Thermodynamics-based models of transcriptional regulation by enhancers: The roles of synergistic activation, cooperative binding and short-range repression

PLoS Computational Biology

Volumn 6, Issue 9, 2010, Pages

  He, Xin ^a   Samee, Md Abul Hassan ^b   Blatti, Charles ^b   Sinha, Saurabh ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; DNA; MACHINERY; QUANTUM THEORY; STATISTICAL MECHANICS; THERMODYNAMICS; TRANSCRIPTION;

COOPERATIVE BINDING; DNA-BINDING; DNA-BINDING SPECIFICITY; GENES EXPRESSION; HEURISTIC APPROXIMATIONS; MECHANISTICS; QUANTITATIVE MODELS; REGULATORY MECHANISM; SYNERGISTIC ACTIVATION; TRANSCRIPTIONAL REGULATION;

TRANSCRIPTION FACTORS;

REPRESSOR PROTEIN; TRANSCRIPTION FACTOR;

ALGORITHM; ARTICLE; BINDING SITE; COMPUTER MODEL; COMPUTER PREDICTION; COMPUTER PROGRAM; CONTROLLED STUDY; DNA BINDING; DNA SEQUENCE; DROSOPHILA MELANOGASTER; EMBRYO; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE REPRESSION; NONHUMAN; PROMOTER REGION; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; SEQUENCE ANALYSIS; THERMODYNAMICS; TRANSCRIPTION REGULATION;

EID: 78049450019     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000935     Document Type: Article

References (65)

