Highly redundant function of multiple AT-rich sequences as core promoter elements in the TATA-less RPS5 promoter of Saccharomyces cerevisiae

Nucleic Acids Research

Volumn 39, Issue 1, 2011, Pages 59-75

  Sugihara, Fuminori ^a,b   Kasahara, Koji ^a   Kokubo, Tetsuro ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

TATA BINDING PROTEIN; TATA BINDING PROTEIN ASSOCIATED FACTOR;

ACCURACY; ARTICLE; AT RICH SEQUENCE; CONTROLLED STUDY; GENE DOSAGE; GENE FUNCTION; GENE IDENTIFICATION; HOMOLOGOUS RECOMBINATION; MOLECULAR RECOGNITION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; TATA BOX; TRANSCRIPTION INITIATION SITE;

EUKARYOTA; METAZOA; SACCHAROMYCES CEREVISIAE;

EID: 78651343432     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq741     Document Type: Article

References (91)

1. Hahn, S. (2004) Structure and mechanism of the RNA polymerase II transcription machinery. Nat. Struct. Mol. Biol., 11, 394-403.
2. Thomas, M.C. and Chiang, C.M. (2006) The general transcription machinery and general cofactors. Crit. Rev. Biochem. Mol. Biol., 41, 105-178.
3. Venters, B.J. and Pugh, B.F. (2009) How eukaryotic genes are transcribed. Crit. Rev. Biochem. Mol. Biol., 44, 117-141.
4. Tora, L. (2002) A unified nomenclature for TATA box binding protein (TBP)-associated factors (TAFs) involved in RNA polymerase II transcription. Genes Dev., 16, 673-675.
5. Ranish, J.A., Yudkovsky, N. and Hahn, S. (1999) Intermediates in formation and activity of the RNA polymerase II preinitiation complex: holoenzyme recruitment and a postrecruitment role for the TATA box and TFIIB. Genes Dev., 13, 49-63.
6. Johnson, K.M., Wang, J., Smallwood, A., Arayata, C. and Carey, M. (2002) TFIID and human mediator coactivator complexes assemble cooperatively on promoter DNA. Genes Dev., 16, 1852-1863.
7. Johnson, K.M. and Carey, M. (2003) Assembly of a mediator/ TFIID/TFIIA complex bypasses the need for an activator. Curr. Biol., 13, 772-777.
8. Lieberman, P.M. and Berk, A.J. (1994) A mechanism for TAFs in transcriptional activation: activation domain enhancement of TFIID-TFIIA-promoter DNA complex formation. Genes Dev., 8, 995-1006.
9. Chi, T., Lieberman, P., Ellwood, K. and Carey, M. (1995) A general mechanism for transcriptional synergy by eukaryotic activators. Nature, 377, 254-257.
10. Matangkasombut, O., Auty, R. and Buratowski, S. (2004) Structure and function of the TFIID complex. Adv. Protein Chem., 67, 67-92.
11. 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.
12. Kim, J. and Iyer, V.R. (2004) Global role of TATA box-binding protein recruitment to promoters in mediating gene expression profiles. Mol. Cell. Biol., 24, 8104-8112.
13. Basehoar, A.D., Zanton, S.J. and Pugh, B.F. (2004) Identification and distinct regulation of yeast TATA box-containing genes. Cell, 116, 699-709.
14. Gershenzon, N.I. and Ioshikhes, I.P. (2005) Synergy of human Pol II core promoter elements revealed by statistical sequence analysis. Bioinformatics, 21, 1295-1300.
15. Jin, V.X., Singer, G.A., Agosto-Perez, F.J., Liyanarachchi, S. and Davuluri, R.V. (2006) Genome-wide analysis of core promoter elements from conserved human and mouse orthologous pairs. BMC Bioinformatics, 7, 114.
16. Yang, C., Bolotin, E., Jiang, T., Sladek, F.M. and Martinez, E. (2007) Prevalence of the initiator over the TATA box in human and yeast genes and identification of DNA motifs enriched in human TATA-less core promoters. Gene, 389, 52-65.
17. Huisinga, K.L. and Pugh, B.F. (2004) A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae. Mol. Cell, 13, 573-585.
18. Van Werven, F.J., Van Teeffelen, H.A., Holstege, F.C. and Timmers, H.T. (2009) Distinct promoter dynamics of the basal transcription factor TBP across the yeast genome. Nat. Struct. Mol. Biol., 16, 1043-1048.
19. Morachis, J.M., Murawsky, C.M. and Emerson, B.M. (2010) Regulation of the p53 transcriptional response by structurally diverse core promoters. Genes Dev., 24, 135-147.
