST/hPAF49 has a role in the activation of transcription by UBF. Mol Cell Biol 26 (in press)
59. Panova TB, Panov Ki, Russell J, Zomerdijk JCBM (2006) CK2 associates with initiation-competent RNA polymerase I and has multiple roles in rDNA transcription. Mol Cell Biol 26 (in press)
60. Pelletier G, Stefanovsky VY, Faubladier M, Hirschler-Laszkiewicz I, Savard J, Rothblum LI, Cote J, Moss T (2000) Competitive recruitment of CBP and Rb-HDAC regulates UBF acetylation and ribosomal transcription. Mol Cell 6: 1059-1066
61. Peyroche G, Milkereit P, Bischler N, Tschochner H, Schultz P, Sentenac A, Carles C, Riva M (2000) The recruitment of RNA polymerase I on rDNA is mediated by the interaction of the A43 subunit with Rrn3. EMBO J 19: 5473-5482
62. Ptashne M, Gann A (1997) Transcriptional activation by recruitment. Nature 386: 569-577
63. Putnam CD, Copenhaver GP, Denton ML, Pikaard CS (1994) The RNA polymerase I transactivator upstream binding factor requires its dimerization domain and high-mobility-group (HMG) box 1 to bend, wrap, and positively supercoil enhancer DNA. Mol Cell Biol 14: 6476-6488
64. Reeder RH (1999) Regulation of RNA polymerase I transcription in yeast and vertebrates. Prog Nucleic Acid Res Mol Biol 62: 293-327
65. Reeder RH, Pikaard CS, McStay B (1995) UBF, an architectural element for RNA polymerase I promoters. In Nucleic Acids and Molecular Biology, Eckstein F, Lilley DMJ (eds) Vol. 9, pp 251-263. Berlin, Heidelberg: Springer-Verlag
66. Russell J, Zomerdijk JCBM (2005) RNA-polymerase-I-directed rDNA transcription, life and works. Trends Biochem Sci 30: 87-96
67. Schnapp A, Grummt I (1991) Transcription complex formation at the mouse rDNA promoter involves the stepwise association of four transcription factors and RNA polymerase I. J Biol Chem 266: 24588-24595
68. Schnapp G, Santori F, Carles C, Riva M, Grummt I (1994) The HMG box-containing nucleolar transcription factor UBF interacts with a specific subunit of RNA polymerase I. EMBO J 13: 190-199
69. Seither P, Iben S, Grummt I (1998) Mammalian RNA polymerase I exists as a holoenzyme with associated basal transcription factors. J Mol Biol 275: 43-53
70. Smith SD, O'Mahony DJ, Kinsella BT, Rothblum LI (1993) Transcription from the rat 45S ribosomal DNA promoter does not require the factor UBF. Gene Expr 3: 229-236
71. Stefanovsky V, Langlois F, Gagnon-Kugler T, Rothblum LI, Moss T (2006) Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phosphorylation and r-chromatin remodeling. Mol Cell 21: 629-639
72. Stefanovsky VY, Pelletier G, Bazett-Jones DP, Crane-Robinson C, Moss T (2001a) DNA looping in the RNA polymerase I enhance-some is the result of non-cooperative in-phase bending by two UBF molecules. Nucleic Acids Res 29: 3241-3247
73. Stefanovsky VY, Pelletier G, Hannan R, Gagnon-Kugler T, Rothblum LI, Moss T (2001b) An immediate response of ribosomal transcription to growth factor stimulation in mammals is mediated by ERK phosphorylation of UBF. Mol Cell 8: 1063-1073
74. Tuan JC, Zhai W, Comai L (1999) Recruitment of TATA-binding protein-TAFI complex SL1 to the human ribosomal DNA promoter is mediated by the carboxy-terminal activation domain of upstream binding factor (UBF) and is regulated by UBF phosphorylation. Mol Cell Biol 19: 2872-2879
75. Voit R, Grummt I (2001) Phosphorylation of UBF at serine 388 is required for interaction with RNA polymerase I and activation of rDNA transcription. Proc Natl Acad Sci USA 98: 13631-13636
76. Voit R, Hoffmann M, Grummt I (1999) Phosphorylation by G1-specific cdk-cyclin complexes activates the nucleolar transcription factor UBF. EMBO J 18: 1891-1899
77. Voit R, Kuhn A, Sander EE, Grummt I (1995) Activation of mammalian ribosomal gene transcription requires phosphorylation of the nucleolar transcription factor UBF. Nucleic Acids Res 23: 2593-2599
78. Voit R, Schnapp A, Kuhn A, Rosenbauer H, Hirschmann P, Stunnenberg HG, Grummt I (1992) The nucleolar transcription factor mUBF is phosphorylated by casein kinase II in the C-terminal hyperacidic tail which is essential for transactivation. EMBO J 11: 2211-2218
79. Warner JR (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24: 437-440
80. Zomerdijk JCBM, Beckmann H, Comai L, Tjian R (1994) Assembly of transcriptionally active RNA polymerase I initiation factor SL1 from recombinant subunits. Science 266: 2015-2018
81. Zomerdijk JCBM, Tjian R (1998) Initiation of transcription on human rRNA genes. In Transcription of Eukaryotic Ribosomal RNA Genes by RNA Polymerase I. Paule MR (ed) New York, Austin, TX: Springer-Verlag