Genomic Regions Flanking E-Box Binding Sites Influence DNA Binding Specificity of bHLH Transcription Factors through DNA Shape

Cell Reports

Volumn 3, Issue 4, 2013, Pages 1093-1104

  Gordân, Raluca ^a,b   Shen, Ning ^b   Dror, Iris ^d   Zhou, Tianyin ^d   Horton, John ^c   Rohs, Remo ^d   Bulyk, Martha L ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DUKE UNIVERSITY   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DNA; PROTEIN CBF1; PROTEIN TYE7; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA SEQUENCE; GENE SEQUENCE; IN VITRO STUDY; IN VIVO STUDY; MATHEMATICAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BINDING SITES; DNA; E-BOX ELEMENTS; GENOME, FUNGAL; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; NUCLEOTIDE MOTIFS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-ACTIVATORS;

EUKARYOTA;

EID: 84876955991     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.03.014     Document Type: Article

References (51)

1. Arvey A., Agius P., Noble W.S., Leslie C. Sequence and chromatin determinants of cell-type-specific transcription factor binding. Genome Res. 2012, 22:1723-1734.
2. Atchley W.R., Fitch W.M. A natural classification of the basic helix-loop-helix class of transcription factors. Proc. Natl. Acad. Sci. USA 1997, 94:5172-5176.
3. Badis G., Berger M.F., Philippakis A.A., Talukder S., Gehrke A.R., Jaeger S.A., Chan E.T., Metzler G., Vedenko A., Chen X., et al. Diversity and complexity in DNA recognition by transcription factors. Science 2009, 324:1720-1723.
4. Berger M.F., Bulyk M.L. Universal protein-binding microarrays for the comprehensive characterization of the DNA-binding specificities of transcription factors. Nat. Protoc. 2009, 4:393-411.
5. Berger M.F., Philippakis A.A., Qureshi A.M., He F.S., Estep P.W., Bulyk M.L. Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat. Biotechnol. 2006, 24:1429-1435.
6. Bishop E.P., Rohs R., Parker S.C., West S.M., Liu P., Mann R.S., Honig B., Tullius T.D. A map of minor groove shape and electrostatic potential from hydroxyl radical cleavage patterns of DNA. ACS Chem. Biol. 2011, 6:1314-1320.
7. Brownlie P., Ceska T., Lamers M., Romier C., Stier G., Teo H., Suck D. The crystal structure of an intact human Max-DNA complex: new insights into mechanisms of transcriptional control. Structure 1997, 5:509-520.
8. Bulyk M.L. Computational prediction of transcription-factor binding site locations. Genome Biol. 2003, 5:201.
9. Busser B.W., Shokri L., Jaeger S.A., Gisselbrecht S.S., Singhania A., Berger M.F., Zhou B., Bulyk M.L., Michelson A.M. Molecular mechanism underlying the regulatory specificity of a Drosophila homeodomain protein that specifies myoblast identity. Development 2012, 139:1164-1174.
10. Cai M., Davis R.W. Yeast centromere binding protein CBF1, of the helix-loop-helix protein family, is required for chromosome stability and methionine prototrophy. Cell 1990, 61:437-446.
11. Chang C.-C., Lin C.-J. LIBSVM: a library for support vector machines. ACM Trans. Intell. Syst. Technol. 2011, 2:27.
12. Cherry J.M., Hong E.L., Amundsen C., Balakrishnan R., Binkley G., Chan E.T., Christie K.R., Costanzo M.C., Dwight S.S., Engel S.R., et al. Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res. 2012, 40(Database issue):D700-D705.
13. Cole C., Barber J.D., Barton G.J. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 2008, 36(Web Server issue):W197-W201.
14. De Masi F., Grove C.A., Vedenko A., Alibés A., Gisselbrecht S.S., Serrano L., Bulyk M.L., Walhout A.J. Using a structural and logics systems approach to infer bHLH-DNA binding specificity determinants. Nucleic Acids Res. 2011, 39:4553-4563.
