Unraveling determinants of transcription factor binding outside the core binding site

Genome Research

Volumn 25, Issue 7, 2015, Pages 1018-1029

  Levo, Michal ^a   Zalckvar, Einat ^a   Sharon, Eilon ^a   Machado, Ana Carolina Dantas ^b   Kalma, Yael ^a   Lotam Pompan, Maya ^a   Weinberger, Adina ^a   Yakhini, Zohar ^c,d   Rohs, Remo ^b   Segal, Eran ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b University of Southern California ^*  (United States)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^d AGILENT LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; TRANSCRIPTION FACTOR; NUCLEOSOME; POLY(DA); POLYADENYLIC ACID; POLYTHYMIDYLIC ACID; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; BINDING ASSAY; BINDING SITE; CONCENTRATION (PARAMETERS); DNA FLANKING REGION; DNA SEQUENCE; DNA TEMPLATE; GENE EXPRESSION; GENE LIBRARY; GENE SEQUENCE; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR PROBE; NUCLEOSOME; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; QUANTITATIVE STUDY; BIOLOGY; GENETICS; METABOLISM; PROCEDURES; REGULATORY SEQUENCE; SACCHAROMYCES CEREVISIAE; THERMODYNAMICS;

BINDING SITES; COMPUTATIONAL BIOLOGY; NUCLEOSOMES; POLY A; POLY T; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; SACCHAROMYCES CEREVISIAE; THERMODYNAMICS; TRANSCRIPTION FACTORS;

EID: 84937031367     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.185033.114     Document Type: Article

References (47)

