Manipulating nucleosome disfavoring sequences allows fine-tune regulation of gene expression in yeast

Nature Genetics

Volumn 44, Issue 7, 2012, Pages 743-750

  Raveh Sadka, Tali ^a   Levo, Michal ^a   Shabi, Uri ^a   Shany, Boaz ^a   Keren, Leeat ^a   Lotan Pompan, Maya ^a   Zeevi, Danny ^a   Sharon, Eilon ^a   Weinberger, Adina ^a   Segal, Eran ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; FUNGAL GENE; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; YEAST;

BASE SEQUENCE; BINDING SITES; DNA, FUNGAL; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; MOLECULAR SEQUENCE DATA; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; YEASTS;

EUKARYOTA;

EID: 84862984796     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.2305     Document Type: Article

References (44)

1. Ptashne, M. & Gann, A. Genes and Signals (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2002).
2. Kornberg, R.D. & Lorch, Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98, 285-294 (1999). (Pubitemid 29380564)
3. Polach, K.J. & Widom, J. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J. Mol. Biol. 254, 130-149 (1995).
4. Kim, H.D. & O'Shea, E.K. A quantitative model of transcription factor-activated gene expression. Nat. Struct. Mol. Biol. 15, 1192-1198 (2008).
5. Lam, F.H., Steger, D.J. & O'Shea, E.K. Chromatin decouples promoter threshold from dynamic range. Nature 453, 246-250 (2008). (Pubitemid 351667976)
6. Liu, X., Lee, C.K., Granek, J.A., Clarke, N.D. & Lieb, J.D. Whole-genome comparison of Leu3 binding in vitro and in vivo reveals the importance of nucleosome occupancy in target site selection. Genome Res. 16, 1517-1528 (2006). (Pubitemid 44878490)
7. Raveh-Sadka, T., Levo, M. & Segal, E. Incorporating nucleosomes into thermodynamic models of transcription regulation. Genome Res. 19, 1480-1496 (2009).
8. Anderson, J.D. & Widom, J. Poly(dA-dT) promoter elements increase the equilibrium accessibility of nucleosomal DNA target sites. Mol. Cell. Biol. 21, 3830-3839 (2001). (Pubitemid 32466994)
9. Segal, E. & Widom, J. Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr. Opin. Struct. Biol. 19, 65-71 (2009).
10. Kaplan, N. et al. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458, 362-366 (2009).
11. Yuan, G.C. et al. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309, 626-630 (2005).
12. Zhang, Y. et al. Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat. Struct. Mol. Biol. 16, 847-852 (2009).
13. Dechering, K.J., Cuelenaere, K., Konings, R.N. & Leunissen, J.A. Distinct frequency-distributions of homopolymeric DNA tracts in different genomes. Nucleic Acids Res. 26, 4056-4062 (1998). (Pubitemid 28401361)
14. Field, Y. et al. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLOS Comput. Biol. 4, e1000216 (2008).
15. Iyer, V. & Struhl, K. Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J. 14, 2570-2579 (1995).
16. Knutson, B.A. & Hahn, S. Domains of Tra1 important for activator recruitment and transcription coactivator functions of SAGA and NuA4 complexes. Mol. Cell. Biol. 31, 818-831 (2011).
17. Kuo, M.H., vom Baur, E., Struhl, K. & Allis, C.D. Gcn4 activator targets Gcn5 histone acetyltransferase to specific promoters independently of transcription. Mol. Cell 6, 1309-1320 (2000). (Pubitemid 32045924)
18. Zeevi, D. et al. Compensation for differences in gene copy number among yeast ribosomal proteins is encoded within their promoters. Genome Res. 21, 2114-2128 (2011).
19. Fordyce, P.M. et al. De novo identification and biophysical characterization of transcription-factor binding sites with microfluidic affinity analysis. Nat. Biotechnol. 28, 970-975 (2010).
