Widespread evidence of cooperative DNA binding by transcription factors in Drosophila development

Nucleic Acids Research

Volumn 41, Issue 17, 2013, Pages 8237-8252

  Kazemian, Majid ^a,b   Pham, Hannah ^c   Wolfe, Scot A ^c   Brodsky, Michael H ^c   Sinha, Saurabh ^a,d  

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

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; TRANSCRIPTION FACTOR;

ACCURACY; ARTICLE; BINDING AFFINITY; BINDING SITE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; GENE CONTROL; IN VITRO STUDY; INSECT DEVELOPMENT; MOLECULAR DYNAMICS; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS;

ANIMALS; BINDING SITES; DNA; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOMICS; PROTEIN BINDING; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

EID: 84884959191     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt598     Document Type: Article

References (78)

1. Levine,M. and Davidson,E.H. (2005) Gene regulatory networks for development. Proc. Natl Acad. Sci. USA, 102, 4936-4942.
2. Ip,Y.T., Park,R.E., Kosman,D., Yazdanbakhsh,K. and Levine,M. (1992) Dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo. Genes Dev., 6, 1518-1530.
3. Harrison,M.M., Li,X.Y., Kaplan,T., Botchan,M.R. and Eisen,M.B. (2011) Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transition. PLoS Genet., 7, e1002266.
4. Magnani,L., Eeckhoute,J. and Lupien,M. (2011) Pioneer factors: directing transcriptional regulators within the chromatin environment. Trends Genet., 27, 465-474.
5. Fakhouri,W.D., Ay,A., Sayal,R., Dresch,J., Dayringer,E. and Arnosti,D.N. (2010) Deciphering a transcriptional regulatory code: modeling short-range repression in the Drosophila embryo. Mol. Syst. Biol., 6, 341.
6. Mirny,L.A. (2010) Nucleosome-mediated cooperativity between transcription factors. Proc. Natl Acad. Sci. USA, 107, 22534-22539.
7. Arnosti,D.N., Gray,S., Barolo,S., Zhou,J. and Levine,M. (1996) The gap protein knirps mediates both quenching and direct repression in the Drosophila embryo. EMBO J., 15, 3659-3666. (Pubitemid 26239778)
8. Barolo,S. and Levine,M. (1997) hairy mediates dominant repression in the Drosophila embryo. EMBO J., 16, 2883-2891. (Pubitemid 27226224)
9. Johnson,A.D., Meyer,B.J. and Ptashne,M. (1979) Interactions between DNA-bound repressors govern regulation by the lambda phage repressor. Proc. Natl Acad. Sci. USA, 76, 5061-5065. (Pubitemid 10231821)
10. Ptashne,M. (1992) A Genetic Witch : Phage Lambd and Higher Organisms, 2nd edn. Cell Press: Blackwell Scientific Publications, Cambridge, MA.
11. Lelli,K.M., Slattery,M. and Mann,R.S. (2012) Disentangling the many layers of eukaryotic transcriptional regulation. Annu. Rev. Genet., 46, 43-68.
12. Kondoh,H. and Kamachi,Y. (2010) SOX-partner code for cell specification: Regulatory target selection and underlying molecular mechanisms. Int. J Biochem Cell Biol., 42, 391-399.
13. Hollenhorst,P.C., McIntosh,L.P. and Graves,B.J. (2011) Genomic and biochemical insights into the specificity of ETS transcription factors. Ann. Rev. Biochem., 80, 437-471.
14. Giot,L., Bader,J.S., Brouwer,C., Chaudhuri,A., Kuang,B., Li,Y., Hao,Y.L., Ooi,C.E., Godwin,B., Vitols,E. et al. (2003) A protein interaction map of Drosophila melanogaster. Science, 302, 1727-1736. (Pubitemid 37505730)
