UBF levels determine the number of active ribosomal RNA genes in mammals

Journal of Cell Biology

Volumn 183, Issue 7, 2008, Pages 1259-1274

  Sanij, Elaine ^a   Poortinga, Gretchen ^a   Sharkey, Kerith ^a   Hung, Sandy ^a   Holloway, Timothy P ^a   Quin, Jaclyn ^a   Robb, Elysia ^a,g   Wong, Lee H ^b   Thomas, Walter G ^c   Stefanovsky, Victor ^d   Moss, Tom ^d   Rothblum, Lawrence ^e   Hannan, Katherine M ^a   McArthur, Grant A ^a,f   Pearson, Richard B ^a,f   Hannan, Ross D ^a,f  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b ROYAL CHILDREN'S HOSPITAL   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d LAVAL UNIVERSITY   (Canada)

^e UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF MELBOURNE   (Australia)

^g FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CURVED DNA; HIGH MOBILITY GROUP B1 PROTEIN; HISTONE H1; MITOGEN ACTIVATED PROTEIN KINASE; RIBOSOME RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR UPSTREAM BINDING FACTOR; TRANSCRIPTION FACTOR UPSTREAM BINDING FACTOR 1; UNCLASSIFIED DRUG; DNA DIRECTED RNA POLYMERASE; HISTONE; ISOPROTEIN; RIBOSOME DNA; TRANSCRIPTION FACTOR UBF;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DEPLETION; DNA STRUCTURE; GENE MUTATION; GENE NUMBER; GENE POOL; GENE SILENCING; MAMMAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; RNA SYNTHESIS; RNA TRANSCRIPTION; TRANSCRIPTION REGULATION; ANIMAL; BIOLOGICAL MODEL; CELL STRAIN 3T3; CHROMATIN; DNA METHYLATION; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSCRIPTION; GENETICS; HIGH MOBILITY GROUP BOX DOMAIN; METABOLISM; RNA GENE;

MAMMALIA;

ANIMALS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; DNA, RIBOSOMAL; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; GENES, RRNA; HISTONES; HMG-BOX DOMAINS; MICE; MODELS, GENETIC; NIH 3T3 CELLS; POL1 TRANSCRIPTION INITIATION COMPLEX PROTEINS; PROTEIN ISOFORMS; RNA POLYMERASE I; TRANSCRIPTION, GENETIC;

EID: 59449110517     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200805146     Document Type: Article

References (51)

