Hmo1 directs pre-initiation complex assembly to an appropriate site on its target gene promoters by masking a nucleosome-free region

Nucleic Acids Research

Volumn 39, Issue 10, 2011, Pages 4136-4150

  Kasahara, Koji ^a   Ohyama, Yoshifumi ^a   Kokubo, Tetsuro ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP B PROTEIN; PROTEIN HMO1; UNCLASSIFIED DRUG; HIGH MOBILITY GROUP PROTEIN; HMO1 PROTEIN, S CEREVISIAE; RIBOSOMAL PROTEIN S5; RIBOSOME PROTEIN; RNA POLYMERASE II; RPB1 PROTEIN, S CEREVISIAE; RPB9 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR II; TRANSCRIPTION FACTOR TFIIF;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; GENE; GENE SEQUENCE; INTERVENING REGION; NONHUMAN; NUCLEOSOME; PREINITIATION COMPLEX; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; RIBOSOMAL PROTEIN GENE; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION INITIATION SITE; UPSTREAM ACTIVATING SEQUENCE; GENE DELETION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION;

SACCHAROMYCES CEREVISIAE;

GENE DELETION; HIGH MOBILITY GROUP PROTEINS; MUTATION; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; RIBOSOMAL PROTEINS; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS, TFII; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

EID: 79961179258     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq1334     Document Type: Article

References (64)

