A combination of computational and experimental approaches identifies DNA sequence constraints associated with target site binding specificity of the transcription factor CSL

Nucleic Acids Research

Volumn 42, Issue 16, 2014, Pages 10550-10563

  Torella, Rubben ^a   Li, Jinghua ^a   Kinrade, Eddie ^a,b   Cerda Moya, Gustavo ^a   Contreras, Ashley N ^c   Foy, Robert ^a,b   Stojnic, Robert ^a,b   Glen, Robert C ^a   Kovall, Rhett A ^c   Adryan, Boris ^a,b   Bray, Sarah J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEOPROTEIN; DNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CSL; UNCLASSIFIED DRUG; CYTOSINE; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; PROTEIN BINDING; RBPJ PROTEIN, MOUSE;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; COMPUTER MODEL; COMPUTER PREDICTION; CONTROLLED STUDY; DNA SEQUENCE; IN VITRO STUDY; IN VIVO STUDY; MATHEMATICAL ANALYSIS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN FUNCTION; SIMULATION; CHEMISTRY; COMPUTER PROGRAM; COMPUTER SIMULATION; CONSENSUS SEQUENCE; METABOLISM; NUCLEOTIDE MOTIF; REGULATORY SEQUENCE;

BINDING SITES; COMPUTER SIMULATION; CONSENSUS SEQUENCE; CYTOSINE; DNA; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; MOLECULAR DYNAMICS SIMULATION; NUCLEOTIDE MOTIFS; PROTEIN BINDING; REGULATORY ELEMENTS, TRANSCRIPTIONAL; SOFTWARE;

EID: 84921341502     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku730     Document Type: Article

References (62)

1. Rohs, R., Jin, X.S., West, S.M., Joshi, R., Honig, B., and Mann, R.S.Rohs, R., Jin, X.S., 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.
2. Rohs, R., West, S.M., Liu, P., and Honig, B.Rohs, R., West, S.M., Liu, P., and Honig, B. (2009) Nuance in the double-helix and its role in protein-DNA recognition. Curr. Opin. Struc. Biol., 19, 171-177.
3. Rohs, R., West, S.M., Sosinsky, A., Liu, P., Mann, R.S., and Honig, B.Rohs, R., West, S.M., Sosinsky, A., Liu, P., Mann, R.S., and Honig, B. (2009) The role of DNA shape in protein-DNA recognition. Nature, 461, 1248-1253.
4. Seeman, N.C., Rosenberg, J.M., and Rich, A.Seeman, N.C., Rosenberg, J.M., and Rich, A. (1976) Sequence-specific recognition of double helical nucleic-acids by proteins. Proc. Natl Acad. Sci. U.S.A., 73, 804-808.
5. Otwinowski, Z., Schevitz, R.W., Zhang, R.G., Lawson, C.L., Joachimiak, A., Marmorstein, R.Q., Luisi, B.F., and Sigler, P.B.Otwinowski, Z., Schevitz, R.W., Zhang, R.G., Lawson, C.L., Joachimiak, A., Marmorstein, R.Q., Luisi, B.F., and Sigler, P.B. (1988) Crystal-structure of Trp repressor operator complex at atomic resolution. Nature, 335, 321-329.
6. Kovall, R.A. and Blacklow, S.C.Kovall, R.A. and Blacklow, S.C. (2010) Mechanistic insights into Notch receptor signaling from structural and biochemical studies. Curr. Top. Dev. Biol., 92, 31-71.
7. Doyle, T.G., Wen, C.H., and Greenwald, I.Doyle, T.G., Wen, C.H., and Greenwald, I. (2000) SEL-8, a nuclear protein required for LIN-12 and GLP-1 signaling in Caenorhabditis elegans. Proc. Natl Acad. Sci. U.S.A., 97, 7877-7881.
8. Petcherski, A.G. and Kimble, J.Petcherski, A.G. and Kimble, J. (2000) LAG-3 is a putative transcriptional activator in the C-elegans Notch pathway. Nature, 405, 364-368.
