From DNA sequence to transcriptional behaviour: a quantitative approach (original) (raw)

• Casadaban, M. J. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J. Mol. Biol. 104, 541–555 (1976).
  CAS PubMed Google Scholar
• Guarente, L. & Ptashne, M. Fusion of Escherichia coli lacZ to the cytochrome c gene of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 78, 2199–2203 (1981).
  CAS PubMed PubMed Central Google Scholar
• Bellen, H. J. et al. P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev. 3, 1288–1300 (1989).
  CAS PubMed Google Scholar
• Wilson, M. D. et al. Species-specific transcription in mice carrying human chromosome 21. Science 322, 434–438 (2008).
  CAS PubMed PubMed Central Google Scholar
• Rajewsky, N., Vergassola, M., Gaul, U. & Siggia, E. D. Computational detection of genomic _cis_-regulatory modules applied to body patterning in the early Drosophila embryo. BMC Bioinformatics 3, 30 (2002).
  PubMed PubMed Central Google Scholar
• Sinha, S., van Nimwegen, E. & Siggia, E. D. A probabilistic method to detect regulatory modules. Bioinformatics 19 (Suppl. 1), i292–i301 (2003).
  PubMed Google Scholar
• Granek, J. A. & Clarke, N. D. Explicit equilibrium modeling of transcription-factor binding and gene regulation. Genome Biol. 6, R87 (2005).
  PubMed PubMed Central Google Scholar
• Segal, E. et al. A genomic code for nucleosome positioning. Nature 442, 772–778 (2006). This paper shows that genomes encode the location of many of their nucleosomes and that this intrinsically encoded nucleosome organization might facilitate specific chromosome functions.
  CAS PubMed PubMed Central Google Scholar
• Ioshikhes, I. P., Albert, I., Zanton, S. J. & Pugh, B. F. Nucleosome positions predicted through comparative genomics. Nature Genet. 38, 1210–1215 (2006). This paper shows that different nucleosome architectures might be encoded at different classes of regulatory sequences.
  CAS PubMed Google Scholar
• 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). This study develops an equilibrium-based thermodynamic model that relates factor binding to gene expression in Drosophila melanogaster early embryonic patterning.
  CAS PubMed Google Scholar
• Bintu, L. et al. Transcriptional regulation by the numbers: models. Curr. Opin. Genet. Dev. 15, 116–124 (2005).
  CAS PubMed PubMed Central Google Scholar
• Buchler, N. E., Gerland, U. & Hwa, T. On schemes of combinatorial transcription logic. Proc. Natl Acad. Sci. USA 100, 5136–5141 (2003).
  CAS PubMed PubMed Central Google Scholar
• Dodd, I. B., Shearwin, K. E. & Sneppen, K. Modelling transcriptional interference and DNA looping in gene regulation. J. Mol. Biol. 369, 1200–1213 (2007).
  CAS PubMed Google Scholar
• Kuhlman, T., Zhang, Z., Saier, M. H. Jr & Hwa, T. Combinatorial transcriptional control of the lactose operon of Escherichia coli. Proc. Natl Acad. Sci. USA 104, 6043–6048 (2007).
  CAS PubMed PubMed Central Google Scholar
• Kaplan, N. et al. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458, 362–366 (2009). This study directly measured the intrinsically encoded nucleosome organization of the genome and showed that it is similar to the in vivo organization. A model of nucleosome occupancy trained on in vitro reconstituted yeast nucleosomes significantly predicts nucleosome organization in Caenorhabditis elegans.
  CAS PubMed Google Scholar
• Gertz, J., Siggia, E. D. & Cohen, B. A. Analysis of combinatorial _cis_-regulation in synthetic and genomic promoters. Nature 457, 215–218 (2009). This paper develops and experimentally verifies an equilibrium-based thermodynamic analysis that relates transcription factor binding to gene expression, and shows that these contributions explain a significant fraction of the measured variability in gene expression.