1. Warner, J.R. (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci., 24, 437-440. (Pubitemid 29528205)
2. Kasahara, K., Ohtsuki, K., Ki, S., Aoyama, K., Takahashi, H., Kobayashi, T., Shirahige, K. and Kokubo, T. (2007) Assembly of regulatory factors on rRNA and ribosomal protein genes in Saccharomyces cerevisiae. Mol. Cell. Biol., 27, 6686-6705. (Pubitemid 47483622)
3. Lieb, J.D., Liu, X., Botstein, D. and Brown, P.O. (2001) Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association. Nat. Genet., 28, 327-334. (Pubitemid 32702421)
4. Garbett, K.A., Tripathi, M.K., Cencki, B., Layer, J.H. and Weil, P.A. (2007) Yeast TFIID serves as a coactivator for Rap1p by direct protein-protein interaction. Mol. Cell. Biol., 27, 297-311. (Pubitemid 46013252)
5. Reid, J.L., Iyer, V.R., Brown, P.O. and Struhl, K. (2000) Coordinate regulation of yeast ribosomal protein genes is associated with targeted recruitment of Esa1 histone acetylase. Mol. Cell, 6, 1297-1307. (Pubitemid 32045923)
6. Pina, B., Fernandez-Larrea, J., Garcia-Reyero, N. and Idrissi, F.Z. (2003) The different (sur)faces of Rap1p. Mol. Genet. Genomics, 268, 791-798. (Pubitemid 36458024)
7. Bernstein, B.E., Liu, C.L., Humphrey, E.L., Perlstein, E.O. and Schreiber, S.L. (2004) Global nucleosome occupancy in yeast. Genome Biol., 5, R62.
8. Yu, L. and Morse, R.H. (1999) Chromatin opening and transactivator potentiation by RAP1 in Saccharomyces cerevisiae. Mol. Cell. Biol., 19, 5279-5288. (Pubitemid 29339887)
9. Lascaris, R.F., Groot, E., Hoen, P.B., Mager, W.H. and Planta, R.J. (2000) Different roles for abf1p and a T-rich promoter element in nucleosome organization of the yeast RPS28A gene. Nucleic Acids Res., 28, 1390-1396. (Pubitemid 30142682)
10. Hartley, P.D. and Madhani, H.D. (2009) Mechanisms that specify promoter nucleosome location and identity. Cell, 137, 445-458.
11. Wade, J.T., Hall, D.B. and Struhl, K. (2004) The transcription factor Ifh1 is a key regulator of yeast ribosomal protein genes. Nature, 432, 1054-1058. (Pubitemid 40052239)
12. Schawalder, S.B., Kabani, M., Howald, I., Choudhury, U., Werner, M. and Shore, D. (2004) Growth-regulated recruitment of the essential yeast ribosomal protein gene activator Ifh1. Nature, 432, 1058-1061. (Pubitemid 40052240)
13. Martin, D.E., Soulard, A. and Hall, M.N. (2004) TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell, 119, 969-979. (Pubitemid 40037610)
14. Rudra, D., Zhao, Y. and Warner, J.R. (2005) Central role of Ifh1p-Fhl1p interaction in the synthesis of yeast ribosomal proteins. EMBO J., 24, 533-542. (Pubitemid 40343255)
15. Fingerman, I., Nagaraj, V., Norris, D. and Vershon, A.K. (2003) Sfp1 plays a key role in yeast ribosome biogenesis. Eukaryot. Cell, 2, 1061-1068. (Pubitemid 37298720)
16. Jorgensen, P., Rupes, I., Sharom, J.R., Schneper, L., Broach, J.R. and Tyers, M. (2004) A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev., 18, 2491-2505. (Pubitemid 39362892)
17. Marion, R.M., Regev, A., Segal, E., Barash, Y., Koller, D., Friedman, N. and O'Shea, E.K. (2004) Sfp1 is a stress-and nutrient-sensitive regulator of ribosomal protein gene expression. Proc. Natl Acad. Sci. USA, 101, 14315-14322. (Pubitemid 39346746)
18. Gadal, O., Labarre, S., Boschiero, C. and Thuriaux, P. (2002) Hmo1, an HMG-box protein, belongs to the yeast ribosomal DNA transcription system. EMBO J., 21, 5498-5507. (Pubitemid 35231029)
19. Alekseev, S.Y., Kovaltsova, S.V., Fedorova, I.V., Gracheva, L.M., Evstukhina, T.A., Peshekhonov, V.T. and Korolev, V.G. (2002) HSM2 (HMO1) gene participates in mutagenesis control in yeast Saccharomyces cerevisiae. DNA Repair, 1, 287-297. (Pubitemid 38340225)
20. Berger, A.B., Decourty, L., Badis, G., Nehrbass, U., Jacquier, A. and Gadal, O. (2007) Hmo1 is required for TOR-dependent regulation of ribosomal protein gene transcription. Mol. Cell. Biol., 27, 8015-8026. (Pubitemid 350086433)
21. Bermejo, R., Capra, T., Gonzalez-Huici, V., Fachinetti, D., Cocito, A., Natoli, G., Katou, Y., Mori, H., Kurokawa, K., Shirahige, K. et al. (2009) Genome-organizing factors Top2 and Hmo1 prevent chromosome fragility at sites of S phase transcription. Cell, 138, 870-884.
22. Hall, D.B., Wade, J.T. and Struhl, K. (2006) An HMG protein, Hmo1, associates with promoters of many ribosomal protein genes and throughout the rRNA gene locus in Saccharomyces cerevisiae. Mol. Cell. Biol., 26, 3672-3679.