20. Hill, D.E., Hope, I.A., Macke, J.P. & Struhl, K. Saturation mutagenesis of the yeast his3 regulatory site: requirements for transcriptional induction and for binding by GCN4 activator protein. Science 234, 451-457 (1986). (Pubitemid 17181426)
21. Zhu, C. et al. High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res. 19, 556-566 (2009).
22. Yuan, G.C. & Liu, J.S. Genomic sequence is highly predictive of local nucleosome depletion. PLOS Comput. Biol. 4, e13 (2008).
23. Sekinger, E.A., Moqtaderi, Z. & Struhl, K. Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Mol. Cell 18, 735-748 (2005). (Pubitemid 40804808)
24. Miller, J.A. & Widom, J. Collaborative competition mechanism for gene activation in vivo. Mol. Cell. Biol. 23, 1623-1632 (2003). (Pubitemid 36246044)
25. Kornberg, R.D. & Stryer, L. Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res. 16, 6677-6690 (1988).
26. Beer, M.A. & Tavazoie, S. Predicting gene expression from sequence. Cell 117, 185-198 (2004). (Pubitemid 38496239)
27. Bintu, L. et al. Transcriptional regulation by the numbers: models. Curr. Opin. Genet. Dev. 15, 116-124 (2005). (Pubitemid 40410659)
28. Gertz, J., Siggia, E.D. & Cohen, B.A. Analysis of combinatorial cis-regulation in synthetic and genomic promoters. Nature 457, 215-218 (2009).
29. Segal, E., Raveh-Sadka, T., Schroeder, M., Unnerstall, U. & Gaul, U. Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 451, 535-540 (2008). (Pubitemid 351186263)
30. Wasson, T. & Hartemink, A.J. An ensemble model of competitive multi-factor binding of the genome. Genome Res. 19, 2101-2112 (2009).
31. MacIsaac, K.D. et al. An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 7, 113 (2006).
32. Zhu, C. et al. High-resolution DNA binding specificity analysis of yeast transcription factors. Genome Res. 19, 556-566 (2009).
33. Bar-Even, A. et al. Noise in protein expression scales with natural protein abundance. Nat. Genet. 38, 636-643 (2006). (Pubitemid 43927304)
34. Taniguchi, Y. et al. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329, 533-538 (2010).
35. Bai, L., Charvin, G., Siggia, E.D. & Cross, F.R. Nucleosome-depleted regions in cell-cycle-regulated promoters ensure reliable gene expression in every cell cycle. Dev. Cell 18, 544-555 (2010).
36. Raser, J.M. & O'Shea, E.K. Control of stochasticity in eukaryotic gene expression. Science 304, 1811-1814 (2004). (Pubitemid 38787899)
37. Cai, L., Friedman, N. & Xie, X.S. Stochastic protein expression in individual cells at the single molecule level. Nature 440, 358-362 (2006).
38. Friedman, N., Cai, L. & Xie, X.S. Linking stochastic dynamics to population distribution: an analytical framework of gene expression. Phys. Rev. Lett. 97, 168302 (2006).
39. Ercan, S., Lubling, Y., Segal, E. & Lieb, J.D. High nucleosome occupancy is encoded at X-linked gene promoters in C. elegans. Genome Res. 21, 237-244 (2011).
40. Chen, W. & Struhl, K. Saturation mutagenesis of a yeast his3 "TATA element": genetic evidence for a specific TATA-binding protein. Proc. Natl. Acad. Sci. USA 85, 2691-2695 (1988).
41. Ben Yehezkel, T. et al. De novo DNA synthesis using single molecule PCR. Nucleic Acids Res. 36, e107 (2008).
42. Linshiz, G. et al. Recursive construction of perfect DNA molecules from imperfect oligonucleotides. Mol. Syst. Biol. 4, 191 (2008).
43. Shabi, U. et al. Processing DNA molecules as text. Syst. Synth. Biol. 4, 227-236 (2010).
44. Gietz, R.D. & Schiestl, R.H. Microtiter plate transformation using the LiAc/SS carrier DNA/PEG method. Nat. Protoc. 2, 5-8 (2007). (Pubitemid 47040062)