1. Alzuherri, H.M., and R.J. White. 1999. Regulation of RNA polymerase I transcription in response to F9 embryonal carcinoma stem cell differentiation. J. Biol. Chem. 274:4328-4334.
2. Chen, D., A.S. Belmont, and S. Huang. 2004. Upstream binding factor association induces large-scale chromatin decondensation. Proc. Natl. Acad. Sci. USA. 101:15106-15111.
3. Conconi, A., R.M. Widmer, T. Koller , and J.M. Sogo. 1989. Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell. 57:753-761.
4. Dammann, R., R. Lucchini,T. Koller, and J.M. Sogo. 1993. Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucleic Acids Res. 21:2331-2338.
5. Datta, P.K., S. Budhiraja, R.R. Reichel, and S.T. Jacob . 1997 . Regulation of ribosomal RNA gene transcription during retinoic acid-induced differentiation of mouse teratocarcinoma cells. Exp. Cell Res. 231:198-205.
6. Dickins, R.A., K. McJunkin, E. Hernando, P.K. Premsrirut, V. Krizhanovsky, D.J. Burgess, S.Y. Kim, C. Cordon-Cardo, L. Zender , G.J. Hannon, and S.W. Lowe. 2007. Tissue-specif c and reversible RNA interference in transgenic mice. Nat. Genet. 39:914-921.
7. French, S.L., Y.N. Osheim, F. Cioci, M. Nomura, and A.L. Beyer. 2003. In exponentially growing Saccharomyces cerevisiae cells, rRNA synthesis is determined by the summed RNA polymerase I loading rate rather than by the number of active genes. Mol. Cell. Biol. 23:1558-1568.
8. Grummt, I., and C.S. Pikaard. 2003. Epigenetic silencing of RNA polymerase I transcription. Nat. Rev. Mol. Cell Biol. 4:641-649.
9. Hannan, R.D., V. Stefanovsky , L. Taylor , T . Moss, and L.I. Rothblum. 1996. Overexpression of the transcription factor UBF1 is suff cient to increase ribosomal DNA transcription in neonatal cardiomyocytes: implications for cardiac hypertrophy. Proc. Natl. Acad. Sci. USA. 93:8750-8755.
10. Hannan, R., V. Stefanovsky, T. Arino, L. Rothblum, and T. Moss . 1999 . Cellular regulation of ribosomal DNA transcription: both rat and Xenopus UBF1 stimulate rDNA transcription in 3T3 fbroblasts. Nucleic Acids Res. 27:1205-1213.
11. Heliot, L., H. Kaplan, L. Lucas, C. Klein, A. Beorchia, M. Doco-Fenzy, M. Menager, M. Thiry , M.F. O'Donohue, and D. Ploton. 1997. Electron tomography of metaphase nucleolar organizer regions: evidence for a twisted-loop organization. Mol. Biol. Cell. 8:2199-2216.
12. Hirschler-Laszkiewicz, I., A. Cavanaugh, Q. Hu, J. Catania, M.L. Avantaggiati, and L.I. Rothblum. 2001. The role of acetylation in rDNA transcription. Nucleic Acids Res. 29:4114-4124.
13. Huang, S., L.I. Rothblum, and D. Chen. 2006. Ribosomal chromatin organization. Biochem. Cell Biol. 84:444-449.
14. Jantzen, H.M., A.M. Chow, D.S. King, and R. Tjian. 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.
15. Jorgensen, P., and M. Tyers. 2004. How cells coordinate growth and division. Curr. Biol. 14:R1014-R1027.
16. Kermekchiev, M., J.L. Workman, and C.S. Pikaard. 1997. Nucleosome binding by the polymerase I transactivator upstream binding factor displaces linker histone H1. Mol. Cell. Biol. 17:5833-5842.
17. Kuhn, A., R. Voit, V. Stefanovsky , R. Evers, M. Bianchi, and I. Grummt. 1994. Functional differences between the two splice variants of the nucleolar transcription factor UBF: the second HMG box determines specif city of DNA binding and transcriptional activity. EMBO J. 13:416-424.
18. Larson, D.E., W. Xie, M. Glibetic, D. O'Mahony , B.H. Sells, and L.I. Rothblum. 1993 . Coordinated decreases in rRNA gene transcription factors and rRNA synthesis during muscle cell differentiation. Proc. Natl. Acad. Sci. USA. 90:7933-7936.
19. Lawrence, R.J., K. Earley, O. Pontes, M. Silva, Z.J. Chen, N. Neves, W. Viegas, and C.S. Pikaard. 2004. A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol. Cell. 13:599-609.
20. Li, J., G. Langst, and I. Grummt. 2006. NoRC-dependent nucleosome positioning silences rRNA genes. EMBO J. 25:5735-5741.
21. Liu, M., X. Tu, G. Ferrari-Amorotti, B. Calabretta, and R. Baserga. 2007. Downregulation of the upstream binding factor1 by glycogen synthase kinase3beta in myeloid cells induced to differentiate. J. Cell. Biochem. 100:1154-1169.
22. Mais, C., J.E. Wright, J.L. Prieto, S.L. Raggett, and B. McStay . 2005. UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery. Genes Dev. 19:50-64.
23. Mayer, C., and I. Grummt. 2005. Cellular stress and nucleolar function. Cell Cycle. 4:1036-1038.
24. McArthur, G.A., K.P. Foley, M.L. Fero, C.R. Walkley, A.J. Deans, J.M. Roberts, and R.N. Eisenman . 2002 . MAD1 and p27(KIP1) cooperate to promote terminal differentiation of granulocytes and to inhibit Myc expression and cyclin E-CDK2 activity. Mol. Cell. Biol. 22:3014-3023.
25. McStay, B., M.W. Frazier , and R.H. Reeder . 1991 . xUBF contains a novel dimerization domain essential for RNA polymerase I transcription. Genes Dev. 5:1957-1968.
26. Moss, T. 2004. At the crossroads of growth control; making ribosomal RNA. Curr. Opin. Genet. Dev. 14:210-217.
