Hmo1, an HMG-box protein, belongs to the yeast ribosomal DNA transcription system

EMBO Journal

Volumn 21, Issue 20, 2002, Pages 5498-5507

  Gadal, Olivier ^a   Labarre, Sylvie ^a   Boschiero, Claire ^a   Thuriaux, Pierre ^a  

^a CEA SACLAY   (France)

Author keywords

Nucleolus; RNA polymerase I; SGS1; Topoisomerases; UBF

Indexed keywords

DNA BINDING PROTEIN; DNA DIRECTED RNA POLYMERASE; DNA TOPOISOMERASE; HELICASE; HIGH MOBILITY GROUP B1 PROTEIN; MUTANT PROTEIN; PROTEIN FOB1; PROTEIN PAF53; PROTEIN RPA34; PROTEIN RPA49; RIBOSOME PROTEIN; RIBOSOME RNA; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING KINETICS; CELL NUCLEUS; ENZYME ANALYSIS; ENZYME DEFECT; ENZYME SYNTHESIS; EUKARYOTE; GENE MUTATION; GENE OVEREXPRESSION; HIGH MOBILITY GROUP BOX DOMAIN; LETHAL MUTANT; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; RIBOSOME; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; YEAST;

AMINO ACID SEQUENCE; ANIMALS; CELL NUCLEOLUS; DNA, FUNGAL; DNA, RIBOSOMAL; GENE DELETION; GENE EXPRESSION; GENES, FUNGAL; HIGH MOBILITY GROUP PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; RNA POLYMERASE I; RNA, FUNGAL; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION, GENETIC;

ANIMALIA; EUKARYOTA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0037107455     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf539     Document Type: Article

References (66)