  CAS PubMed Google Scholar
• Foat, B. C., Morozov, A. V. & Bussemaker, H. J. Statistical mechanical modeling of genome-wide transcription factor occupancy data by MatrixREDUCE. Bioinformatics 22, e141–e149 (2006).
  CAS PubMed Google Scholar
• Gupta, S. et al. Predicting human nucleosome occupancy from primary sequence. PLoS Comput. Biol. 4, e1000134 (2008).
  PubMed PubMed Central Google Scholar
• Sinha, S., Adler, A. S., Field, Y., Chang, H. Y. & Segal, E. Systematic functional characterization of _cis_-regulatory motifs in human core promoters. Genome Res. 18, 477–488 (2008).
  CAS PubMed PubMed Central Google Scholar
• Richmond, T. J. & Davey, C. A. The structure of DNA in the nucleosome core. Nature 423, 145–150 (2003).
  CAS PubMed Google Scholar
• Gencheva, M. et al. In vitro and in vivo nucleosome positioning on the ovine β-lactoglobulin gene are related. J. Mol. Biol. 361, 216–230 (2006).
  CAS PubMed Google Scholar
• Thastrom, A., Bingham, L. M. & Widom, J. Nucleosomal locations of dominant DNA sequence motifs for histone–DNA interactions and nucleosome positioning. J. Mol. Biol. 338, 695–709 (2004).
  CAS PubMed Google Scholar
• Satchwell, S. C., Drew, H. R. & Travers, A. A. Sequence periodicities in chicken nucleosome core DNA. J. Mol. Biol. 191, 659–675 (1986).
  CAS PubMed Google Scholar
• Albert, I. et al. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446, 572–576 (2007).
  CAS PubMed Google Scholar
• Johnson, S. M., Tan, F. J., McCullough, H. L., Riordan, D. P. & Fire, A. Z. Flexibility and constraint in the nucleosome core landscape of Caenorhabditis elegans chromatin. Genome Res. 16, 1505–1516 (2006).
  CAS PubMed PubMed Central Google Scholar
• Field, Y. et al. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput. Biol. 4, e1000216 (2008). This study shows that the encoded nucleosome organization is predictive of, and might be the cause of, differences in the transcriptional noise and activation dynamics of regulatory sequences and the utilization efficiency of DNA replication origins.
  PubMed PubMed Central Google Scholar
• Yuan, G. C. & Liu, J. S. Genomic sequence is highly predictive of local nucleosome depletion. PLoS Comput. Biol. 4, e13 (2008).
  PubMed PubMed Central Google Scholar
• Lee, W. et al. A high-resolution atlas of nucleosome occupancy in yeast. Nature Genet. 39, 1235–1244 (2007).
  CAS PubMed Google Scholar
• Peckham, H. E. et al. Nucleosome positioning signals in genomic DNA. Genome Res. 17, 1170–1177 (2007).
  CAS PubMed PubMed Central Google Scholar
• Korber, P., Luckenbach, T., Blaschke, D. & Horz, W. Evidence for histone eviction in trans upon induction of the yeast PHO5 promoter. Mol. Cell. Biol. 24, 10965–10974 (2004).
  CAS PubMed PubMed Central Google Scholar
• Vignali, M., Hassan, A. H., Neely, K. E. & Workman, J. L. ATP-dependent chromatin-remodeling complexes. Mol. Cell. Biol. 20, 1899–1910 (2000).
  CAS PubMed PubMed Central Google Scholar
• Pavlovic, J., Banz, E. & Parish, R. W. The effects of transcription on the nucleosome structure of four Dictyostelium genes. Nucleic Acids Res. 17, 2315–2332 (1989).
  CAS PubMed PubMed Central Google Scholar
• Henikoff, S. Nucleosome destabilization in the epigenetic regulation of gene expression. Nature Rev. Genet. 9, 15–26 (2008).
  CAS PubMed Google Scholar
• Gasser, R., Koller, T. & Sogo, J. M. The stability of nucleosomes at the replication fork. J. Mol. Biol. 258, 224–239 (1996).