15. Drucker H., Burges C.J.C., Kaufman L., Smola A., Vapnik V. Support vector regression machines. Adv. Neural Inf. Process. Syst. 1997, 9:155-161.
16. Ferré-D'Amaré A.R., Pognonec P., Roeder R.G., Burley S.K. Structure and function of the b/HLH/Z domain of USF. EMBO J. 1994, 13:180-189.
17. Fong A.P., Yao Z., Zhong J.W., Cao Y., Ruzzo W.L., Gentleman R.C., Tapscott S.J. Genetic and epigenetic determinants of neurogenesis and myogenesis. Dev. Cell 2012, 22:721-735.
18. Gordân R., Hartemink A.J., Bulyk M.L. Distinguishing direct versus indirect transcription factor-DNA interactions. Genome Res. 2009, 19:2090-2100.
19. Gordân R., Murphy K.F., McCord R.P., Zhu C., Vedenko A., Bulyk M.L. Curated collection of yeast transcription factor DNA binding specificity data reveals novel structural and gene regulatory insights. Genome Biol. 2011, 12:R125.
20. Grove C.A., De Masi F., Barrasa M.I., Newburger D.E., Alkema M.J., Bulyk M.L., Walhout A.J. A multiparameter network reveals extensive divergence between C. elegans bHLH transcription factors. Cell 2009, 138:314-327.
21. Harbison C.T., Gordon D.B., Lee T.I., Rinaldi N.J., Macisaac K.D., Danford T.W., Hannett N.M., Tagne J.B., Reynolds D.B., Yoo J., et al. Transcriptional regulatory code of a eukaryotic genome. Nature 2004, 431:99-104.
22. Harris R., Mackoy T., Dantas Machado A., Xu D., Rohs R., Fenley M. Innovations in biomolecular modeling and simulation. Biomolecular Sciences Series 2012, 53-80. Royal Society of Chemistry Publishing, London. T. Schlick (Ed.).
23. Hesselberth J.R., Chen X., Zhang Z., Sabo P.J., Sandstrom R., Reynolds A.P., Thurman R.E., Neph S., Kuehn M.S., Noble W.S., et al. Global mapping of protein-DNA interactions in vivo by digital genomic footprinting. Nat. Methods 2009, 6:283-289.
24. Hollenhorst P.C., Chandler K.J., Poulsen R.L., Johnson W.E., Speck N.A., Graves B.J. DNA specificity determinants associate with distinct transcription factor functions. PLoS Genet. 2009, 5:e1000778.
25. Joshi R., Passner J.M., Rohs R., Jain R., Sosinsky A., Crickmore M.A., Jacob V., Aggarwal A.K., Honig B., Mann R.S. Functional specificity of a Hox protein mediated by the recognition of minor groove structure. Cell 2007, 131:530-543.
26. Kent N.A., Eibert S.M., Mellor J. Cbf1p is required for chromatin remodeling at promoter-proximal CACGTG motifs in yeast. J. Biol. Chem. 2004, 279:27116-27123.
27. Lavery R., Sklenar H. Defining the structure of irregular nucleic acids: conventions and principles. J. Biomol. Struct. Dyn. 1989, 6:655-667.
28. Lee T.A., Jorgensen P., Bognar A.L., Peyraud C., Thomas D., Tyers M. Dissection of combinatorial control by the Met4 transcriptional complex. Mol. Biol. Cell 2010, 21:456-469.
29. Lelli K.M., Slattery M., Mann R.S. Disentangling the many layers of eukaryotic transcriptional regulation. Annu. Rev. Genet. 2012, 46:43-68.
30. Leonard D.A., Rajaram N., Kerppola T.K. Structural basis of DNA bending and oriented heterodimer binding by the basic leucine zipper domains of Fos and Jun. Proc. Natl. Acad. Sci. USA 1997, 94:4913-4918.
31. Ma P.C., Rould M.A., Weintraub H., Pabo C.O. Crystal structure of MyoD bHLH domain-DNA complex: perspectives on DNA recognition and implications for transcriptional activation. Cell 1994, 77:451-459.
32. MacIsaac K.D., Wang T., Gordon D.B., Gifford D.K., Stormo G.D., Fraenkel E. An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 2006, 7:113.
33. Maerkl S.J., Quake S.R. A systems approach to measuring the binding energy landscapes of transcription factors. Science 2007, 315:233-237.
