DNA-dependent formation of transcription factor pairs alters their binding specificity

Nature

Volumn 527, Issue 7578, 2015, Pages 384-388

  Jolma, Arttu ^a   Yin, Yimeng ^a   Nitta, Kazuhiro R ^a   Dave, Kashyap ^a   Popov, Alexander ^b   Taipale, Minna ^a   Enge, Martin ^a   Kivioja, Teemu ^c   Morgunova, Ekaterina ^a   Taipale, Jussi ^a,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HETERODIMER; LIGAND; TRANSCRIPTION FACTOR;

CHEMICAL BINDING; COMPOSITE; CRYSTAL STRUCTURE; DNA; GENE EXPRESSION; GENOME; PROTEIN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING; DNA SEQUENCE; GENE EXPRESSION; HUMAN; HYDROGEN BOND; MOUSE; NONHUMAN; POSITION WEIGHT MATRIX; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA INTERACTION; PROTEIN PROTEIN INTERACTION; X RAY DIFFRACTION; AMINO ACID SEQUENCE; BINDING SITE; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE; REPRODUCIBILITY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA; GENE EXPRESSION REGULATION; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEOTIDE MOTIFS; REPRODUCIBILITY OF RESULTS; SUBSTRATE SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 84947717868     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature15518     Document Type: Article

References (74)