9. Nam, Y., Weng, A.P., Aster, J.C., and Blacklow, S.C.Nam, Y., Weng, A.P., Aster, J.C., and Blacklow, S.C. (2003) Structural requirements for assembly of the CSL center dot Intracellular Notch1 center dot Mastermind-like 1 transcriptional activation complex. J. Biol. Chem., 278, 21232-21239.
10. Wilson, J.J. and Kovall, R.A. Wilson, J.J. and Kovall, R.A. (2006) Crystal structure of the CSL-Notch-Mastermind ternary complex bound to DNA. Cell, 124, 985-996.
11. Mathelier, A., Zhao, X., Zhang, A.W., Parcy, F., Worsley-Hunt, R., Arenillas, D.J., Buchman, S., Chen, C.Y., Chou, A., and Ienasescu, H.Mathelier, A., Zhao, X., Zhang, A.W., Parcy, F., Worsley-Hunt, R., Arenillas, D.J., Buchman, S., Chen, C.Y., Chou, A., and Ienasescu, H. (2013) JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res., 42, D142-D147.
12. Bryne, J.C., Valen, E., Tang, M.H., Marstrand, T., Winther, O., da Piedade, I., Krogh, A., Lenhard, B., and Sandelin, A.Bryne, J.C., Valen, E., Tang, M.H., Marstrand, T., Winther, O., da Piedade, I., Krogh, A., Lenhard, B., and Sandelin, A. (2008) JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update. Nucleic Acids Res., 36, D102-D106.
13. Fryer, C.J., Lamar, E., Turbachova, I., Kintner, C., and Jones, K.A.Fryer, C.J., Lamar, E., Turbachova, I., Kintner, C., and Jones, K.A. (2002) Mastermind mediates chromatin-specific transcription and turnover of the Notch enhancer complex. Genes Dev., 16, 1397-1411.
14. Wallberg, A.E., Pedersen, K., Lendahl, U., and Roeder, R.G.Wallberg, A.E., Pedersen, K., Lendahl, U., and Roeder, R.G. (2002) p300 and PCA act cooperatively to mediate transcriptional activation from chromatin templates by Notch intracellular domains in vitro. Mol. Cell. Biol., 22, 7812-7819.
15. Kovall, R.A. and Hendrickson, W.A.Kovall, R.A. and Hendrickson, W.A. (2004) Crystal structure of the nuclear effector of Notch signaling, CSL, bound to DNA. EMBO J., 23, 3441-3451.
16. Nam, Y., Sliz, P., Song, L., Aster, J.C., and Blacklow, S.C.Nam, Y., Sliz, P., Song, L., Aster, J.C., and Blacklow, S.C. (2006) Structural basis for cooperativity in recruitment of MAML coactivators to Notch transcription complexes. Cell, 124, 973-983.
17. Friedmann, D.R., Wilson, J.J., and Kovall, R.A.Friedmann, D.R., Wilson, J.J., and Kovall, R.A. (2008) RAM-induced allostery facilitates assembly of a notch pathway active transcription complex. J. Biol. Chem., 283, 14781-14791.
18. Kurth, P., Preiss, A., Kovall, R.A., and Maier, D.Kurth, P., Preiss, A., Kovall, R.A., and Maier, D. (2011) Molecular analysis of the Notch repressor-complex in Drosophila: characterization of potential hairless binding sites on suppressor of hairless. Plos One, 6, e27986.
19. Del Bianco, C., Vedenko, A., Choi, S.H., Berger, M.F., Shokri, L., Bulyk, M.L., and Blacklow, S.C.Del Bianco, C., Vedenko, A., Choi, S.H., Berger, M.F., Shokri, L., Bulyk, M.L., and Blacklow, S.C. (2010) Notch and MAML-1 complexation do not detectably alter the DNA binding specificity of the transcription factor CSL. Plos One, 5, e15034.
20. Sali, A. and Blundell, T.L.Sali, A. and Blundell, T.L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol., 234, 779-815.