15. Guruharsha,K.G., Rual,J.F., Zhai,B., Mintseris,J., Vaidya,P., Vaidya,N., Beekman,C., Wong,C., Rhee,D.Y., Cenaj,O. et al. (2011) A protein complex network of Drosophila melanogaster. Cell, 147, 690-703.
16. Ito,T., Chiba,T., Ozawa,R., Yoshida,M., Hattori,M. and Sakaki,Y. (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl Acad. Sci. USA, 98, 4569-4574. (Pubitemid 32295017)
17. Yu,H., Braun,P., Yildirim,M.A., Lemmens,I., Venkatesan,K., Sahalie,J., Hirozane-Kishikawa,T., Gebreab,F., Li,N., Simonis,N. et al. (2008) High-quality binary protein interaction map of the yeast interactome network. Science, 322, 104-110.
18. Simonis,N., Rual,J.F., Carvunis,A.R., Tasan,M., Lemmens,I., Hirozane-Kishikawa,T., Hao,T., Sahalie,J.M., Venkatesan,K., Gebreab,F. et al. (2009) Empirically controlled mapping of the Caenorhabditis elegans protein-protein interactome network. Nat. Methods, 6, 47-54.
19. Whitington,T., Frith,M.C., Johnson,J. and Bailey,T.L. (2011) Inferring transcription factor complexes from ChIP-seq data. Nucleic Acids Res., 39, e98.
20. Braun,P., Tasan,M., Dreze,M., Barrios-Rodiles,M., Lemmens,I., Yu,H., Sahalie,J.M., Murray,R.R., Roncari,L., de Smet,A.S. et al. (2009) An experimentally derived confidence score for binary protein-protein interactions. Nat. Methods, 6, 91-97.
21. Varjosalo,M., Sacco,R., Stukalov,A., van Drogen,A., Planyavsky,M., Hauri,S., Aebersold,R., Bennett,K.L., Colinge,J., Gstaiger,M. et al. (2013) Interlaboratory reproducibility of largescale human protein-complex analysis by standardized AP-MS. Nat. Methods, 10, 307-314.
22. Ravasi,T., Suzuki,H., Cannistraci,C.V., Katayama,S., Bajic,V.B., Tan,K., Akalin,A., Schmeier,S., Kanamori-Katayama,M., Bertin,N. et al. (2010) An atlas of combinatorial transcriptional regulation in mouse and man. Cell, 140, 744-752.
23. Zhou,Q., Chipperfield,H., Melton,D.A. and Wong,W.H. (2007) A gene regulatory network in mouse embryonic stem cells. Proc. Natl Acad. Sci. USA, 104, 16438-16443. (Pubitemid 350211036)
24. He,X., Samee,M.A., Blatti,C. and Sinha,S. (2010) Thermodynamics-based models of transcriptional regulation by enhancers: the roles of synergistic activation, cooperative binding and short-range repression. PLoS Comput. Biol., 6, pii: e1000935.
25. Frith,M.C., Fu,Y., Yu,L., Chen,J.F., Hansen,U. and Weng,Z. (2004) Detection of functional DNA motifs via statistical overrepresentation. Nucleic Acids Res., 32, 1372-1381. (Pubitemid 38854738)
26. Roider,H.G., Manke,T., O'Keeffe,S., Vingron,M. and Haas,S.A. (2009) PASTAA: identifying transcription factors associated with sets of co-regulated genes. Bioinformatics, 25, 435-442.
27. Nunez-Corcuera,B., Birch,J.L., Yamada,Y. and Williams,J.G. (2012) Transcriptional repression by a bZIP protein regulates Dictyostelium prespore differentiation. PLoS One, 7, e29895.
28. Ng,C.K., Li,N.X., Chee,S., Prabhakar,S., Kolatkar,P.R. and Jauch,R. (2012) Deciphering the Sox-Oct partner code by quantitative cooperativity measurements. Nucleic Acids Res., 40, 4933-4941.
29. Kulakovskiy,I.V., Belostotsky,A.A., Kasianov,A.S., Esipova,N.G., Medvedeva,Y.A., Eliseeva,I.A. and Makeev,V.J. (2011) A deeper look into transcription regulatory code by preferred pair distance templates for transcription factor binding sites. Bioinformatics, 27, 2621-2624.