34. Mann R.S., Chan S.K. Extra specificity from extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet. 1996, 12:258-262.
35. Morin B., Nichols L.A., Holland L.J. Flanking sequence composition differentially affects the binding and functional characteristics of glucocorticoid receptor homo- and heterodimers. Biochemistry 2006, 45:7299-7306.
36. Nagaoka M., Shiraishi Y., Sugiura Y. Selected base sequence outside the target binding site of zinc finger protein Sp1. Nucleic Acids Res. 2001, 29:4920-4929.
37. Neph S., Vierstra J., Stergachis A.B., Reynolds A.P., Haugen E., Vernot B., Thurman R.E., John S., Sandstrom R., Johnson A.K., et al. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 2012, 489:83-90.
38. Nishi K., Park C.S., Pepper A.E., Eichinger G., Innis M.A., Holland M.J. The GCR1 requirement for yeast glycolytic gene expression is suppressed by dominant mutations in the SGC1 gene, which encodes a novel basic-helix-loop-helix protein. Mol. Cell. Biol. 1995, 15:2646-2653.
39. Rajaram N., Kerppola T.K. DNA bending by Fos-Jun and the orientation of heterodimer binding depend on the sequence of the AP-1 site. EMBO J. 1997, 16:2917-2925.
40. Rohs R., Sklenar H., Shakked Z. Structural and energetic origins of sequence-specific DNA bending: Monte Carlo simulations of papillomavirus E2-DNA binding sites. Structure 2005, 13:1499-1509.
41. Rohs R., West S.M., Sosinsky A., Liu P., Mann R.S., Honig B. The role of DNA shape in protein-DNA recognition. Nature 2009, 461:1248-1253.
42. Rohs R., Jin X., West S.M., Joshi R., Honig B., Mann R.S. Origins of specificity in protein-DNA recognition. Annu. Rev. Biochem. 2010, 79:233-269.
43. Shimizu T., Toumoto A., Ihara K., Shimizu M., Kyogoku Y., Ogawa N., Oshima Y., Hakoshima T. Crystal structure of PHO4 bHLH domain-DNA complex: flanking base recognition. EMBO J. 1997, 16:4689-4697.
44. Siggers T., Duyzend M.H., Reddy J., Khan S., Bulyk M.L. Non-DNA-binding cofactors enhance DNA-binding specificity of a transcriptional regulatory complex. Mol. Syst. Biol. 2011, 7:555.
45. Slattery M., Riley T., Liu P., Abe N., Gomez-Alcala P., Dror I., Zhou T., Rohs R., Honig B., Bussemaker H.J., Mann R.S. Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell 2011, 147:1270-1282.
46. Thurman R.E., Rynes E., Humbert R., Vierstra J., Maurano M.T., Haugen E., Sheffield N.C., Stergachis A.B., Wang H., Vernot B., et al. The accessible chromatin landscape of the human genome. Nature 2012, 489:75-82.
47. Wang J., Zhuang J., Iyer S., Lin X., Whitfield T.W., Greven M.C., Pierce B.G., Dong X., Kundaje A., Cheng Y., et al. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 2012, 22:1798-1812.
48. Wei G.H., Badis G., Berger M.F., Kivioja T., Palin K., Enge M., Bonke M., Jolma A., Varjosalo M., Gehrke A.R., et al. Genome-wide analysis of ETS-family DNA-binding in vitro and in vivo. EMBO J. 2010, 29:2147-2160.
49. Wu Z., Delaglio F., Tjandra N., Zhurkin V.B., Bax A. Overall structure and sugar dynamics of a DNA dodecamer from homo- and heteronuclear dipolar couplings and 31P chemical shift anisotropy. J. Biomol. NMR 2003, 26:297-315.
50. Zhou X., O'Shea E.K. Integrated approaches reveal determinants of genome-wide binding and function of the transcription factor Pho4. Mol. Cell 2011, 42:826-836.
51. Zhu C., Byers K.J., McCord R.P., Shi Z., Berger M.F., Newburger D.E., Saulrieta K., Smith Z., Shah M.V., Radhakrishnan M., et al. High-resolution DNA-binding specificity analysis of yeast transcription factors. Genome Res. 2009, 19:556-566.