Core promoter sequence in yeast is a major determinant of expression level

Genome Research

Volumn 25, Issue 7, 2015, Pages 1008-1017

  Lubliner, Shai ^a   Regev, Ifat ^a   Lotan Pompan, Maya ^a   Edelheit, Sarit ^a   Weinberger, Adina ^a   Segal, Eran ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

POLY(DEOXYADENYLATE DEOXYTHYMIDYLATE); TATA BINDING PROTEIN;

ARTICLE; DNA FLANKING REGION; FUNGAL GENE; GENE CONTROL; GENE EXPRESSION; GENE LOCATION; GENE SEQUENCE; GENETIC VARIABILITY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE STUDY; SACCHAROMYCES; TRANSCRIPTION INITIATION; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; TATA BOX; TRANSCRIPTION INITIATION SITE; YEAST;

GENE EXPRESSION REGULATION, FUNGAL; GENOMICS; PROMOTER REGIONS, GENETIC; TATA BOX; TRANSCRIPTION INITIATION SITE; TRANSCRIPTIONAL ACTIVATION; YEASTS;

EID: 84937033956     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.188193.114     Document Type: Article

References (43)

1. Aow JSZ, Xue X, Run J-Q, Lim GFS, Goh WS, Clarke ND. 2013. Differential binding of the related transcription factors Pho4 and Cbf1 can tune the sensitivity of promoters to different levels of an induction signal. Nucleic Acids Res 41: 4877-4887.
2. Basehoar AD, Zanton SJ, Pugh BF. 2004. Identification and distinct regulation of yeast TATA box-containing genes. Cell 116: 699-709.
3. Bushnell DA, Westover KD, Davis RE, Kornberg RD. 2004. Structural basis of transcription: an RNA polymerase II-TFIIB cocrystal at 4.5 Angstroms. Science 303: 983-988.
4. Chen W, Struhl K. 1988. Saturation mutagenesis of a yeast his3 "TATA element": genetic evidence for a specific TATA-binding protein. Proc Natl Acad Sci 85: 2691-2695.
5. Dvir S, Velten L, Sharon E, Zeevi D, Carey LB, Weinberger A, Segal E. 2013. Deciphering the rules by which 5′-UTR sequences affect protein expression in yeast. Proc Natl Acad Sci 110: E2792-E2801.
6. Faitar SL, Brodie SA, Ponticelli AS. 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.
7. Field Y, Kaplan N, Fondufe-Mittendorf Y, Moore IK, Sharon E, Lubling Y, Widom J, Segal E. 2008. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput Biol 4: e1000216.
8. Fishburn J, Hahn S. 2012. Architecture of the yeast RNA polymerase II open complex and regulation of activity by TFIIF. Mol Cell Biol 32: 12-25.
9. Furter-Graves EM, Hall BD. 1990. DNA sequence elements required for transcription initiation of the Schizosaccharomyces pombe ADH gene in Saccharomyces cerevisiae. Mol Gen Genet 223: 407-416.
10. Giardina C, Lis JT. 1993. DNA melting on yeast RNA polymerase II promoters. Science 261: 759-762.
11. Goel S, Krishnamurthy S, Hampsey M. 2012. Mechanism of start site selection by RNA polymerase II: interplay between TFIIB and Ssl2/XPB helicase subunit of TFIIH. J Biol Chem 287: 557-567.
12. Gordân R, Shen N, Dror I, Zhou T, Horton J, Rohs R, Bulyk ML. 2013. Genomic regions flanking E-box binding sites influence DNA binding specificity of bHLH transcription factors through DNA shape. Cell Rep 3: 1093-1104.
13. Hahn S, Hoar ET, 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 82: 8562-8566.
14. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, LeProust EM, Hughes TR, Lieb JD, Widom J, et al. 2009. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458: 362-366.
15. Keren L, Zackay O, Lotan-Pompan M, Barenholz U, Dekel E, Sasson V, Aidelberg G, Bren A, Zeevi D, Weinberger A, et al. 2013. Promoters maintain their relative activity levels under different growth conditions. Mol Syst Biol 9: 701.
16. Kuehner JN, Brow DA. 2006. Quantitative analysis of in vivo initiator selection by yeast RNA polymerase II supports a scanning model. J Biol Chem 281: 14119-14128.
17. LeProust EM, Peck BJ, Spirin K, McCuen HB, Moore B, Namsaraev E, Caruthers MH. 2010. Synthesis of high-quality libraries of long (150mer) oligonucleotides by a novel depurination controlled process. Nucleic Acids Res 38: 2522-2540.
18. Levo M, Segal E. 2014. In pursuit of design principles of regulatory sequences. Nat Rev Genet 15: 453-468.