20. Smale, S.T. and Kadonaga, J.T. (2003) The RNA polymerase II core promoter. Annu. Rev. Biochem, 72, 449-479.
21. Sandelin, A., Carninci, P., Lenhard, B., Ponjavic, J., Hayashizaki, Y. and Hume, D.A. (2007) Mammalian RNA polymerase II core promoters: insights from genome-wide studies. Nat. Rev. Genet., 8, 424-436.
22. Juven-Gershon, T., Hsu, J.Y., Theisen, J.W. and Kadonaga, J.T. (2008) The RNA polymerase II core promoter - the gateway to transcription. Curr. Opin. Cell. Biol., 20, 253-259.
23. Anish, R., Hossain, M.B., Jacobson, R.H. and Takada, S. (2009) Characterization of transcription from TATA-less promoters: identification of a new core promoter element XCPE2 and analysis of factor requirements. PLoS One, 4, e5103.
24. Yarden, G., Elfakess, R., Gazit, K. and Dikstein, R. (2009) Characterization of sINR, a strict version of the Initiator core promoter element. Nucleic Acids Res., 37, 4234-4246.
25. Ohler, U. and Wassarman, D.A. (2010) Promoting developmental transcription. Development, 137, 15-26.
26. Theisen, J.W., Lim, C.Y. and Kadonaga, J.T. (2010) Three key subregions contribute to the function of the downstream RNA polymerase II core promoter. Mol. Cell. Biol., 30, 3471-3479.
27. Butler, J.E. and Kadonaga, J.T. (2001) Enhancer-promoter specificity mediated by DPE or TATA core promoter motifs. Genes Dev., 15, 2515-2519.
28. Ohtsuki, S., Levine, M. and Cai, H.N. (1998) Different core promoters possess distinct regulatory activities in the Drosophila embryo. Genes Dev., 12, 547-556.
29. Juven-Gershon, T., Hsu, J.Y. and Kadonaga, J.T. (2008) Caudal, a key developmental regulator, is a DPE-specific transcriptional factor. Genes Dev., 22, 2823-2830.
30. Sengupta, T., Cohet, N., Morle, F. and Bieker, J.J. (2009) Distinct modes of gene regulation by a cell-specific transcriptional activator. Proc. Natl Acad. Sci. USA, 106, 4213-4218.
31. Struhl, K. (1986) Constitutive and inducible Saccharomyces cerevisiae promoters: evidence for two distinct molecular mechanisms. Mol. Cell. Biol., 6, 3847-3853.
32. Harbury, P.A. and Struhl, K. (1989) Functional distinctions between yeast TATA elements. Mol. Cell. Biol., 9, 5298-5304.
33. Tsukihashi, Y., Kawaichi, M. and Kokubo, T. (2001) Requirement for yeast TAF145 function in transcriptional activation of the RPS5 promoter that depends on both core promoter structure and upstream activating sequences. J. Biol. Chem., 276, 25715-25726.
34. Cheng, J.X., Floer, M., Ononaji, P., Bryant, G. and Ptashne, M. (2002) Responses of four yeast genes to changes in the transcriptional machinery are determined by their promoters. Curr. Biol., 12, 1828-1832.
35. 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.
36. Li, X.Y., Bhaumik, S.R., Zhu, X., Li, L., Shen, W.C., Dixit, B.L. and Green, M.R. (2002) Selective recruitment of TAFs by yeast upstream activating sequences. Implications for eukaryotic promoter structure. Curr. Biol., 12, 1240-1244.
37. Zhong, P. and Melcher, K. (2010) Identification and characterization of the activation domain of Ifh1, an activator of model TATA-less genes. Biochem. Biophys. Res. Commun., 392, 77-82.
38. Chen, W. and Struhl, K. (1988) Saturation mutagenesis of a yeast his3 "TATA element": genetic evidence for a specific TATA-binding protein. Proc. Natl Acad. Sci. USA, 85, 2691-2695.
39. Hahn, S., Buratowski, S., Sharp, P.A. and Guarente, L. (1989) Yeast TATA-binding protein TFIID binds to TATA elements with both consensus and nonconsensus DNA sequences. Proc. Natl Acad. Sci. USA, 86, 5718-5722.
40. Stewart, J.J., Fischbeck, J.A., Chen, X. and Stargell, L.A. (2006) Non-optimal TATA elements exhibit diverse mechanistic consequences. J. Biol. Chem., 281, 22665-22673.
41. Chen, W. and Struhl, K. (1985) Yeast mRNA initiation sites are determined primarily by specific sequences, not by the distance from the TATA element. EMBO J., 4, 3273-3280.