21. Fiser, A., Do, R.K., and Sali, A.Fiser, A., Do, R.K., and Sali, A. (2000) Modeling of loops in protein structures. Protein Sci., 9, 1753-1773.
22. Li, H., Robertson, A.D., and Jensen, J.H.Li, H., Robertson, A.D., and Jensen, J.H. (2005) Very fast empirical prediction and rationalization of protein pK(a) values. Proteins, 61, 704-721.
23. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C.Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C. (2006) Comparison of multiple amber force fields and development of improved protein backbone parameters. Proteins, 65, 712-725.
24. Guerois, R., Nielsen, J.E., and Serrano, L.Guerois, R., Nielsen, J.E., and Serrano, L. (2002) Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J. Mol. Biol., 320, 369-387.
25. Nadra, A.D., Serrano, L., and Alibes, A.Nadra, A.D., Serrano, L., and Alibes, A. (2011) DNA-binding specificity prediction with FoldX. Methods Enzymol., 498, 3-18.
26. Crooks, G.E., Hon, G., Chandonia, J.M., and Brenner, S.E.Crooks, G.E., Hon, G., Chandonia, J.M., and Brenner, S.E. (2004)WebLogo: a sequence logo generator. Genome Res., 14, 1188-1190.
27. Case, D.A., Cheatham, T.E.I., Darden, T.A., Gholke, R., Luo, R., Merz, K.M., Onufriev, A., Simmerling, C.L., Wang, J., and Woods, R.Case, D.A., Cheatham, T.E.I., Darden, T.A., Gholke, R., Luo, R., Merz, K.M., Onufriev, A., Simmerling, C.L., Wang, J., and Woods, R. (2005) J. Computat. Chem., pp. 1668-1688.
28. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C.Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins, 65, 712-725.
29. Götz, A.W., Williamson, M.J., Xu, D., Poole, D., Le Grand, S., and Walker, R.C. Götz, A.W., Williamson, M.J., Xu, D., Poole, D., Le Grand, S., and Walker, R.C. (2012) Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. Generalized born. J. Chem. Theory Comput., 8, 1542-1555.
30. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., and Klein, M.L.Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., and Klein, M.L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926-935.
31. Berendsen, H.J.C., Postma, J.P.M., Vangunsteren, W.F., Dinola, A., and Haak, J.R.Berendsen, H.J.C., Postma, J.P.M., Vangunsteren, W.F., Dinola, A., and Haak, J.R. (1984) Molecular-dynamics with coupling to an external bath. J. Chem. Phys., 81, 3684-3690.
32. Torella, R., Moroni, E., Caselle, M., Morra, G., and Colombo, G.Torella, R., Moroni, E., Caselle, M., Morra, G., and Colombo, G. (2010) Investigating dynamic and energetic determinants of protein nucleic acid recognition: analysis of the zinc finger zif268-DNA complexes. BMC Struct. Biol., 10, 42.
33. Ragona, L., Colombo, G., Catalano, M., and Molinari, H.Ragona, L., Colombo, G., Catalano, M., and Molinari, H. (2005) Determinants of protein stability and folding: comparative analysis of beta-lactoglobulins and liver basic fatty acid binding protein. Proteins, 61, 366-376.
34. Perera, R.L., Torella, R., Klinge, S., Kilkenny, M.L., Maman, J.D., and Pellegrini, L.Perera, R.L., Torella, R., Klinge, S., Kilkenny, M.L., Maman, J.D., and Pellegrini, L. (2013) Mechanism for priming DNA synthesis by yeast DNA polymerase alpha. eLife, 2, e00482.
35. Morra, G., Potestio, R., Micheletti, C., and Colombo, G.Morra, G., Potestio, R., Micheletti, C., and Colombo, G. (2012) Corresponding functional dynamics across the Hsp90 chaperone family: insights from a multiscale analysis of MD simulations. Plos Comput. Biol., 8, e1002433.
36. Morra, G., Verkhivker, G., and Colombo, G.Morra, G., Verkhivker, G., and Colombo, G. (2009) Modeling signal propagation mechanisms and ligand-based conformational dynamics of the Hsp90 molecular chaperone full-length dimer. PLoS Comput. Biol., 5, e1000323.