30. Hannenhalli,S. and Levy,S. (2002) Predicting transcription factor synergism. Nucleic Acids Res., 30, 4278-4284. (Pubitemid 35175195)
31. Papatsenko,D., Goltsev,Y. and Levine,M. (2009) Organization of developmental enhancers in the Drosophila embryo. Nucleic Acids Res., 37, 5665-5677.
32. Makeev,V.J., Lifanov,A.P., Nazina,A.G. and Papatsenko,D.A. (2003) Distance preferences in the arrangement of binding motifs and hierarchical levels in organization of transcription regulatory information. Nucleic Acids Res., 31, 6016-6026. (Pubitemid 37442327)
33. Yokoyama,K.D., Ohler,U. and Wray,G.A. (2009) Measuring spatial preferences at fine-scale resolution identifies known and novel cis-regulatory element candidates and functional motif-pair relationships. Nucleic Acids Res., 37, e92.
34. Lifanov,A.P., Makeev,V.J., Nazina,A.G. and Papatsenko,D.A. (2003) Homotypic regulatory clusters in Drosophila. Genome Res., 13, 579-588.
35. Gotea,V., Visel,A., Westlund,J.M., Nobrega,M.A., Pennacchio,L.A. and Ovcharenko,I. (2010) Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res., 20, 565-577.
36. Noyes,M.B., Meng,X., Wakabayashi,A., Sinha,S., Brodsky,M.H. and Wolfe,S.A. (2008) A systematic characterization of factors that regulate Drosophila segmentation via a bacterial one-hybrid system. Nucleic Acids Res., 36, 2547-2560. (Pubitemid 351659570)
37. Noyes,M.B., Christensen,R.G., Wakabayashi,A., Stormo,G.D., Brodsky,M.H. and Wolfe,S.A. (2008) Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell, 133, 1277-1289. (Pubitemid 351852912)
38. Enuameh,M.S., Asriyan,Y., Richards,A., Christensen,R.G., Hall,V.L., Kazemian,M., Zhu,C., Pham,H., Cheng,Q., Blatti,C. et al. (2013) Global analysis of Drosophila Cys2-His2 zinc finger proteins reveals a multitude of novel recognition motifs and binding determinants. Genome Res., 23, 928-940.
39. Zhu,L.J., Christensen,R.G., Kazemian,M., Hull,C.J., Enuameh,M.S., Basciotta,M.D., Brasefield,J.A., Zhu,C., Asriyan,Y., Lapointe,D.S. et al. (2011) FlyFactorSurvey: a database of Drosophila transcription factor binding specificities determined using the bacterial one-hybrid system. Nucleic Acids Res., 39, D111-D117.
40. Kazemian,M., Blatti,C., Richards,A., McCutchan,M., Wakabayashi-Ito,N., Hammonds,A.S., Celniker,S.E., Kumar,S., Wolfe,S.A., Brodsky,M.H. et al. (2010) Quantitative analysis of the Drosophila segmentation regulatory network using pattern generating potentials. PLoS Biol, 8, pii: e1000456.
41. Sinha,S., van Nimwegen,E. and Siggia,E.D. (2003) A probabilistic method to detect regulatory modules. Bioinformatics, 19(Suppl. 1), i292-i301.
42. Li,X.Y., Thomas,S., Sabo,P.J., Eisen,M.B., Stamatoyannopoulos,J.A. and Biggin,M.D. (2011) The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding. Genome Biol., 12, R34.
43. Li,X.Y., MacArthur,S., Bourgon,R., Nix,D., Pollard,D.A., Iyer,V.N., Hechmer,A., Simirenko,L., Stapleton,M., Luengo Hendriks,C.L. et al. (2008) Transcription factors bind thousands of active and inactive regions in the Drosophila blastoderm. PLoS Biol., 6, e27.