  CAS PubMed Google Scholar
• Johnson, D. S., Mortazavi, A., Myers, R. M. & Wold, B. Genome-wide mapping of in vivo protein–DNA interactions. Science 316, 1497–1502 (2007).
  CAS PubMed Google Scholar
• Harbison, C. T. et al. Transcriptional regulatory code of a eukaryotic genome. Nature 431, 99–104 (2004).
  CAS PubMed PubMed Central Google Scholar
• Bulyk, M. L., Gentalen, E., Lockhart, D. J. & Church, G. M. Quantifying DNA–protein interactions by double-stranded DNA arrays. Nature Biotechnol. 17, 573–577 (1999).
  CAS Google Scholar
• Mukherjee, S. et al. Rapid analysis of the DNA-binding specificities of transcription factors with DNA microarrays. Nature Genet. 36, 1331–1339 (2004).
  CAS PubMed Google Scholar
• Maerkl, S. J. & Quake, S. R. A systems approach to measuring the binding energy landscapes of transcription factors. Science 315, 233–237 (2007).
  CAS PubMed Google Scholar
• Berger, M. F. et al. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133, 1266–1276 (2008).
  CAS PubMed PubMed Central Google Scholar
• Zhu, C. et al. High-resolution DNA binding specificity analysis of yeast transcription factors. Genome Res. 19, 556–566 (2009).
  CAS PubMed PubMed Central Google Scholar
• Badis, G. et al. A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol. Cell 32, 878–887 (2008). This study provides direct quantitative measurements of the sequence preferences of over 100 transcription factors from yeast.
  CAS PubMed PubMed Central Google Scholar
• Schroeder, M. D. et al. Transcriptional control in the segmentation gene network of Drosophila. PLoS Biol. 2, e271 (2004).
  PubMed PubMed Central Google Scholar
• Tanay, A. Extensive low-affinity transcriptional interactions in the yeast genome. Genome Res. 16, 962–972 (2006).
  CAS PubMed PubMed Central Google Scholar
• Miller, J. A. & Widom, J. Collaborative competition mechanism for gene activation in vivo. Mol. Cell. Biol. 23, 1623–1632 (2003).
  CAS PubMed PubMed Central Google Scholar
• Li, X. Y. et al. Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol. 6, e27 (2008).
  PubMed PubMed Central Google Scholar
• Shea, M. A. & Ackers, G. K. The OR control system of bacteriophage lambda. A physical–chemical model for gene regulation. J. Mol. Biol. 181, 211–230 (1985).
  CAS PubMed Google Scholar
• Hayes, J. J. & Wolffe, A. P. The interaction of transcription factors with nucleosomal DNA. Bioessays 14, 597–603 (1992).
  CAS PubMed Google Scholar
• Thomas, G. H. & Elgin, S. C. Protein/DNA architecture of the DNase I hypersensitive region of the Drosophila hsp26 promoter. EMBO J. 7, 2191–2201 (1988).
  CAS PubMed PubMed Central Google Scholar
• Zeitlinger, J. et al. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nature Genet. 39, 1512–1516 (2007).
  CAS PubMed Google Scholar
• Hendrix, D. A., Hong, J. W., Zeitlinger, J., Rokhsar, D. S. & Levine, M. S. Promoter elements associated with RNA pol II stalling in the Drosophila embryo. Proc. Natl Acad. Sci. USA 105, 7762–7767 (2008).
  CAS PubMed PubMed Central Google Scholar
• Mavrich, T. N. et al. Nucleosome organization in the Drosophila genome. Nature 453, 358–362 (2008).
  CAS PubMed PubMed Central Google Scholar
• Mavrich, T. N. et al. A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res. 18, 1073–1083 (2008).
  CAS PubMed PubMed Central Google Scholar
• Shivaswamy, S. et al. Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol. 6, e65 (2008).
  PubMed PubMed Central Google Scholar
• Yuan, G. C. et al. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309, 626–630 (2005). The first high-resolution analysis of nucleosome positions in vivo at a genomic scale. The results show that there are stereotyped nucleosome organizations at promoters and add to the evidence that poly(dA:dT) tracts are unfavourable to nucleosome occupancy genome-wide.