42. Nagawa, F. and Fink, G.R. (1985) The relationship between the "TATA"sequence and transcription initiation sites at the HIS4 gene of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 82, 8557-8561.
43. Hahn, S., Hoar, E.T. and Guarente, L. (1985) Each of three "TATA elements"specifies a subset of the transcription initiation sites at the CYC-1 promoter of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 82, 8562-8566.
44. McNeil, J.B. and Smith, M. (1986) Transcription initiation of the Saccharomyces cerevisiae iso-1-cytochrome c gene. Multiple, independent T-A-T-A sequences. J. Mol. Biol., 187, 363-378.
45. Mosch, H.U., Graf, R. and Braus, G.H. (1992) Sequence-specific initiator elements focus initiation of transcription to distinct sites in the yeast TRP4 promoter. EMBO J., 11, 4583-4590.
46. Ohishi-Shofuda, T., Suzuki, Y., Yano, K., Sakurai, H. and Fukasawa, T. (1999) Transcription initiation mediated by initiator binding protein in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun., 255, 157-163.
47. 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.
48. Chalkley, G.E. and Verrijzer, C.P. (1999) DNA binding site selection by RNA polymerase II TAFs: a TAF(II)250- TAF(II)150 complex recognizes the initiator. EMBO J., 18, 4835-4845.
49. Struhl, K. (1989) Molecular mechanisms of transcriptional regulation in yeast. Annu. Rev. Biochem., 58, 1051-1077.
50. Juven-Gershon, T., Cheng, S. and Kadonaga, J.T. (2006) Rational design of a super core promoter that enhances gene expression. Nat. Methods, 3, 917-922.
51. Lee, D.H., Gershenzon, N., Gupta, M., Ioshikhes, I.P., Reinberg, D. and Lewis, B.A. (2005) Functional characterization of core promoter elements: the downstream core element is recognized by TAF1. Mol. Cell. Biol., 25, 9674-9686.
52. Singer, V.L., Wobbe, C.R. and Struhl, K. (1990) A wide variety of DNA sequences can functionally replace a yeast TATA element for transcriptional activation. Genes Dev., 4, 636-645.
53. Mahadevan, S. and Struhl, K. (1990) Tc, an unusual promoter element required for constitutive transcription of the yeast HIS3 gene. Mol. Cell. Biol., 10, 4447-4455.
54. Iyer, V. and Struhl, K. (1995) Mechanism of differential utilization of the his3 TR and TC TATA elements. Mol. Cell. Biol., 15, 7059-7066.
55. Shen, W.C. and Green, M.R. (1997) Yeast TAF(II)145 functions as a core promoter selectivity factor, not a general coactivator. Cell, 90, 615-624.
56. Sanders, S.L., Garbett, K.A. and Weil, P.A. (2002) Molecular characterization of Saccharomyces cerevisiae TFIID. Mol. Cell. Biol., 22, 6000-6013.
57. Shen, W.C., Bhaumik, S.R., Causton, H.C., Simon, I., Zhu, X., Jennings, E.G., Wang, T.H., Young, R.A. and Green, M.R. (2003) Systematic analysis of essential yeast TAFs in genome-wide transcription and preinitiation complex assembly. EMBO J., 22, 3395-3402.
58. 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.
59. Longtine, M.S., McKenzie, A. 3rd, 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.
60. Kitazono, A.A., Tobe, B.T., Kalton, H., Diamant, N. and Kron, S.J. (2002) Marker-fusion PCR for one-step mutagenesis of essential genes in yeast. Yeast, 19, 141-149.
61. 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.
62. Takahata, S., Ryu, H., Ohtsuki, K., Kasahara, K., Kawaichi, M. and Kokubo, T. (2003) Identification of a novel TATA element-binding protein binding region at the N terminus of the Saccharomyces cerevisiae TAF1 protein. J. Biol. Chem., 278, 45888-45902.
63. 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.
64. 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.
65. 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.
66. 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.
67. 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.
68. Zhao, Y., McIntosh, K.B., Rudra, D., Schawalder, S., Shore, D. and Warner, J.R. (2006) Fine-structure analysis of ribosomal protein gene transcription. Mol. Cell. Biol., 26, 4853-4862.