44. Kaplan,T., Li,X.Y., Sabo,P.J., Thomas,S., Stamatoyannopoulos,J.A., Biggin,M.D. and Eisen,M.B. (2011) Quantitative models of the mechanisms that control genome-wide patterns of transcription factor binding during early Drosophila development. PLoS Genet., 7, e1001290.
45. MacArthur,S., Li,X.Y., Li,J., Brown,J.B., Chu,H.C., Zeng,L., Grondona,B.P., Hechmer,A., Simirenko,L., Keranen,S.V. et al. (2009) Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions. Genome Biol., 10, R80.
46. Zinzen,R.P., Girardot,C., Gagneur,J., Braun,M. and Furlong,E.E. (2009) Combinatorial binding predicts spatio-temporal cisregulatory activity. Nature, 462, 65-70.
47. Nien,C.Y., Liang,H.L., Butcher,S., Sun,Y., Fu,S., Gocha,T., Kirov,N., Manak,J.R. and Rushlow,C. (2011) Temporal coordination of gene networks by Zelda in the early Drosophila embryo. PLoS Genet., 7, e1002339.
48. Celniker,S.E., Dillon,L.A., Gerstein,M.B., Gunsalus,K.C., Henikoff,S., Karpen,G.H., Kellis,M., Lai,E.C., Lieb,J.D., MacAlpine,D.M. et al. (2009) Unlocking the secrets of the genome. Nature, 459, 927-930.
49. Schuettengruber,B., Ganapathi,M., Leblanc,B., Portoso,M., Jaschek,R., Tolhuis,B., van Lohuizen,M., Tanay,A. and Cavalli,G. (2009) Functional anatomy of polycomb and trithorax chromatin landscapes in Drosophila embryos. PLoS Biol., 7, e13.
50. Benson,G. (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res., 27, 573-580. (Pubitemid 29210025)
51. Jurka,J. (2000) Repbase update: a database and an electronic journal of repetitive elements. Trends Genet., 16, 418-420. (Pubitemid 30665376)
52. Tomancak,P., Berman,B.P., Beaton,A., Weiszmann,R., Kwan,E., Hartenstein,V., Celniker,S.E. and Rubin,G.M. (2007) Global analysis of patterns of gene expression during Drosophila embryogenesis. Genome Biol., 8, R145.
53. Tomancak,P., Beaton,A., Weiszmann,R., Kwan,E., Shu,S., Lewis,S.E., Richards,S., Ashburner,M., Hartenstein,V., Celniker,S.E. et al. (2002) Systematic determination of patterns of gene expression during Drosophila embryogenesis. Genome Biol., 3, RESEARCH0088.
54. Gupta,S., Stamatoyannopoulos,J.A., Bailey,T.L. and Noble,W.S. (2007) Quantifying similarity between motifs. Genome Biol., 8, R24.
55. Warde-Farley,D., Donaldson,S.L., Comes,O., Zuberi,K., Badrawi,R., Chao,P., Franz,M., Grouios,C., Kazi,F., Lopes,C.T. et al. (2010) The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res., 38, W214-W220.
56. Stark,C., Breitkreutz,B.J., Chatr-Aryamontri,A., Boucher,L., Oughtred,R., Livstone,M.S., Nixon,J., Van Auken,K., Wang,X., Shi,X. et al. (2011) The BioGRID Interaction Database: 2011 update. Nucleic Acids Res., 39, D698-D704.
57. Grant,C.E., Bailey,T.L. and Noble,W.S. (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics, 27, 1017-1018.
58. Barrios-Rodiles,M., Brown,K.R., Ozdamar,B., Bose,R., Liu,Z., Donovan,R.S., Shinjo,F., Liu,Y., Dembowy,J., Taylor,I.W. et al. (2005) High-throughput mapping of a dynamic signaling network in mammalian cells. Science, 307, 1621-1625. (Pubitemid 40354744)
59. Vizoso Pinto,M.G., Villegas,J.M., Peter,J., Haase,R., Haas,J., Lotz,A.S., Muntau,A.C. and Baiker,A. (2009) LuMPIS-a modified luminescence-based mammalian interactome mapping pull-down assay for the investigation of protein-protein interactions encoded by GC-low ORFs. Proteomics, 9, 5303-5308.