37. Pagano, K., Torella, R., Foglieni, C., Bugatti, A., Tomaselli, S., Zetta, L., Presta, M., Rusnati, M., Taraboletti, G., and Colombo, G. et al.Pagano, K., Torella, R., Foglieni, C., Bugatti, A., Tomaselli, S., Zetta, L., Presta, M., Rusnati, M., Taraboletti, G., and Colombo, G. ((2012)) Direct and allosteric inhibition of the FGF2/HSPGs/FGFR1 ternary complex formation by an antiangiogenic, thrombospondin-1-mimic small molecule. Plos One, 7, e36990.
38. Brou, C., Logeat, F., Lecourtois, M., Vandekerckhove, J., Kourilsky, P., Schweisguth, F., and Israel, A.Brou, C., Logeat, F., Lecourtois, M., Vandekerckhove, J., Kourilsky, P., Schweisguth, F., and Israel, A. (1994) Inhibition of the DNA-binding activity of Drosophila suppressor of hairless and of its human homolog, Kbf2/Rbp-J-Kappa, by direct protein-protein interaction with Drosophila hairless. Genes Dev., 8, 2491-2503.
39. Krejci, A. and Bray, S.Krejci, A. and Bray, S. (2007) Notch activation stimulates transient and selective binding of Su(H)/CSL to target enhancers. Genes Dev., 21, 1322-1327.
40. Furriols, M. and Bray, S.Furriols, M. and Bray, S. (2000) Dissecting the mechanisms of suppressor of hairless function. Dev. Biol., 227, 520-532.
41. Housden, B., Millen, K., and Bray, S.J.Housden, B., Millen, K., and Bray, S.J. (2012) Drosophila reporter vectors compatible with Phi C31 integrase transgenesis techniques and their use to generate new Notch reporter fly lines. G3 (Bethesda), 2, 79-82.
42. Bischof, J., Maeda, R.K., Hediger, M., Karch, F., and Basler, K.Bischof, J., Maeda, R.K., Hediger, M., Karch, F., and Basler, K. (2007) An optimized transgenesis system for Drosophila using germ-line-specific phi C31 integrases. Proc. Natl Acad. Sci. U.S.A., 104, 3312-3317.
43. Schweisguth, F. and Posakony, J.W.Schweisguth, F. and Posakony, J.W. (1992) Suppressor of hairless, the Drosophila homolog of the mouse recombination signal binding-protein gene, controls sensory organ cell fates. Cell, 69, 1199-1212.
44. Friedmann, D.R. and Kovall, R.A.Friedmann, D.R. and Kovall, R.A. (2010) Thermodynamic and structural insights into CSL-DNA complexes. Protein Sci., 19, 34-46.
45. Lai, E.C., Bodner, R., and Posakony, J.W.Lai, E.C., Bodner, R., and Posakony, J.W. (2000) The enhancer of split complex of Drosophila includes four Notch-regulated members of the Bearded gene family. Development, 127, 3441-3455.
46. Schymkowitz, J.W.H., Rousseau, F., Martins, I.C., Ferkinghoff-Borg, J., Stricher, F., and Serrano, L.Schymkowitz, J.W.H., Rousseau, F., Martins, I.C., Ferkinghoff-Borg, J., Stricher, F., and Serrano, L. (2005) Prediction of water and metal binding sites and their affinities by using the Fold-X force field. Proc. Natl Acad. Sci. U.S.A., 102, 10147-10152.
47. Alibes, A., Nadra, A.D., De Masi, F., Bulyk, M.L., Serrano, L., and Stricher, F.Alibes, A., Nadra, A.D., De Masi, F., Bulyk, M.L., Serrano, L., and Stricher, F. (2010) Using protein design algorithms to understand the molecular basis of disease caused by protein-DNA interactions: the Pax6 example. Nucleic Acids Res., 38, 7422-7431.