1. Shlyueva, D., Stampfel, G. & Stark, A. Transcriptional enhancers: from properties to genome-wide predictions. Nature Rev. Genet. 15, 272-286 (2014).
2. Levo, M. & Segal, E. In pursuit of design principles of regulatory sequences. Nature Rev. Genet. 15, 453-468 (2014).
3. Slattery, M. et al. Absence of a simple code: how transcription factors read the genome. Trends Biochem. Sci. 39, 381-399 (2014).
4. Rodda, D. J. et al. Transcriptional regulation of Nanog by OCT4 and SOX2. J. Biol. Chem. 280, 24731-24737 (2005).
5. Panne, D., Maniatis, T. & Harrison, S. C. An atomic model of the interferon-beta enhanceosome. Cell 129, 1111-1123 (2007).
6. De Val, S. et al. Combinatorial regulation of endothelial gene expression by Ets and Forkhead transcription factors. Cell 135, 1053-1064 (2008).
7. Badis, G. et al. Diversity and complexity in DNA recognition by transcription factors. Science 324, 1720-1723 (2009).
8. Jolma, A. et al. DNA-binding specificities of human transcription factors. Cell 152, 327-339 (2013).
9. Vaquerizas, J. M., Kummerfeld, S. K., Teichmann, S. A. & Luscombe, N. M. A census of human transcription factors: function, expression and evolution. Nature Rev. Genet. 10, 252-263 (2009).
10. Najafabadi, H. S. et al. C2H2 zinc finger proteins greatly expand the human regulatory lexicon. Nature Biotechnol. 33, 555-562 (2015).
11. Emery, P. et al. A consensus motif in the RFX DNA binding domain and binding domain mutants with altered specificity. Mol. Cell. Biol. 16, 4486-4494 (1996).
12. Kurokawa, R. et al. Differential orientations of the DNA-binding domain and carboxy-terminal dimerization interface regulate binding site selection by nuclear receptor heterodimers. Genes Dev. 7, 1423-1435 (1993).
13. Mohibullah, N., Donner, A., Ippolito, J. A. & Williams, T. SELEX and missing phosphate contact analyses reveal flexibility within the AP-2α protein: DNA binding complex. Nucleic Acids Res. 27, 2760-2769, (1999).
14. Slattery, M. et al. Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell 147, 1270-1282 (2011).
15. Grove, C. A. et al. A multiparameter network reveals extensive divergence between C. elegans bHLH transcription factors. Cell 138, 314-327 (2009).
16. Nitta, K. R. et al. Conservation of transcription factor binding specificities across 600 million years of bilateria evolution. eLife 4, e04837 (2015).
17. Kim, S. et al. Probing allostery through DNA. Science 339, 816-819 (2013).
18. Rhee, H. S. & Pugh, B. F. Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution. Cell 147, 1408-1419 (2011).
19. Yan, J. et al. Transcription factor binding in human cells occurs in dense clusters formed around cohesin anchor sites. Cell 154, 801-813 (2013).
20. Guturu, H., Doxey, A. C., Wenger, A. M. & Bejerano, G. Structure-aided prediction of mammalian transcription factor complexes in conserved non-coding elements. Phil. Trans. R. Soc. Lond. B 368, 20130029 (2013).
21. Wei, G. H. et al. Genome-wide analysis of ETS-family DNA-binding in vitro and in vivo. EMBO J. 29, 2147-2160 (2010).
22. Mirny, L. A. Nucleosome-mediated cooperativity between transcription factors. Proc. Natl Acad. Sci. USA 107, 22534-22539 (2010).
23. Wasson, T. & Hartemink, A. J. An ensemble model of competitive multi-factor binding of the genome. Genome Res. 19, 2101-2112 (2009).
24. Poss, Z. C., Ebmeier, C. C. & Taatjes, D. J. The Mediator complex and transcription regulation. Crit. Rev. Biochem. Mol. Biol. 48, 575-608 (2013).
25. Kagey, M. H. et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467, 430-435 (2010).
26. Nishizawa, M. & Nagata, S. cDNA clones encoding leucine-zipper proteins which interact with G-CSF gene promoter element 1-binding protein. FEBS Lett. 299, 36-38 (1992).
27. Shen, W. F. et al. AbdB-like Hox proteins stabilize DNA binding by the Meis1 homeodomain proteins. Mol. Cell. Biol. 17, 6448-6458 (1997).
28. Williams, D. C., Jr, Cai, M. & Clore, G. M. Molecular basis for synergistic transcriptional activation by Oct1 and Sox2 revealed from the solution structure of the 42-kDa Oct1·Sox2·Hoxb1-DNA ternary transcription factor complex. J. Biol. Chem. 279, 1449-1457 (2004).
29. Cohen, S. X. et al. Structure of the GCM domain-DNA complex: a DNA-binding domain with a novel fold and mode of target site recognition. EMBO J. 22, 1835-1845 (2003).
30. Mo, Y., Vaessen, B., Johnston, K. & Marmorstein, R. Structure of the Elk-1-DNA complex reveals how DNA-distal residues affect ETS domain recognition of DNA. Nature Struct. Mol. Biol. 7, 292-297 (2000).
31. Jolma, A. et al. Multiplexed massively parallel SELEX for characterization of human transcription factor binding specificities. Genome Res. 20, 861-873 (2010).
32. Katainen, R. et al. CTCF/cohesion-binding sites are frequently mutated in cancer. Nature Genetics 47, 818-821 (2015).
33. Guo, Y. et al. Discovering homotypic binding events at high spatial resolution. Bioinformatics 26, 3028-3034 (2010).
34. Passner, J. M., Ryoo, H. D., Shen, L., Mann, R. S. & Aggarwal, A. K. Structure of a DNA-bound Ultrabithorax-Extradenticle homeodomain complex. Nature 397, 714-719 (1999).
35. Vincentelli, R. et al. High-throughput protein expression screening and purification in Escherichia coli. Methods 55, 65-72 (2011).
36. Keshava Prasad, T. S. et al. Human Protein Reference Database-2009 update. Nucleic Acids Res. 37, D767-D772 (2009).
37. Ravasi, T. et al. An atlas of combinatorial transcriptional regulation in mouse and man. Cell 140, 744-752 (2010).