1. Alexeev DG, Lipanov AA, Skuratovskii I. 1987. Poly(dA).poly(dT) is a B-type double helix with a distinctively narrow minor groove. Nature 325: 821-823.
2. Anderson JD, Widom J. 2001. Poly(dA-dT) promoter elements increase the equilibrium accessibility of nucleosomal DNA target sites. Mol Cell Biol 21: 3830-3839.
3. Bao Y, White CL, Luger K. 2006. Nucleosome core particles containing a poly(dA.dT) sequence element exhibit a locally distorted DNA structure. J Mol Biol 361: 617-624.
4. Berger MF, Bulyk ML. 2009. Universal protein-binding microarrays for the comprehensive characterization of the DNA-binding specificities of transcription factors. Nat Protoc 4: 393-411.
5. Blecher-Gonen R, Barnett-Itzhaki Z, Jaitin D, Amann-Zalcenstein D, Lara-Astiaso D, Amit I. 2013. High-throughput chromatin immunoprecipitation for genome-wide mapping of in vivo protein-DNA interactions and epigenomic states. Nat Protoc 8: 539-554.
6. Ellenberger TE, Brandl CJ, Struhl K, Harrison SC. 1992. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted α helices: crystal structure of the protein-DNA complex. Cell 71: 1223-1237.
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. Fordyce PM, Gerber D, Tran D, Zheng J, Li H, DeRisi JL, Quake SR. 2010. De novo identification and biophysical characterization of transcription-factor binding sites with microfluidic affinity analysis. Nat Biotechnol 28: 970-975.
9. Friedman J, Hastie T, Tibshirani R. 2010. Regularization paths for generalized linear models via coordinate descent. J Stat Softw 33: 1-22.
10. Gordan 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.
11. Guertin MJ, Lis JT. 2010. Chromatin landscape dictates HSF binding to target DNA elements. PLoS Genet 6: e1001114.
12. Guertin MJ, Martins AL, Siepel A, Lis JT. 2012. Accurate prediction of inducible transcription factor binding intensities in vivo. PLoS Genet 8: e1002610.
13. Hahn S, Young ET. 2011. Transcriptional regulation in Saccharomyces cerevisiae: transcription factor regulation and function, mechanisms of initiation, and roles of activators and coactivators. Genetics 189: 705-736.
14. Hill DE, Hope IA, Macke JP, Struhl K. 1986. Saturation mutagenesis of the yeast his3 regulatory site: requirements for transcriptional induction and for binding by GCN4 activator protein. Science 234: 451-457.
15. Jacob F, Monod J. 1961. Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3: 318-356.
16. Jolma A, Yan J, Whitington T, Toivonen J, Nitta KR, Rastas P, Morgunova E, Enge M, Taipale M, Wei G, et al. 2013. DNA-binding specificities of human transcription factors. Cell 152: 327-339.
17. 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.
18. Keller W, Konig P, Richmond TJ. 1995. Crystal structure of a bZIP/DNA complex at 2.2 A: determinants of DNA specific recognition. J Mol Biol 254: 657-667.
19. Kim S, Brostromer E, Xing D, Jin J, Chong S, Ge H, Wang S, Gu C, Yang L, Gao YQ, et al. 2013. Probing allostery through DNA. Science 339: 816-819.
20. Lelli KM, Slattery M, Mann RS. 2012. Disentangling the many layers of eukaryotic transcriptional regulation. Annu Rev Genet 46: 43-68.
21. 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.
22. Levo M, Segal E. 2014. In pursuit of design principles of regulatory sequences. Nat Rev Genet 15: 453-468.
23. Liu X, Lee CK, Granek JA, Clarke ND, Lieb JD. 2006. 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.
24. Maerkl SJ, Quake SR. 2007. A systems approach to measuring the binding energy landscapes of transcription factors. Science 315: 233-237.
25. Marmorstein R, Carey M, Ptashne M, Harrison SC. 1992. DNA recognition by GAL4: structure of a protein-DNA complex. Nature 356: 408-414.
26. Morozov AV, Siggia ED. 2007. Connecting protein structure with predictions of regulatory sites. Proc Natl Acad Sci 104: 7068-7073.
27. Nutiu R, Friedman RC, Luo S, Khrebtukova I, Silva D, Li R, Zhang L, Schroth GP, Burge CB. 2011. Direct measurement of DNA affinity landscapes on a high-throughput sequencing instrument. Nat Biotechnol 29: 659-664.
28. Oliphant AR, Brandl CJ, Struhl K. 1989. Defining the sequence specificity of DNA-binding proteins by selecting binding sites from random-sequence oligonucleotides: analysis of yeast GCN4 protein. Mol Cell Biol 9: 2944-2949.
29. Rajkumar AS, Denervaud N, Maerkl SJ. 2013. Mapping the fine structure of a eukaryotic promoter input-output function. Nat Genet 45: 1207-1215.
30. Raveh-Sadka T, Levo M, Segal E. 2009. Incorporating nucleosomes into thermodynamic models of transcription regulation. Genome Res 19: 1480-1496.
31. 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.
32. Rohs R, West SM, Sosinsky A, Liu P, Mann RS, Honig B. 2009. The role of DNA shape in protein-DNA recognition. Nature 461: 1248-1253.
33. Rohs R, Jin X, West SM, Joshi R, Honig B, Mann RS. 2010. Origins of specificity in protein-DNA recognition. Annu Rev Biochem 79: 233-269.
34. Segal E, Widom J. 2009a. From DNA sequence to transcriptional behaviour: a quantitative approach. Nat Rev Genet 10: 443-456.
35. Segal E, Widom J. 2009b. Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr Opin Struct Biol 19: 65-71.
36. 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.
37. Siggers T, Duyzend MH, Reddy J, Khan S, Bulyk ML. 2011. Non-DNA-binding cofactors enhance DNA-binding specificity of a transcriptional regulatory complex. Mol Syst Biol 7: 555.
38. Slattery M, Riley T, Liu P, Abe N, Gomez-Alcala P, Dror I, Zhou T, Rohs R, Honig B, Bussemaker HJ, et al. 2011. Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell 147: 1270-1282.
39. Slattery M, Zhou T, Yang L, Dantas Machado AC, Gordan R, Rohs R. 2014. Absence of a simple code: how transcription factors read the genome. Trends Biochem Sci 39: 381-399.
40. Struhl K, Segal E. 2013. Determinants of nucleosome positioning. Nat Struct Mol Biol 20: 267-273.
41. White MA, Myers CA, Corbo JC, Cohen BA. 2013. Massively parallel in vivo enhancer assay reveals that highly local features determine the cis-regulatory function of ChIP-seq peaks. Proc Natl Acad Sci 110: 11952-11957.
42. Wong D, Teixeira A, Oikonomopoulos S, Humburg P, Lone IN, Saliba D, Siggers T, Bulyk M, Angelov D, Dimitrov S, et al. 2011. Extensive characterization of NF-kappaB binding uncovers non-canonical motifs and advances the interpretation of genetic functional traits. Genome Biol 12: R70.
43. Yang L, Zhou T, Dror I, Mathelier A, Wasserman WW, Gordan R, Rohs R. 2014. TFBSshape: a motif database for DNA shape features of transcription factor binding sites. Nucleic Acids Res 42: D148-D155.
44. Zhang Y, Moqtaderi Z, Rattner BP, Euskirchen G, Snyder M, Kadonaga JT, Liu XS, Struhl K. 2009. Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat Struct Mol Biol 16: 847-852.
45. Zhou X, O'Shea EK. 2011. Integrated approaches reveal determinants of genome-wide binding and function of the transcription factor Pho4. Mol Cell 42: 826-836.
46. Zhou T, Yang L, Lu Y, Dror I, Dantas Machado AC, Ghane T, Di Felice R, Rohs R. 2013. DNAshape: a method for the high-throughput prediction of DNA structural features on a genomic scale. Nucleic Acids Res 41: W56-W62.
47. Zhu C, Byers KJ, McCord RP, Shi Z, Berger MF, Newburger DE, Saulrieta K, Smith Z, Shah MV, Radhakrishnan M, et al. 2009. High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res 19: 556-566.