27. Moss, T., V. Stefanovsky, F. Langlois, and T. Gagnon-Kugler. 2006. A new paradigm for the regulation of the mammalian ribosomal RNA genes. Biochem. Soc. Trans. 34:1079-1081.
28. Moss, T., F. Langlois, T. Gagnon-Kugler, and V. Stefanovsky. 2007. A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell. Mol. Life Sci. 64:29-49.
29. O'Mahony, D.J., and L.I. Rothblum. 1991. Identif cation of two forms of the RNA polymerase I transcription factor UBF. Proc. Natl. Acad. Sci. USA 88:3180-3184.
30. O'Mahony, D.J., S.D. Smith, W. Xie, and L.I. Rothblum. 1992. 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.
31. O'Neill, T.E., J.G. Smith, and E.M. Bradbury. 1993. Histone octamer dissociation is not required for transcript elongation through arrays of nucleosome cores by phage T7 RNA polymerase in vitro. Proc. Natl. Acad. Sci. USA. 90:6203-6207.
32. O'Sullivan, A.C., G.J. Sullivan, and B. McStay . 2002. UBF binding in vivo is not restricted to regulatory sequences within the vertebrate ribosomal DNA repeat. Mol. Cell. Biol. 22:657-668.
33. Panov, K.I., J.K. Friedrich, J. Russell, and J.C. Zomerdijk. 2006. UBF activates RNA polymerase I transcription by stimulating promoter escape. EMBO J. 25:3310-3322.
34. Percipalle, P., N. Fomproix, E. Cavellan, R. Voit, G. Reimer, T. Kruger, J. Thyberg, U. Scheer, I. Grummt, and A.K. Farrants. 2006. The chromatin remodelling complex WSTF-SNF2h interacts with nuclear myosin 1 and has a role in RNA polymerase I transcription. EMBO Rep. 7:525-530.
35. Ploton, D., M. Menager, and J.J. Adnet. 1984. Simultaneous high resolution localization of Ag-NOR proteins and nucleoproteins in interphasic and mitotic nuclei. Histochem. J. 16:897-906.
36. Poortinga, G., K.M. Hannan, H. Snelling, C.R. Walkley, A. Jenkins, K. Sharkey, M. Wall, Y. Brandenburger, M. Palatsides, R.B. Pearson, et al. 2004. MAD1 and c-MYC regulate UBF and rDNA transcription during granulocyte differentiation. EMBO J. 23:3325-3335.
37. Prior , C.P. , C.R. Cantor , E.M. Johnson, V.C. Littau, and V.G. Allfrey. 1983. Reversible changes in nucleosome structure and histone H3 accessibility in transcriptionally active and inactive states of rDNA chromatin. Cell. 34:1033-1042.
38. Roussel, P., and D. Hernandez-Verdun. 1994. Identif cation of Ag-NOR proteins, markers of proliferation related to ribosomal gene activity. Exp. Cell Res. 214:465-472.
39. Santoro, R., and I. Grummt. 2001. Molecular mechanisms mediating methylationdependent silencing of ribosomal gene transcription. Mol. Cell. 8 : -725 .
40. Santoro, R., and I. Grummt. 2005. Epigenetic mechanism of rRNA gene silencing: temporal order of NoRC-mediated histone modif cation, chromatin remodeling, and DNA methylation. Mol. Cell. Biol. 25:2539-2546.
41. Santoro, R., J. Li, and I. Grummt. 2002. The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat. Genet. 32:393-396.
42. Smith, S.D., E. Oriahi, H.F. Yang-Yen, W.Q. Xie, C. Chen, and L.I. Rothblum. 1990 . Interaction of RNA polymerase I transcription factors with a promoter in the nontranscribed spacer of rat ribosomal DNA. Nucleic Acids Res. 18:1677-1685.
43. Stefanovsky , V., and T. Moss. 2006. Regulation of rRNA synthesis in human and mouse cells is not determined by changes in active gene count. Cell Cycle. 5:735-739.
44. Stefanovsky , V.Y., and T. Moss. 2008. The splice variants of UBF differentially regulate RNA polymerase I transcription elongation in response to ERK phosphorylation. Nucleic Acids Res. 36:5093-5101.
45. Stefanovsky, V.Y., G. Pelletier, D.P. Bazett-Jones, C. Crane-Robinson, and T. Moss . 2001a . DNA looping in the RNA polymerase I enhancesome is the result of non-cooperative in-phase bending by two UBF molecules. Nucleic Acids Res. 29:3241-3247.
46. Stefanovsky , V.Y., G. Pelletier, R. Hannan, T. Gagnon-Kugler, L.I. Rothblum, and T. Moss . 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.
47. Stefanovsky , V., F. Langlois, T. Gagnon-Kugler , L.I. Rothblum, and T. Moss . 2006a . Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phosphorylation and r-chromatin remodeling. Mol. Cell. 21:629-639.
48. Stefanovsky , V.Y., F . Langlois, D. Bazett-Jones, G. Pelletier , and T. Moss. 2006b . ERK modulates DNA bending and enhancesome structure by phosphorylating HMG1-boxes 1 and 2 of the RNA polymerase I transcription factor UBF. Biochemistry. 45:3626-3634.
49. Strohner, R., A. Nemeth, P. Jansa, U. Hofmann-Rohrer, R. Santoro, G. Langst, and I. Grummt. 2001. NoRC-a novel member of mammalian ISWI- containing chromatin remodeling machines. EMBO J. 20:4892-4900.
50. Walkley, C.R., L.E. Purton, H.J. Snelling, Y.D. Yuan, H. Nakajima, P. Chambon, R.A. Chandraratna, and G.A. McArthur. 2004. Identif cation of the molecular requirements for an RAR alpha-mediated cell cycle arrest during granulocytic differentiation. Blood. 103:1286-1295.
51. Weisenberger, D., and U. Scheer . 1995 . A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis. J. Cell Biol. 129:561-575.