60. Hallikas,O. and Taipale,J. (2006) High-throughput assay for determining specificity and affinity of protein-DNA binding interactions. Nat. Protoc., 1, 215-222.
61. Nourmohammad,A. and Lassig,M. (2011) Formation of regulatory modules by local sequence duplication. PLoS Comput. Biol., 7, e1002167.
62. Spitz,F. and Furlong,E.E. (2012) Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet, 13, 613-626.
63. Moyle-Heyrman,G., Tims,H.S. and Widom,J. (2011) Structural constraints in collaborative competition of transcription factors against the nucleosome. J. Mol. Biol., 412, 634-646.
64. Miller,J.A. and Widom,J. (2003) Collaborative competition mechanism for gene activation in vivo. Mol. Cell. Biol., 23, 1623-1632. (Pubitemid 36246044)
65. Granok,H., Leibovitch,B.A., Shaffer,C.D. and Elgin,S.C. (1995) Chromatin. Ga-ga over GAGA factor. Curr. Biol., 5, 238-241.
66. Lehmann,M. (2004) Anything else but GAGA: a nonhistone protein complex reshapes chromatin structure. Trends Genet., 20, 15-22. (Pubitemid 38032816)
67. Leibovitch,B.A., Lu,Q., Benjamin,L.R., Liu,Y., Gilmour,D.S. and Elgin,S.C. (2002) GAGA factor and the TFIID complex collaborate in generating an open chromatin structure at the Drosophila melanogaster hsp26 promoter. Mol. Cell. Biol., 22, 6148-6157. (Pubitemid 34857835)
68. Zaret,K.S. and Carroll,J.S. (2011) Pioneer transcription factors: establishing competence for gene expression. Genes Dev., 25, 2227-2241.
69. Okada,M. and Hirose,S. (1998) Chromatin remodeling mediated by Drosophila GAGA factor and ISWI activates fushi tarazu gene transcription in vitro. Mol. Cell. Biol., 18, 2455-2461. (Pubitemid 28183415)
70. Yanez-Cuna,J.O., Dinh,H.Q., Kvon,E.Z., Shlyueva,D. and Stark,A. (2012) Uncovering cis-regulatory sequence requirements for context-specific transcription factor binding. Genome Res., 22, 2018-2030.
71. Slattery,M., Riley,T., Liu,P., Abe,N., Gomez-Alcala,P., Dror,I., Zhou,T., Rohs,R., Honig,B., Bussemaker,H.J. et al. (2011) Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell, 147, 1270-1282.
72. Pan,Y. and Nussinov,R. (2009) Cooperativity dominates the genomic organization of p53-response elements: a mechanistic view. PLoS Comput. Biol., 5, e1000448.
73. Crocker,J., Tamori,Y. and Erives,A. (2008) Evolution acts on enhancer organization to fine-tune gradient threshold readouts. PLoS Biol., 6, e263.
74. Negre,N., Brown,C.D., Ma,L., Bristow,C.A., Miller,S.W., Wagner,U., Kheradpour,P., Eaton,M.L., Loriaux,P., Sealfon,R. et al. (2011) A cis-regulatory map of the Drosophila genome. Nature, 471, 527-531.
75. Jolma,A., Yan,J., Whitington,T., Toivonen,J., Nitta,K.R., Rastas,P., Morgunova,E., Enge,M., Taipale,M., Wei,G. et al. (2013) DNA-binding specificities of human transcription factors. Cell, 152, 327-339.
76. Kim,S., Brostromer,E., Xing,D., Jin,J., Chong,S., Ge,H., Wang,S., Gu,C., Yang,L., Gao,Y.Q. et al. (2013) Probing allostery through DNA. Science, 339, 816-819.
77. Klemm,J.D. and Pabo,C.O. (1996) Oct-1 POU domain-DNA interactions: cooperative binding of isolated subdomains and effects of covalent linkage. Genes Dev., 10, 27-36. (Pubitemid 26025296)
78. Rohs,R., Jin,X., West,S.M., Joshi,R., Honig,B. and Mann,R.S. (2010) Origins of specificity in protein-DNA recognition. Annu. Rev. Biochem., 79, 233-269.