1. Aprikian, P., Moorefield, B. and Reeder, R.H. (2001) New model for the yeast RNA polymerase I transcription cycle. Mol. Cell. Biol., 21, 4847-4855.
2. Baudin, A., Ozier-Kalogeropoulos, O., Denouel, A., Lacroute, F., and Cullin, C. (1993) A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res., 21, 3329-3330.
3. Bolotin-Fukuhara, M. et al. (2000) Genomic exploration of the hemiascomycetous yeasts: II. Kluyveromyces lactis. FEBS Lett., 487, 66-70.
4. Briand, J.F., Navarro, F., Rematier, P., Boschiero, C., Labarre, S., Werner, M., Shpakovski, G.V. and Thuriaux, P. (2001a) Partners of Rpb8p, a small subunit shared by yeast RNA polymerases I, II and III. Mol. Cell. Biol., 21, 6056-6065.
5. Briand J.F., Navarro, F., Gadal, O. and Thuriaux, P. (2001b) Cross talk between tRNA and rRNA synthesis in Saccharomyces cerevisiae. Mol. Cell. Biol., 21, 189-195.
6. Carles, C. and Riva, M. (1998) Yeast RNA polymerase I subunits and genes. In Paule, M.R. (ed.), Transcription of Ribosomal RNA Genes by Eukaryotic RNA Polymerase 1. Springer Verlag, pp. 9-38.
7. Chédin, S., Ferri, M.L., Peyroche, G., Andrau, J.C., Jourdain, S., Lefebvre, O., Werner, M., Carles, C. and Sentenac, A. (1998) The yeast RNA polymerase III transcription machinery: A paradigm for eukaryotic gene activation. Cold Spring Harbor Symp. Quant. Biol., 63, 381-389.
8. Christman, M.F., Dietrich, F.S., Levin, N.A., Sadoff, B.U. and Fink, G.R. (1993) The rRNA-encoding DNA array has an altered structure in topoisomerase I mutants of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA, 90, 7637-7641.
9. Comai, L., Tanese, N. and 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.
10. Defossez, P.A., Prusty, R., Kaeberlein, M., Lin, S.J., Ferrigno, P., Silver, P.A., Keil, R.L. and Guarente, L. (1999) Elimination of replication block protein Fob1 extends the life span of yeast mother cells. Mol. Cell, 3, 447-455.
11. Dolinski, K.J. and Heitman, J. (1999) Hmo1p, a high mobility group 1/2 homolog, genetically and physically interacts with the yeast FKBP12 prolyl isomerase. Genetics, 151, 935-944.
12. Eberhard, D., Tora, L., Egly, J.M. and Grummt, I. (1993) A TBP-containing multiprotein complex (TIF-IB) mediates transcription specificity of murine RNA polymerase I. Nucleic Acids Res., 21, 4180-4186.
13. Freeman, L., Aragon-Alcaide, L. and Strunnikov, A. (2000) The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J. Cell Biol., 149, 811-824.
14. Gadal, O., Mariotte-Labarre, S., Chédin, S., Quemeneur, E., Carles, C., Sentenac, A. and Thuriaux, P. (1997) A34.5, a nonessential component of yeast RNA polymerase I, cooperates with subunit A14 and DNA topoisomerase I to produce a functional rRNA synthesis machine. Mol. Cell. Biol., 17, 1787-1795.
15. Gadal, O., Strauss, D., Kessl, J., Trumpower, B., Tollervey, D. and Hurt, E. (2001) Nuclear export of 60S ribosomal subunits depends on Xpo1p and requires a nuclear export sequence-containing factor, Nmd3p, that associates with the large subunit protein Rp110p. Mol. Cell. Biol., 21, 3405-3415.
16. Galy, V., Olivo-Marin, J.C., Scherthan, H., Doye, V., Rascalou, N. and Nehrbass, U. (2000) Nuclear pore complexes in the organization of silent telomeric chromatin. Nature, 403, 108-112.
17. Gangloff, S., McDonald, J.P., Bendixen, C., Arthur, L. and Rothstein, R. (1994) The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: A potential eukaryotic reverse gyrase. Mol. Cell. Biol., 14, 8391-8398.
18. Gangloff, S., Soustelle, C. and Fabre, F. (2000) Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat. Genet., 25, 192-194.
19. Grummt, I., Roth, E. and Paule, M.R. (1982) Ribosomal RNA transcription in vitro is species specific. Nature, 296, 173-174.
20. Hampsey, M. (1998) Molecular genetics of the RNA polymerase II general transcriptional machinery. Microbiol. Mol. Biol. Rev., 62, 465-503.
21. Hanada, K., Song, C.Z., Yamamoto, K., Yano, K., Maeda, Y., Yamaguchi, K. and 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.
22. Hannan, R.D., Stefanovsky, V., Taylor, L., Moss, T. and Rothblum, L.I. (1996) Overexpression of the transcription factor UBF1 is sufficient to increase ribosomal DNA transcription in neonatal cardiomyocytes: Implications for cardiac hypertrophy. Proc. Natl. Acad. Sci. USA, 93, 8750-8755.