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar
• 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). An early demonstration that particular regulatory sequences encode low nucleosome occupancy.
  CAS PubMed Google Scholar
• Valouev, A. et al. A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res. 18, 1051–1063 (2008).
  CAS PubMed PubMed Central Google Scholar
• Kornberg, R. D. & Stryer, L. Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res. 16, 6677–6690 (1988). This paper develops the idea of statistical nucleosome positioning. Simple steric exclusion together with the high density of nucleosomes along the genome leads to a periodic ordering of nucleosomes away from boundary constraints.
  CAS PubMed PubMed Central Google Scholar
• Schones, D. E. et al. Dynamic regulation of nucleosome positioning in the human genome. Cell 132, 887–898 (2008).
  CAS PubMed Google Scholar
• Raveh-Sadka, T., Levo, M. & Segal, E. Incorporating nucleosomes into thermodynamic models of transcription regulation. Genome Res. 19 May 2009 (doi:10.1101/gr.088260.108).
  CAS PubMed PubMed Central Google Scholar
• Khorasanizadeh, S. The nucleosome: from genomic organization to genomic regulation. Cell 116, 259–272 (2004).
  CAS PubMed Google Scholar
• Narlikar, G. J., Fan, H. Y. & Kingston, R. E. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108, 475–487 (2002).
  CAS PubMed Google Scholar
• Kornberg, R. D. & Lorch, Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98, 285–294 (1999).
  CAS PubMed Google Scholar
• Lam, F. H., Steger, D. J. & O'Shea, E. K. Chromatin decouples promoter threshold from dynamic range. Nature 453, 246–250 (2008). This paper shows experimentally that the relationship between nucleosome organization and the factor-binding affinity landscape determines the dynamics of activation of Pho genes in yeast.
  CAS PubMed PubMed Central Google Scholar
• Kim, H. D. & O'Shea, E. K. A quantitative model of transcription factor-activated gene expression. Nature Struct. Mol. Biol. 15, 1192–1198 (2008).
  CAS Google Scholar
• Polach, K. J. & Widom, J. A model for the cooperative binding of eukaryotic regulatory proteins to nucleosomal target sites. J. Mol. Biol. 258, 800–812 (1996).
  CAS PubMed Google Scholar
• Giniger, E. & Ptashne, M. Cooperative DNA binding of the yeast transcriptional activator GAL4. Proc. Natl Acad. Sci. USA 85, 382–386 (1988).
  CAS PubMed PubMed Central Google Scholar
• Tanaka, M. Modulation of promoter occupancy by cooperative DNA binding and activation-domain function is a major determinant of transcriptional regulation by activators in vivo. Proc. Natl Acad. Sci. USA 93, 4311–4315 (1996).
  CAS PubMed PubMed Central Google Scholar
• Ma, X., Yuan, D., Diepold, K., Scarborough, T. & Ma, J. The Drosophila morphogenetic protein Bicoid binds DNA cooperatively. Development 122, 1195–1206 (1996).
  CAS PubMed Google Scholar
• Rubin-Bejerano, I., Mandel, S., Robzyk, K. & Kassir, Y. Induction of meiosis in Saccharomyces cerevisiae depends on conversion of the transcriptional represssor Ume6 to a positive regulator by its regulated association with the transcriptional activator Ime1. Mol. Cell. Biol. 16, 2518–2526 (1996).
  CAS PubMed PubMed Central Google Scholar
• Ma, J. Crossing the line between activation and repression. Trends Genet. 21, 54–59 (2005).
  CAS PubMed Google Scholar
• Felsenfeld, G. & Groudine, M. Controlling the double helix. Nature 421, 448–453 (2003).
  PubMed Google Scholar
• Robert, F. et al. Global position and recruitment of HATs and HDACs in the yeast genome. Mol. Cell 16, 199–209 (2004).