23. Kasahara, K., Ki, S., Aoyama, K., Takahashi, H. and Kokubo, T. (2008) Saccharomyces cerevisiae HMO1 interacts with TFIID and participates in start site selection by RNA polymerase II. Nucleic Acids Res., 36, 1343-1357. (Pubitemid 351330949)
24. Kim, H. and Livingston, D.M. (2009) Suppression of a DNA polymerase delta mutation by the absence of the high mobility group protein Hmo1 in Saccharomyces cerevisiae. Curr. Genet., 55, 127-138.
25. Lu, J., Kobayashi, R. and Brill, S.J. (1996) Characterization of a high mobility group 1/2 homolog in yeast. J. Biol. Chem., 271, 33678-33685.
26. Merz, K., Hondele, M., Goetze, H., Gmelch, K., Stoeckl, U. and Griesenbeck, J. (2008) Actively transcribed rRNA genes in S. cerevisiae are organized in a specialized chromatin associated with the high-mobility group protein Hmo1 and are largely devoid of histone molecules. Genes Dev., 22, 1190-1204. (Pubitemid 351656578)
27. Goetze, H., Wittner, M., Hamperl, S., Hondele, M., Merz, K., Stoeckl, U. and Griesenbeck, J. (2010) Alternative chromatin structures of the 35S rRNA genes in Saccharomyces cerevisiae provide a molecular basis for the selective recruitment of RNA polymerases I and II. Mol. Cell. Biol., 30, 2028-2045.
28. Goncalves, P.M., Griffioen, G., Minnee, R., Bosma, M., Kraakman, L.S., Mager, W.H. and Planta, R.J. (1995) Transcription activation of yeast ribosomal protein genes requires additional elements apart from binding sites for Abf1p or Rap1p. Nucleic Acids Res., 23, 1475-1480.
29. Mencia, M., Moqtaderi, Z., Geisberg, J.V., Kuras, L. and Struhl, K. (2002) Activator-specific recruitment of TFIID and regulation of ribosomal protein genes in yeast. Mol. Cell, 9, 823-833. (Pubitemid 34454892)
30. Khaperskyy, D.A., Ammerman, M.L., Majovski, R.C. and Ponticelli, A.S. (2008) Functions of Saccharomyces cerevisiae TFIIF during transcription start site utilization. Mol. Cell. Biol., 28, 3757-3766. (Pubitemid 351732910)
31. Ghazy, M.A., Brodie, S.A., Ammerman, M.L., Ziegler, L.M. and Ponticelli, A.S. (2004) Amino acid substitutions in yeast TFIIF confer upstream shifts in transcription initiation and altered interaction with RNA polymerase II. Mol. Cell. Biol., 24, 10975-10985. (Pubitemid 39603151)
32. Freire-Picos, M.A., Krishnamurthy, S., Sun, Z.W. and Hampsey, M. (2005) Evidence that the Tfg1/Tfg2 dimer interface of TFIIF lies near the active center of the RNA polymerase II initiation complex. Nucleic Acids Res., 33, 5045-5052. (Pubitemid 41487812)
33. Sun, Z.W. and Hampsey, M. (1995) Identification of the gene (SSU71/TFG1) encoding the largest subunit of transcription factor TFIIF as a suppressor of a TFIIB mutation in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA., 92, 3127-3131.
34. Chen, B.S. and Hampsey, M. (2004) Functional interaction between TFIIB and the Rpb2 subunit of RNA polymerase II: implications for the mechanism of transcription initiation. Mol. Cell. Biol., 24, 3983-3991. (Pubitemid 38496175)
35. Ziegler, L.M., Khaperskyy, D.A., Ammerman, M.L. and Ponticelli, A.S. (2003) Yeast RNA polymerase II lacking the Rpb9 subunit is impaired for interaction with transcription factor IIF. J. Biol. Chem., 278, 48950-48956.
36. Sun, Z.W., Tessmer, A. and Hampsey, M. (1996) Functional interaction between TFIIB and the Rpb9 (Ssu73) subunit of RNA polymerase II in Saccharomyces cerevisiae. Nucleic Acids Res., 24, 2560-2566. (Pubitemid 26237155)
37. Hull, M.W., McKune, K. and Woychik, N.A. (1995) RNA polymerase II subunit RPB9 is required for accurate start site selection. Genes Dev., 9, 481-490.
38. Chen, Z.A., Jawhari, A., Fischer, L., Buchen, C., Tahir, S., Kamenski, T., Rasmussen, M., Lariviere, L., Bukowski-Wills, J.C., Nilges, M. et al. (2010) Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry. EMBO J., 29, 717-726.
39. Eichner, J., Chen, H.T., Warfield, L. and Hahn, S. (2010) Position of the general transcription factor TFIIF within the RNA polymerase II transcription preinitiation complex. EMBO J., 29, 706-716.
40. Amberg, D.C., Burke, D.J. and Strathern, J.N. (2005) Methods in Yeast Genetics: a Cold Spring Harbor Laboratory Course Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Kasahara, K., Kawaichi, M. and Kokubo, T. (2004) In vivo synthesis of Taf1p lacking the TAF N-terminal domain using alternative transcription or translation initiation sites. Genes Cells, 9, 709-721. (Pubitemid 39206611)
42. Berroteran, R.W., Ware, D.E. and Hampsey, M. (1994) The sua8 suppressors of Saccharomyces cerevisiae encode replacements of conserved residues within the largest subunit of RNA polymerase II and affect transcription start site selection similarly to sua7 (TFIIB) mutations. Mol. Cell. Biol., 14, 226-237.