19. Levo M, Zalckvar E, Sharon E, Dantas Machado AC, Kalma Y, Lotam-Pompan M, Weinberger A, Yakhini Z, Rohs R, Segal E. 2015. Unraveling determinants of transcription factor binding outside the core binding site. Genome Res (this issue). doi: 10.1101/gr.185033.114.
20. Lieb JD, Liu X, Botstein D, Brown PO. 2001. Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association. Nat Genet 28: 327-334.
21. Lubliner S, Keren L, Segal E. 2013. Sequence features of yeast and human core promoters that are predictive of maximal promoter activity. Nucleic Acids Res 41: 5569-5581.
22. Mahadevan S, Struhl K. 1990. Tc, an unusual promoter element required for constitutive transcription of the yeast HIS3 gene. Mol Cell Biol 10: 4447-4455.
23. Maicas E, Friesen JD. 1990. A sequence pattern that occurs at the transcription initiation region of yeast RNA polymerase II promoters. Nucleic Acids Res 18: 3387-3393.
24. Miller G, Hahn S. 2006. A DNA-tethered cleavage probe reveals the path for promoter DNA in the yeast preinitiation complex. Nat Struct Mol Biol 13: 603-610.
25. Miura F, Kawaguchi N, Sese J, Toyoda A, Hattori M, Morishita S, Ito T. 2006. A large-scale full-length cDNA analysis to explore the budding yeast transcriptome. Proc Natl Acad Sci 103: 17846-17851.
26. Mogno I, Vallania F, Mitra RD, Cohen BA. 2010. TATA is a modular component of synthetic promoters. Genome Res 20: 1391-1397.
27. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M. 2008. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344-1349.
28. Rajkumar AS, Dénervaud N, Maerkl SJ. 2013. Mapping the fine structure of a eukaryotic promoter input-output function. Nat Genet 45: 1207-1215.
29. Raveh-Sadka T, Levo M, Shabi U, Shany B, Keren L, Lotan-Pompan M, Zeevi D, Sharon E, Weinberger A, Segal E. 2012. Manipulating nucleosome disfavoring sequences allows fine-tune regulation of gene expression in yeast. Nat Genet 44: 743-750.
30. Rhee HS, Pugh BF. 2012. Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 483: 295-301.
31. Segal E, Widom J. 2009. Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr Opin Struct Biol 19: 65-71.
32. Seizl M, Hartmann H, Hoeg F, Kurth F, Martin DE, Söding J, Cramer P. 2011. A conserved GA element in TATA-less RNA polymerase II promoters. PLoS One 6: e27595.
33. Sharon E, Kalma Y, Sharp A, Raveh-Sadka T, Levo M, Zeevi D, Keren L, Yakhini Z, Weinberger A, Segal E. 2012. Inferring gene regulatory logic from high-throughput measurements of thousands of systematically designed promoters. Nat Biotechnol 30: 521-530.
34. Singer VL, Wobbe CR, Struhl K. 1990. A wide variety of DNA sequences can functionally replace a yeast TATA element for transcriptional activation. Genes Dev 4: 636-645.
35. Smale ST, Kadonaga JT. 2003. The RNA polymerase II core promoter. Annu Rev Biochem 72: 449-479.
36. Stewart JJ, Stargell LA. 2001. The stability of the TFIIA-TBP-DNA complex is dependent on the sequence of the TATAAA element. J Biol Chem 276: 30078-30084.
37. Sugihara F, Kasahara K, Kokubo T. 2011. Highly redundant function of multiple AT-rich sequences as core promoter elements in the TATAless RPS5 promoter of Saccharomyces cerevisiae. Nucleic Acids Res 39: 59-75.
38. Tanay A, Regev A, Shamir R. 2005. Conservation and evolvability in regulatory networks: the evolution of ribosomal regulation in yeast. Proc Natl Acad Sci 102: 7203-7208.
39. Wu R, Li H. 2010. Positioned and G/C-capped poly(dA:dT) tracts associate with the centers of nucleosome-free regions in yeast promoters. Genome Res 20: 473-484.
40. Wurtzel O, Sapra R, Chen F, Zhu Y, Simmons BA, Sorek R. 2010. A single-base resolution map of an archaeal transcriptome. Genome Res 20: 133-141.
41. Zeevi D, Lubliner S, Lotan-Pompan M, Hodis E, Vesterman R, Weinberger A, Segal E. 2014. Molecular dissection of the genetic mechanisms that underlie expression conservation in orthologous yeast ribosomal promoters. Genome Res 24: 1991-1999.
42. Zehavi Y, Kuznetsov O, Ovadia-Shochat A, Juven-Gershon T. 2014. Core promoter functions in the regulation of gene expression of Drosophila dorsal target genes. J Biol Chem 289: 11993-12004.
43. Zhang Z, Dietrich FS. 2005. Mapping of transcription start sites in Saccharomyces cerevisiae using 5′ SAGE. Nucleic Acids Res 33: 2838-2851.