69. Rudra, D., Mallick, J., Zhao, Y. and Warner, J.R. (2007) Potential interface between ribosomal protein production and pre-rRNA processing. Mol. Cell. Biol., 27, 4815-4824.
70. Gordan, R., Hartemink, A.J. and Bulyk, M.L. (2009) Distinguishing direct versus indirect transcription factor-DNA interactions. Genome Res., 19, 2090-2100.
71. Hothorn, M., Neumann, H., Lenherr, E.D., Wehner, M., Rybin, V., Hassa, P.O., Uttenweiler, A., Reinhardt, M., Schmidt, A., Seiler, J. et al. (2009) Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science, 324, 513-516.
72. Ki, S., Sugihara, F., Kasahara, K., Tochio, H., Okada-Marubayashi, A., Tomita, S., Morita, M., Ikeguchi, M., Shirakawa, M. and Kokubo, T. (2006) A novel magnetic resonance-based method to measure gene expression in living cells. Nucleic Acids Res., 34, e51.
73. 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.
74. Harbison, C.T., Gordon, D.B., Lee, T.I., Rinaldi, N.J., Macisaac, K.D., Danford, T.W., Hannett, N.M., Tagne, J.B., Reynolds, D.B., Yoo, J. et al. (2004) Transcriptional regulatory code of a eukaryotic genome. Nature, 431, 99-104.
75. Lascaris, R.F., Mager, W.H. and Planta, R.J. (1999) DNA-binding requirements of the yeast protein Rap1p as selected in silico from ribosomal protein gene promoter sequences. Bioinformatics, 15, 267-277.
76. 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.
77. Giardina, C. and Lis, J.T. (1993) DNA melting on yeast RNA polymerase II promoters. Science, 261, 759-762.
78. Hampsey, M. (2006) The Pol II initiation complex: finding a place to start. Nat. Struct. Mol. Biol., 13, 564-566.
79. Zhang, Z. and Dietrich, F.S. (2005) Mapping of transcription start sites in Saccharomyces cerevisiae using 50 SAGE. Nucleic Acids Res., 33, 2838-2851.
80. Faitar, S.L., Brodie, S.A. and Ponticelli, A.S. (2001) Promoter-specific shifts in transcription initiation conferred by yeast TFIIB mutations are determined by the sequence in the immediate vicinity of the start sites. Mol. Cell. Biol., 21, 4427-4440.
81. Bhaumik, S.R. and Green, M.R. (2002) Differential requirement of SAGA components for recruitment of TATA-box-binding protein to promoters in vivo. Mol. Cell. Biol., 22, 7365-7371.
82. Shukla, A., Bajwa, P. and Bhaumik, S.R. (2006) SAGA-associated Sgf73p facilitates formation of the preinitiation complex assembly at the promoters either in a HAT-dependent or independent manner in vivo. Nucleic Acids Res., 34, 6225-6232.
83. Li, X.Y., Bhaumik, S.R. and Green, M.R. (2000) Distinct classes of yeast promoters revealed by differential TAF recruitment. Science, 288, 1242-1244.
84. Li, X.Y., Virbasius, A., Zhu, X. and Green, M.R. (1999) Enhancement of TBP binding by activators and general transcription factors. Nature, 399, 605-609.
85. Moqtaderi, Z., Keaveney, M. and Struhl, K. (1998) The histone H3-like TAF is broadly required for transcription in yeast. Mol. Cell, 2, 675-682.
86. Spencer, J.V. and Arndt, K.M. (2002) A TATA binding protein mutant with increased affinity for DNA directs transcription from a reversed TATA sequence in vivo. Mol. Cell. Biol., 22, 8744-8755.
87. Cox, J.M., Hayward, M.M., Sanchez, J.F., Gegnas, L.D., Van der Zee, S., Dennis, J.H., Sigler, P.B. and Schepartz, A. (1997) Bidirectional binding of the TATA box binding protein to the TATA box. Proc. Natl Acad. Sci. USA, 94, 13475-13480.
88. Kays, A.R. and Schepartz, A. (2002) Gal4-VP16 and Gal4-AH increase the orientational and axial specificity of TATA box recognition by TATA box binding protein. Biochemistry, 41, 3147-3155.
89. Jiang, C. and Pugh, B.F. (2009) Nucleosome positioning and gene regulation: advances through genomics. Nat. Rev. Genet., 10, 161-172.
90. Segal, E. and Widom, J. (2009) Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr. Opin. Struct. Biol., 19, 65-71.
91. Yarragudi, A., Miyake, T., Li, R. and Morse, R.H. (2004) Comparison of ABF1 and RAP1 in chromatin opening and transactivator potentiation in the budding yeast Saccharomyces cerevisiae. Mol. Cell. Biol., 24, 9152-9164.