1. Davidson EH (2006) The Regulatory Genome: Gene Regulatory Networks in Development and Evolution: Academic Press.
2. Lebrecht D, Foehr M, Smith E, Lopes FJ, Vanario-Alonso CE, et al. (2005) Bicoid cooperative DNA binding is critical for embryonic patterning in Drosophila. Proc Natl Acad Sci U S A 102: 13176-13181.
3. Arnosti DN, Barolo S, Levine M, Small S (1996) The eve stripe 2 enhancer employs multiple modes of transcriptional synergy. Development 122: 205-214.
4. Fakhouri WD, Ay A, Sayal R, Dresch J, Dayringer E, et al. (2010) Deciphering a transcriptional regulatory code: modeling short-range repression in the Drosophila embryo. Mol Syst Biol 6: 341.
5. Shea MA, Ackers GK (1985) The OR control system of bacteriophage lambda. A physical-chemical model for gene regulation. J Mol Biol 181: 211-230.
6. Segal E, Raveh-Sadka T, Schroeder M, Unnerstall U, Gaul U (2008) Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 451: 535-540.
7. Buchler NE, Gerland U, Hwa T (2003) On schemes of combinatorial transcription logic. Proc Natl Acad Sci U S A 100: 5136-5141.
8. Joung JK, Le LU, Hochschild A (1993) Synergistic activation of transcription by Escherichia coli cAMP receptor protein. Proc Natl Acad Sci U S A 90: 3083-3087.
9. Berg OG, von Hippel PH (1987) Selection of DNA binding sites by regulatory proteins. Statistical-mechanical theory and application to operators and promoters. J Mol Biol 193: 723-750.
10. Stormo GD, Fields DS (1998) Specificity, free energy and information content in protein-DNA interactions. Trends Biochem Sci 23: 109-113.
11. Bauer DC, Bailey TL (2009) Optimizing static thermodynamic models of transcriptional regulation. Bioinformatics 25: 1640-1646.
12. Gertz J, Siggia ED, Cohen BA (2009) Analysis of combinatorial cis-regulation in synthetic and genomic promoters. Nature 457: 215-218.
13. Janssens H, Hou S, Jaeger J, Kim AR, Myasnikova E, et al. (2006) Quantitative and predictive model of transcriptional control of the Drosophila melanogaster even skipped gene. Nat Genet 38: 1159-1165.
14. Zinzen RP, Papatsenko D (2007) Enhancer responses to similarly distributed antagonistic gradients in development. PLoS Comput Biol 3: e84.
15. Tanay A (2006) Extensive low-affinity transcriptional interactions in the yeast genome. Genome Res 16: 962-972.
16. Lifanov AP, Makeev VJ, Nazina AG, Papatsenko DA (2003) Homotypic regulatory clusters in Drosophila. Genome Res 13: 579-588.
17. Gray S, Levine M (1996) Transcriptional repression in development. Curr Opin Cell Biol 8: 358-364.
18. Kulkarni MM, Arnosti DN (2005) cis-regulatory logic of short-range transcriptional repression in Drosophila melanogaster. Mol Cell Biol 25: 3411-3420.
19. Makeev VJ, Lifanov AP, Nazina AG, Papatsenko DA (2003) Distance preferences in the arrangement of binding motifs and hierarchical levels in organization of transcription regulatory information. Nucleic Acids Res 31: 6016-6026.
20. Nibu Y, Zhang H, Bajor E, Barolo S, Small S, et al. (1998) dCtBP mediates transcriptional repression by Knirps, Kruppel and Snail in the Drosophila embryo. EMBO J 17: 7009-7020.
21. Sauer F, Fondell JD, Ohkuma Y, Roeder RG, Jackle H (1995) Control of transcription by Kruppel through interactions with TFIIB and TFIIE beta. Nature 375: 162-164.
22. Ptashne M, Gann A Genes & Signals: Cold Spring Harbor Laboratory Press.
23. Green MR (2005) Eukaryotic transcription activation: right on target. Mol Cell 18: 399-402.
24. Carey M (1998) The enhanceosome and transcriptional synergy. Cell 92: 5-8.
25. Struhl K (2001) Gene regulation. A paradigm for precision. Science 293: 1054-1055.
26. Veitia RA (2003) A sigmoidal transcriptional response: cooperativity, synergy and dosage effects. Biol Rev Camb Philos Soc 78: 149-170.
27. Sauer F, Hansen SK, Tjian R (1995) Multiple TAFIIs directing synergistic activation of transcription. Science 270: 1783-1788.
28. Ma X, Yuan D, Diepold K, Scarborough T, Ma J (1996) The Drosophila morphogenetic protein Bicoid binds DNA cooperatively. Development 122: 1195-1206.
29. Hoch M, Gerwin N, Taubert H, Jackle H (1992) Competition for overlapping sites in the regulatory region of the Drosophila gene Kruppel. Science 256: 94-97.
30. Moses AM, Pollard DA, Nix DA, Iyer VN, Li XY, et al. (2006) Large-scale turnover of functional transcription factor binding sites in Drosophila. PLoS Comput Biol 2: e130.
31. Dermitzakis ET, Bergman CM, Clark AG (2003) Tracing the evolutionary history of Drosophila regulatory regions with models that identify transcription factor binding sites. Mol Biol Evol 20: 703-714.
32. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, et al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
33. Hu Z, Killion PJ, Iyer VR (2007) Genetic reconstruction of a functional transcriptional regulatory network. Nat Genet 39: 683-687.
34. Reinitz J, Hou S, Sharp DH (2003) Transcriptional Control in Drosophila. ComPlexUs 1: 54-64.
35. Beer MA, Tavazoie S (2004) Predicting gene expression from sequence. Cell 117: 185-198.