  CAS PubMed PubMed Central Google Scholar
• Dion, M. F. et al. Dynamics of replication-independent histone turnover in budding yeast. Science 315, 1405–1408 (2007).
  CAS PubMed Google Scholar
• Newman, J. R. et al. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441, 840–846 (2006).
  CAS PubMed Google Scholar
• Zhang, Z., Gu, J. & Gu, X. How much expression divergence after yeast gene duplication could be explained by regulatory motif evolution? Trends Genet. 20, 403–407 (2004).
  PubMed Google Scholar
• Tirosh, I., Weinberger, A., Bezalel, D., Kaganovich, M. & Barkai, N. On the relation between promoter divergence and gene expression evolution. Mol. Syst. Biol. 4, 159 (2008).
  PubMed PubMed Central Google Scholar
• Field, Y. et al. Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization. Nature Genet. 41, 438–445 (2009). This paper shows that DNA sequence changes that directly alter the intrinsically encoded nucleosome organization of the genome are associated with, and might be important drivers of, evolutionary divergence in gene expression patterns.
  CAS PubMed Google Scholar
• Bar-Even, A. et al. Noise in protein expression scales with natural protein abundance. Nature Genet. 38, 636–643 (2006).
  CAS PubMed Google Scholar
• Raser, J. M. & O'Shea, E. K. Control of stochasticity in eukaryotic gene expression. Science 304, 1811–1814 (2004).
  CAS PubMed PubMed Central Google Scholar
• Landry, C. R., Lemos, B., Rifkin, S. A., Dickinson, W. J. & Hartl, D. L. Genetic properties influencing the evolvability of gene expression. Science 317, 118–121 (2007).
  CAS PubMed Google Scholar
• Tirosh, I., Weinberger, A., Carmi, M. & Barkai, N. A genetic signature of interspecies variations in gene expression. Nature Genet. 38, 830–834 (2006).
  CAS PubMed Google Scholar
• Blake, W. J., M, K. A., Cantor, C. R. & Collins, J. J. Noise in eukaryotic gene expression. Nature 422, 633–637 (2003).
  CAS PubMed Google Scholar
• Heichinger, C., Penkett, C. J., Bahler, J. & Nurse, P. Genome-wide characterization of fission yeast DNA replication origins. EMBO J. 25, 5171–5179 (2006).
  CAS PubMed PubMed Central Google Scholar
• Kim, S. M., Zhang, D. Y. & Huberman, J. A. Multiple redundant sequence elements within the fission yeast ura4 replication origin enhancer. BMC Mol. Biol. 2, 1 (2001).
  CAS PubMed PubMed Central Google Scholar
• Rippe, K., von Hippel, P. H. & Langowski, J. Action at a distance: DNA-looping and initiation of transcription. Trends Biochem. Sci. 20, 500–506 (1995).
  CAS PubMed Google Scholar
• Fyodorov, D. V. & Kadonaga, J. T. Dynamics of ATP-dependent chromatin assembly by ACF. Nature 418, 897–900 (2002).
  CAS PubMed Google Scholar
• Yang, J. G., Madrid, T. S., Sevastopoulos, E. & Narlikar, G. J. The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing. Nature Struct. Mol. Biol. 13, 1078–1083 (2006).
  CAS Google Scholar
• Whitehouse, I., Rando, O. J., Delrow, J. & Tsukiyama, T. Chromatin remodelling at promoters suppresses antisense transcription. Nature 450, 1031–1035 (2007).
  CAS PubMed Google Scholar
• Rippe, K. et al. DNA sequence- and conformation-directed positioning of nucleosomes by chromatin-remodeling complexes. Proc. Natl Acad. Sci. USA 104, 15635–15640 (2007).
  CAS PubMed PubMed Central Google Scholar
• von Hippel, P. H. & Delagoutte, E. A general model for nucleic acid helicases and their “coupling” within macromolecular machines. Cell 104, 177–190 (2001).
  CAS PubMed Google Scholar
• 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).
  CAS PubMed PubMed Central Google Scholar