23. Hermann-Le Denmat, S., Werner, M., Sentenac, A. and Thuriaux, P. (1994) Suppression of yeast RNA polymerase III mutations by FHLI, a gene coding for a fork head protein involved in rRNA processing. Mol. Cell. Biol., 14, 2905-2913.
24. Iben, S., Tschochner, H., Bier, M., Hoogstraten, D., Hozak, P., Egly, J.M. and Grummt, I. (2002) TFIIH plays an essential role in RNA polymerase I transcription. Cell, 109, 297-306.
25. Jantzen, H.M., Admon, A., Bell, S.P. and Tjian, R. (1990) Nucleolar transcription factor hUBF contains a DNA-binding motif with homology to HMG proteins. Nature, 344, 830-836.
26. Keener, J., Dodd, J.A., Lalo, D. and Nomura, M. (1997) Histones H3 and H4 are components of upstream activation factor required for the highlevel transcription of yeast rDNA by RNA polymerase I. Proc. Natl. Acad. Sci. USA, 94, 13458-13462.
27. Keys, D.A., Vu, L., Steffan, J.S., Dodd, J.A., Yamamoto, R.T., Nogi, Y. and Nomura, M. (1994) RRN6 and RRN7 encode subunits of a multiprotein complex essential for the initiation of rDNA transcription by RNA polymerase I in Saccharomyces cerevisiae. Genes Dev., 8, 2349-2362.
28. Keys, D.A., Lee, B.S., Dodd, J.A., Nguyen, T.T., Vu, L., Fantino, E., Burson, L.M., Nogi, Y. and Nomura, M. (1996) Multiprotein transcription factor UAF interacts with the upstream element of the yeast RNA polymerase I promoter and forms a stable preinitiation complex. Genes Dev., 10, 887-903.
29. Kretzschmar, M., Meisterernst, M. and Roeder, R.G. (1993) Identification of human DNA topoisomerase I as a cofactor for activator-dependent transcription by RNA polymerase II. Proc. Natl. Acad. Sci. USA, 90, 11508-11512.
30. Kruppa, M., Moir, R.D., Kolodrubetz, D. and Willis, I.M. (2001) Nhp6, an HMG1 protein, functions in SNR6 transcription by RNA polymerase III in S.cerevisiae. Mol. Cell, 7, 309-318.
31. Lalo, D., Steffan, J.S., Dodd, J.A. and Nomura, M. (1996) RRN11 encodes the third subunit of the complex containing Rrn6p and Rrn7p that is essential for the initiation of rDNA transcription by yeast RNA polymerase I. J. Biol. Chem., 271, 21062-21067.
32. Léger-Silvestre, I., Trumtel, S., Noaillac-Depeyre, J. and Gas, N. (1999) Functional compartmentalization of the nucleus in the budding yeast Saccharomyces cerevisiae. Chromosoma, 108, 103-113.
33. Liljelund, P., Mariotte, S., Buhler, J.M. and Sentenac, A. (1992) Characterization and mutagenesis of the gene encoding the A49 subunit of RNA polymerase A in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA, 89, 9302-9305.
34. Longtine, M.S., McKenzie, A., Demarini, D.J., Shah, N.G., Wach, A., Brachat, A., Philippsen, P. and Pringle, J.R. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast, 14, 953-961.
35. Lopez, S., Livingstone-Zatchej, M., Jourdain, S., Thoma, F., Sentenac, A. and Marsolier, M.C. (2001) High-mobility-group proteins NHP6A and NHP6B participate in activation of the RNA polymerase III SNR6 gene. Mol. Cell. Biol., 21, 3096-3104.
36. Lu, J., Kobayashi, R. and Brill, S.J. (1996a) Characterization of a high mobility group 1/2 homolog in yeast. J. Biol. Chem., 271, 33678-33685.
37. Lu, J., Mullen, J.R., Brill, S.J., Kleff, S., Romeo, A.M. and Sternglanz, R. (1996b) Human homologues of yeast helicase. Nature, 383, 678-679.
38. Miller, G., Panov, K.I., Friedrich, J.K., Trinkle-Mulcahy, L., Lamond, A.I. and Zomerdijk, J.C. (2001) hRRN3 is essential in the SL1-mediated recruitment of RNA polymerase I to rRNA gene promoters. EMBO J., 20, 1373-1382.
39. Mitsouras, K., Wong, B., Arayata, C., Johnson, R.C. and Carey, M. (2002) The DNA architectural protein HMGB1 displays two distinct modes of action that promote enhanceosome assembly. Mol. Cell. Biol., 22, 4390-4401.
40. Moorefield, B., Greene, E.A. and Reeder, R.H. (2000) RNA polymerase I transcription factor Rrn3 is functionally conserved between yeast and human. Proc. Natl. Acad. Sci. USA, 97, 4724-4729.
41. Moss, T. and Stefanovsky, V.Y. (2002) At the center of eukaryotic life. Cell, 109, 545-548.
42. Neuvéglise, C., Bon, E., Lepingle, A., Wincker, P., Artiguenave, F., Gaillardin, C. and Casaregola, S. (2000) Genomic exploration of the hemiascomycetous yeasts: 9. Saccharomyces kluyveri. FEBS Lett., 487, 56-60.