38. Newman, J. R. & Keating, A. E. Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science 300, 2097-2101 (2003).
39. Klemm, J. D. & Pabo, C. O. Oct-1 POU domain-DNA interactions: cooperative binding of isolated subdomains and effects of covalent linkage. Genes Dev. 10, 27-36 (1996).
40. Panne, D., Maniatis, T. & Harrison, S. C. Crystal structure of ATF-2/c-Jun and IRF-3 bound to the interferon-β enhancer. EMBO J. 23, 4384-4393 (2004).
41. Rigaut, G. et al. A generic protein purification method for protein complex characterization and proteome exploration. Nature Biotechnol. 17, 1030-1032 (1999).
42. Hallikas, O. et al. Genome-wide prediction of mammalian enhancers based on analysis of transcription-factor binding affinity. Cell 124, 47-59 (2006).
43. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235-242 (2011).
44. Moorman, C. et al. Hotspots of transcription factor colocalization in the genome of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 103, 12027-12032 (2006).
45. Yip, K. Y. et al. Classification of human genomic regions based on experimentally determined binding sites of more than 100 transcription-related factors. Genome Biol. 13, R48 (2012).
46. Meireles-Filho, A. C., Bardet, A. F., Yanez-Cuna, J. O., Stampfel, G. & Stark, A. cis-regulatory requirements for tissue-specific programs of the circadian clock. Curr. Biol. 24, 1-10 (2014).
47. Löytynoja, A. & Goldman, N. An algorithm for progressive multiple alignment of sequences with insertions. Proc. Natl Acad. Sci. USA 102, 10557-10562 (2005).
48. Pape, U. J., Rahmann, S. & Vingron, M. Natural similarity measures between position frequency matrices with an application to clustering. Bioinformatics 24, 350-357 (2008).
49. Odrowaz, Z. & Sharrocks, A. D. The ETS transcription factors ELK1 and GABPA regulate different gene networks to control MCF10A breast epithelial cell migration. PLoS ONE 7, e49892 (2012).
50. Huang, Q. et al. A prostate cancer susceptibility allele at 6q22 increases RFX6 expression by modulating HOXB13 chromatin binding. Nature Genet. 46, 126-135, doi: 10.1038/ng.2862 (2014).
51. Huang, Y. et al. Identification and characterization of Hoxa9 binding sites in hematopoietic cells. Blood 119, 388-398 (2012).
52. Penkov, D. et al. Analysis of the DNA-binding profile and function of TALE homeoproteins reveals their specialization and specific interactions with Hox genes/proteins. Cell Reports 3, 1321-1333, (2013).
53. Lindblad-Toh, K. et al. A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478, 476-482 (2011).
54. Korhonen, J., Martinmaki, P., Pizzi, C., Rastas, P. & Ukkonen, E. MOODS: fast search for position weight matrix matches in DNA sequences. Bioinformatics 25, 3181-3182 (2009).
55. Garber, M. et al. Identifying novel constrained elements by exploiting biased substitution patterns. Bioinformatics 25, i54-i62 (2009).
56. Blanchette, M. et al. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res. 14, 708-715 (2004).
57. Savitsky, P. et al. High-throughput production of human proteins for crystallization: the SGC experience. J. Struct. Biol. 172, 3-13 (2010).
58. Bourenkov, G. P. & Popov, A. N. A quantitative approach to data-collection strategies. Acta Crystallogr. D 62, 58-64 (2006).
59. Kabsch, W. Xds. Acta Crystallogr. D 66, 125-132 (2010).
60. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
61. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
62. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
63. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
64. Fitzsimmons, D. et al. Pax-5 (BSAP) recruits Ets proto-oncogene family proteins to form functional ternary complexes on a B-cell-specific promoter. Genes Dev. 10, 2198-2211 (1996).
65. Kim, J. J. et al. Regulation of insulin-like growth factor binding protein-1 promoter activity by FKHR and HOXA10 in primate endometrial cells. Biol. Reprod. 68, 24-30 (2003).
66. Vinson, C. R., Hai, T. & Boyd, S. M. Dimerization specificity of the leucine zipper-containing bZIP motif on DNA binding: prediction and rational design. Genes Dev. 7, 1047-1058 (1993).
67. Williams, T. M., Williams, M. E. & Innis, J. W. Range of HOX/TALE superclass associations and protein domain requirements for HOXA13:MEIS interaction. Dev. Biol. 277, 457-471 (2005).
68. Melnikov, A. et al. Systematic dissection and optimization of inducible enhancers in human cells using a massively parallel reporter assay. Nature Biotechnol. 30, 271-277 (2012).
69. Raveh-Sadka, T. et al. Manipulating nucleosome disfavoring sequences allows fine-tune regulation of gene expression in yeast. Nature Genet. 44, 743-750 (2012).
70. Hochschild, A. & Ptashne, M. Cooperative binding of ë repressors to sites separated by integral turns of the DNA helix. Cell 44, 681-687 (1986).
71. Moretti, R. et al. Targeted chemical wedges reveal the role of allosteric DNA modulation in protein-DNA assembly. ACS Chem. Biol. 3, 220-229 (2008).
72. Aggarwal, A. K., Rodgers, D. W., Drottar, M., Ptashne, M. & Harrison, S. C. Recognition of a DNA operator by the repressor of phage 434: a view at high resolution. Science 242, 899-907 (1988).
73. Jordan, S. R. & Pabo, C. O. Structure of the lambda complex at 2.5Å resolution: details of the repressor-operator interactions. Science 242, 893-899 (1988).
74. Rohs, R. et al. Origins of specificity in protein-DNA recognition. Annu. Rev. Biochem. 79, 233-269 (2010).