36. Zinzen RP, Girardot C, Gagneur J, Braun M, Furlong EE (2009) Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 462: 65-70.
37. Benos PV, Bulyk ML, Stormo GD (2002) Additivity in protein-DNA interactions: how good an approximation is it? Nucleic Acids Res 30: 4442-4451.
38. Maerkl SJ, Quake SR (2007) A systems approach to measuring the binding energy landscapes of transcription factors. Science 315: 233-237.
39. Keller SA, Mao Y, Struffi P, Margulies C, Yurk CE, et al. (2000) dCtBPdependent and -independent repression activities of the Drosophila Knirps protein. Mol Cell Biol 20: 7247-7258.
40. Hermsen R, Tans S, ten Wolde PR (2006) Transcriptional regulation by competing transcription factor modules. PLoS Comput Biol 2: e164.
41. Teif VB (2007) General transfer matrix formalism to calculate DNA-proteindrug binding in gene regulation: application to OR operator of phage lambda. Nucleic Acids Res 35: e80.
42. Andrioli LP, Vasisht V, Theodosopoulou E, Oberstein A, Small S (2002) Anterior repression of a Drosophila stripe enhancer requires three positionspecific mechanisms. Development 129: 4931-4940.
43. Jimenez G, Guichet A, Ephrussi A, Casanova J (2000) Relief of gene repression by torso RTK signaling: role of capicua in Drosophila terminal and dorsoventral patterning. Genes Dev 14: 224-231.
44. Noyes MB, Meng X, Wakabayashi A, Sinha S, Brodsky MH, et al. (2008) A systematic characterization of factors that regulate Drosophila segmentation via a bacterial one-hybrid system. Nucleic Acids Res 36: 2547-2560.
45. Bergman CM, Carlson JW, Celniker SE (2005) Drosophila DNase I footprint database: a systematic genome annotation of transcription factor binding sites in the fruitfly, Drosophila melanogaster. Bioinformatics 21: 1747-1749.
46. Homsi DS, Gupta V, Stormo GD (2009) Modeling the quantitative specificity of DNA-binding proteins from example binding sites. PLoS One 4: e6736.
47. Ray P, Shringarpure S, Kolar M, Xing EP (2008) CSMET: comparative genomic motif detection via multi-resolution phylogenetic shadowing. PLoS Comput Biol 4: e1000090.
48. Borneman AR, Gianoulis TA, Zhang ZD, Yu H, Rozowsky J, et al. (2007) Divergence of transcription factor binding sites across related yeast species. Science 317: 815-819.
49. Ludwig MZ (2002) Functional evolution of noncoding DNA. Curr Opin Genet Dev 12: 634-639.
50. Gao F, Foat BC, Bussemaker HJ (2004) Defining transcriptional networks through integrative modeling of mRNA expression and transcription factor binding data. BMC Bioinformatics 5: 31.
51. Burz DS, Rivera-Pomar R, Jackle H, Hanes SD (1998) Cooperative DNAbinding by Bicoid provides a mechanism for threshold-dependent gene activation in the Drosophila embryo. EMBO J 17: 5998-6009.
52. Chi T, Lieberman P, Ellwood K, Carey M (1995) A general mechanism for transcriptional synergy by eukaryotic activators. Nature 377: 254-257.
53. Gray S, Szymanski P, Levine M (1994) Short-range repression permits multiple enhancers to function autonomously within a complex promoter. Genes Dev 8: 1829-1838.
54. Small S, Arnosti DN, Levine M (1993) Spacing ensures autonomous expression of different stripe enhancers in the even-skipped promoter. Development 119: 762-772.
55. La Rosee-Borggreve A, Hader T, Wainwright D, Sauer F, Jackle H (1999) hairy stripe 7 element mediates activation and repression in response to different domains and levels of Kruppel in the Drosophila embryo. Mech Dev 89: 133-140.
56. Small S, Blair A, Levine M (1996) Regulation of two pair-rule stripes by a single enhancer in the Drosophila embryo. Dev Biol 175: 314-324.
57. Yan R, Small S, Desplan C, Dearolf CR, Darnell JE, Jr. (1996) Identification of a Stat gene that functions in Drosophila development. Cell 84: 421-430.
58. Krumm A, Hickey LB, Groudine M (1995) Promoter-proximal pausing of RNA polymerase II defines a general rate-limiting step after transcription initiation. Genes Dev 9: 559-572.
59. Nakanishi H, Mitarai N, Sneppen K (2008) Dynamical analysis on gene activity in the presence of repressors and an interfering promoter. Biophys J 95: 4228-4240.
60. Zenklusen D, Larson DR, Singer RH (2008) Single-RNA counting reveals alternative modes of gene expression in yeast. Nat Struct Mol Biol 15: 1263-1271.
61. Fowlkes CC, Hendriks CL, Keranen SV, Weber GH, Rubel O, et al. (2008) A quantitative spatiotemporal atlas of gene expression in the Drosophila blastoderm. Cell 133: 364-374.
62. Morozov AV, Fortney K, Gaykalova DA, Studitsky VM, Widom J, et al. (2009) Using DNA mechanics to predict in vitro nucleosome positions and formation energies. Nucleic Acids Res 37: 4707-4722.
63. Wasson T, Hartemink AJ (2009) An ensemble model of competitive multi-factor binding of the genome. Genome Res 19: 2101-2112.
64. Zhu H, Bilgin M, Bangham R, Hall D, Casamayor A, et al. (2001) Global analysis of protein activities using proteome chips. Science 293: 2101-2105.
65. Lusk RW, Eisen MB (2010) Evolutionary mirages: selection on binding site composition creates the illusion of conserved grammars in Drosophila enhancers. PLoS Genet 6: e1000829.