43. Nogi, Y., Vu, L. and Nomura, M. (1991) An approach for isolation of mutants defective in 35S ribosomal RNA synthesis in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA, 88, 7026-7030.
44. Nogi, Y., Yano, R., Dodd, J., Carles, C. and Nomura, M. (1993) Gene RRN4 in Saccharomyces cerevisiae encodes the A12.2 subunit of RNA polymerase I and is essential only at high temperatures. Mol. Cell. Biol., 13, 114-122.
45. Nonet, M., Scafe, C., Sexton, J. and Young, R. (1987) Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol. Cell. Biol., 7, 1602-1611.
46. Parisi, M.A., Xu, B. and Clayton, D.A. (1993) A human mitochondrial transcriptional activator can functionally replace a yeast mitochondrial HMG-box protein both in vivo and in vitro. Mol. Cell. Biol., 13, 1951-1961.
47. Paule, M.R. and White, R.J. (2000) Transcription by RNA polymerases I and III. Nucleic Acids Res., 28, 1283-1298.
48. Peyroche, G., Milkereit, P., Bischler, N., Tschochner, H., Schultz, P., Sentenac, A., Carles, C. and 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.
49. Schnapp, A., Pfleiderer, C., Rosenbauer, H. and Grummt, I. (1990) A growth-dependent transcription initiation factor (TIF-IA) interacting with RNA polymerase I regulates mouse ribosomal RNA synthesis. EMBO J., 9, 2857-2863.
50. Schultz, M.C., Reeder, R.H. and Hahn, S. (1992) Variants of the TATA-binding protein can distinguish subsets of RNA polymerase I, II and III promoters. Cell, 69, 697-702.
51. Shykind, B.M., Kim, J., Stewart, L., Champoux, J.J. and Sharp, P.A. (1997) Topoisomerase I enhances TFIID-TFIIA complex assembly during activation of transcription. Genes Dev., 11, 397-407.
52. Sikorski, R.S. and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics, 122, 19-27.
53. Sinclair, D.A. and Guarente, L. (1997) Extrachromosomal rDNA circles - A cause of aging in yeast. Cell, 91, 1033-1042.
54. Smid, A., Riva, M., Bouet, F., Sentenac, A. and Carles, C. (1995) The association of three subunits with yeast RNA polymerase is stabilized by A14. J. Biol. Chem., 270, 13534-13540.
55. Smith, S.D., O'Mahony, D.J., Kinsella, B.T. and Rothblum, L.I. (1993) Transcription from the rat 45S ribosomal DNA promoter does not require the factor UBF. Gene Expr., 3, 229-236.
56. Stettler, S., Chiannilkulchai, N., Hermann-Le Denmat, S., Lalo, D., Lacroute, F., Sentenac, A. and Thuriaux, P. (1993) A general suppressor of RNA polymerase I, II and III mutations in Saccharomyces cerevisiae. Mol. Gen. Genet., 239, 169-176.
57. Stotz, A. and Linder, P. (1990) The ADE2 gene from Saccharomyces cerevisiae: Sequence and new vectors. Gene, 95, 91-98.
58. Thomas, J.O. and Travers, A.A. (2001) HMG1 and 2 and related 'architectural' DNA-binding proteins. Trends Biochem. Sci., 26, 167-174.
59. Thrash, C., Bankier, A.T., Barrell, B.G. and Sternglanz, R. (1985) Cloning, characterization and sequence of the yeast DNA topoisomerase I gene. Proc. Natl. Acad. Sci. USA, 82, 4374-4378.
60. Van Mullem, V., Landrieux, E., Vandenhaute, J. and Thuriaux, P. (2002a) Rpa12p, a conserved RNA polymerase I subunit with two functional domains. Mol. Microbiol., 43, 1105-1113.
61. Van Mullem, V., Wery, M., Werner, M., Vandenhaute, J. and Thuriaux, P. (2002b) The Rpb9 subunit of RNA polymerase II binds transcription factor TFIIE and interferes with the SAGA and elongator histone acetyltransferases. J. Biol. Chem., 277, 10220-10225.
62. Waldron, C. and Lacroute, F. (1975) Effect of growth rate on the amounts of ribosomal and transfer ribonucleic acids in yeast. J. Bacteriol., 122, 855-865.
63. Wood, V. et al. (2002) The genome sequence of Schizosaccharomyces pombe. Nature, 415, 871-880.
64. Woychik, N.A., Lane, W.S. and Young, R.A. (1991) Yeast RNA polymerase II subunit RPB9 is essential for growth at temperature extremes. J. Biol. Chem., 266, 19053-19055.
65. Yamamoto, R.T., Nogi, Y., Dodd, J.A. and Nomura, M. (1996) RRN3 gene of Saccharomyces cerevisiae encodes an essential RNA polymerase I transcription factor which interacts with the polymerase independently of DNA template. EMBO J., 15, 3964-3973.
66. Zomerdijk, J.C., Beckmann, H., Comai, L. and Tjian, R. (1994) Assembly of transcriptionally active RNA polymerase I initiation factor SL1 from recombinant subunits. Science, 266, 2015-2018.