48. Daily, K., Patel, V.R., Rigor, P., Xie, X., and Baldi, P.Daily, K., Patel, V.R., Rigor, P., Xie, X., and Baldi, P. (2011) MotifMap: integrative genome-wide maps of regulatory motif sites for model species. BMC Bioinformatics, 12, 495.
49. Xie, X., Rigor, P., and Baldi, P.Xie, X., Rigor, P., and Baldi, P. (2009) MotifMap: a human genome-wide map of candidate regulatory motif sites. Bioinformatics, 25, 167-174.
50. Meng, X., Brodsky, M.H., and Wolfe, S.A.Meng, X., Brodsky, M.H., and Wolfe, S.A. (2005) A bacterial one-hybrid system for determining the DNA-binding specificity of transcription factors. Nat. Biotechnol., 23, 988-994.
51. Hertz, G.Z. and Stormo, G.D.Hertz, G.Z. and Stormo, G.D. (1999) Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics, 15, 563-577.
52. Nellesen, D.T., Lai, E.C., and Posakony, J.W.Nellesen, D.T., Lai, E.C., and Posakony, J.W. (1999) Discrete enhancer elements mediate selective responsiveness of enhancer of split complex genes to common transcriptional activators. Dev. Biol., 213, 33-53.
53. Tun, T., Hamaguchi, Y., Matsunami, N., Furukawa, T., Honjo, T., and Kawaichi, M.Tun, T., Hamaguchi, Y., Matsunami, N., Furukawa, T., Honjo, T., and Kawaichi, M. (1994) Recognition sequence of a highly conserved DNA binding protein RBP-J kappa. Nucleic Acids Res., 22, 965-971.
54. Tsuda, L., Kaido, M., Lim, Y.M., Kato, K.K., Aigaki, T.S., and Hayashi, S.G.Tsuda, L., Kaido, M., Lim, Y.M., Kato, K.K., Aigaki, T.S., and Hayashi, S.G. (2006) An NRSF/REST-like repressor downstream of Ebi/SMRTER/Su(H) regulates eye development in Drosophila. EMBO J., 25, 3191-3202.
55. Arnett, K.L., Hass, M., McArthur, D.G., Ilagan, M.X.G., Aster, J.C., Kopan, R., and Blacklow, S.C.Arnett, K.L., Hass, M., McArthur, D.G., Ilagan, M.X.G., Aster, J.C., Kopan, R., and Blacklow, S.C. (2010) Structural and mechanistic insights into cooperative assembly of dimeric Notch transcription complexes. Nat. Struct. Mol. Biol., 17, 1312-1317.
56. Morra, G., Potestio, R., Micheletti, C., and Colombo, G.Morra, G., Potestio, R., Micheletti, C., and Colombo, G. (2012) Corresponding functional dynamics across the Hsp90 Chaperone family: insights from a multiscale analysis of MD simulations. PLoS Comput. Biol., 8, e1002433.
57. Stormo, G.D.Stormo, G.D. (2000) DNA binding sites: representation and discovery. Bioinformatics, 16, 16-23.
58. Stormo, G.D. and Zhao, Y.Stormo, G.D. and Zhao, Y. (2010) Determining the specificity of protein-DNA interactions. Nat. Rev. Genet., 11, 751-760.
59. Ma, B.Y., Tsai, C.J., Pan, Y.P., and Nussinov, R.Ma, B.Y., Tsai, C.J., Pan, Y.P., and Nussinov, R. (2010) Why does binding of proteins to DNA or proteins to proteins not necessarily spell function. ACS Chem. Biol., 5, 265-272.
60. Biggin, M.D.Biggin, M.D. (2011) Animal transcription networks as highly connected, quantitative continua. Dev. Cell, 21, 611-626.
61. Weinkam, P., Pons, J., and Sali, A.Weinkam, P., Pons, J., and Sali, A. (2012) Structure-based model of allostery predicts coupling between distant sites. Proc. Natl Acad. Sci. U.S.A., 109, 4875-4880.
62. Siggers, T. and Gordan, R.Siggers, T. and Gordan, R. (2013) Protein-DNA binding: complexities and multi-protein codes. Nucleic Acids Res., 42, 2099-2111.