43. Majovski, R.C., Khaperskyy, D.A., Ghazy, M.A. and Ponticelli, A.S. (2005) A functional role for the switch 2 region of yeast RNA polymerase II in transcription start site utilization and abortive initiation. J. Biol. Chem., 280, 34917-34923. (Pubitemid 41504626)
44. Giardina, C. and Lis, J.T. (1993) DNA melting on yeast RNA polymerase II promoters. Science, 261, 759-762. (Pubitemid 23278391)
45. Kuehner, J.N. and Brow, D.A. (2006) Quantitative analysis of in vivo initiator selection by yeast RNA polymerase II supports a scanning model. J. Biol. Chem., 281, 14119-14128. (Pubitemid 43848339)
46. Hampsey, M. (2006) The Pol II initiation complex: finding a place to start. Nat. Struct. Mol. Biol., 13, 564-566. (Pubitemid 44036462)
47. Tsukihashi, Y., Miyake, T., Kawaichi, M. and Kokubo, T. (2000) Impaired core promoter recognition caused by novel yeast TAF145 mutations can be restored by creating a canonical TATA element within the promoter region of the TUB2 gene. Mol. Cell. Biol., 20, 2385-2399. (Pubitemid 30152047)
48. Mavrich, T.N., Ioshikhes, I.P., Venters, B.J., Jiang, C., Tomsho, L.P., Qi, J., Schuster, S.C., Albert, I. and Pugh, B.F. (2008) A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res., 18, 1073-1083. (Pubitemid 351931158)
49. Jiang, C. and Pugh, B.F. (2009) Nucleosome positioning and gene regulation: advances through genomics. Nat. Rev. Genet., 10, 161-172.
50. Venters, B.J. and Pugh, B.F. (2009) How eukaryotic genes are transcribed. Crit. Rev. Biochem. Mol. Biol., 44, 117-141.
51. Sugihara, F., Kasahara, K. and Kokubo, T. (2010) Highly redundant function of multiple AT-rich sequences as core promoter elements in the TATA-less RPS5 promoter of Saccharomyces cerevisiae. Nucleic Acids Res., 39, 59-75.
52. Lavoie, H., Hogues, H., Mallick, J., Sellam, A., Nantel, A. and Whiteway, M. (2010) Evolutionary tinkering with conserved components of a transcriptional regulatory network. PLoS Biol., 8, e1000329.
53. Kim, H. and Livingston, D.M. (2006) A high mobility group protein binds to long CAG repeat tracts and establishes their chromatin organization in Saccharomyces cerevisiae. J. Biol. Chem., 281, 15735-15740. (Pubitemid 43848462)
54. Winston, F., Dollard, C., Malone, E.A., Clare, J., Kapakos, J.G., Farabaugh, P. and Minehart, P.L. (1987) Three genes are required for trans-activation of Ty transcription in yeast. Genetics, 115, 649-656.
55. Winston, F., Chaleff, D.T., Valent, B. and Fink, G.R. (1984) Mutations affecting Ty-mediated expression of the HIS4 gene of Saccharomyces cerevisiae. Genetics, 107, 179-197. (Pubitemid 14079516)
56. Fassler, J.S. and Winston, F. (1988) Isolation and analysis of a novel class of suppressor of Ty insertion mutations in Saccharomyces cerevisiae. Genetics, 118, 203-212.
57. Nourani, A., Robert, F. and Winston, F. (2006) Evidence that Spt2/Sin1, an HMG-like factor, plays roles in transcription elongation, chromatin structure, and genome stability in Saccharomyces cerevisiae. Mol. Cell. Biol., 26, 1496-1509. (Pubitemid 43202573)
58. Cheung, V., Chua, G., Batada, N.N., Landry, C.R., Michnick, S.W., Hughes, T.R. and Winston, F. (2008) Chromatin-and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol., 6, e277.
59. Belotserkovskaya, R. and Reinberg, D. (2004) Facts about FACT and transcript elongation through chromatin. Curr. Opin. Genet. Dev., 14, 139-146. (Pubitemid 38520141)
60. Shykind, B.M., Kim, J. and Sharp, P.A. (1995) Activation of the TFIID-TFIIA complex with HMG-2. Genes Dev., 9, 1354-1365.
61. Paull, T.T., Carey, M. and Johnson, R.C. (1996) Yeast HMG proteins NHP6A/B potentiate promoter-specific transcriptional activation in vivo and assembly of preinitiation complexes in vitro. Genes Dev., 10, 2769-2781. (Pubitemid 26384496)
62. Xiao, L., Williams, A.M. and Grove, A. (2010) The C-terminal domain of yeast high mobility group protein HMO1 mediates lateral protein accretion and in-phase DNA bending. Biochemistry, 49, 4051-4059.
63. Papai, G., Tripathi, M.K., Ruhlmann, C., Layer, J.H., Weil, P.A. and Schultz, P. (2010) TFIIA and the transactivator Rap1 cooperate to commit TFIID for transcription initiation. Nature, 465, 956-960.
64. Kang, J.J., Auble, D.T., Ranish, J.A. and Hahn, S. (1995) Analysis of the yeast transcription factor TFIIA: distinct functional regions and a polymerase II-specific role in basal and activated transcription. Mol. Cell. Biol., 15, 1234-1243.