Diversification of transcription factor paralogs via noncanonical modularity in C2H2 Zinc finger DNA binding

Molecular Cell

Volumn 55, Issue 4, 2014, Pages 640-648

  Siggers, Trevor ^a,b   Reddy, Jessica ^a   Barron, Brian ^b   Bulyk, Martha L ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b Boston University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C2H2 ZINC FINGER PROTEIN; DNA; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ARTICLE; ASCOMYCETES; BINDING KINETICS; BINDING SITE; EVOLUTIONARY ADAPTATION; MOLECULAR RECOGNITION; NONHUMAN; PARALOGY; PLEIOTROPY; PROTEIN DNA BINDING;

AMINO ACID MOTIFS; ASCOMYCOTA; CONSERVED SEQUENCE; DNA, FUNGAL; DNA-BINDING PROTEINS; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENOME, FUNGAL; TRANSCRIPTION FACTORS; ZINC FINGERS;

EID: 84906790368     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.06.019     Document Type: Article

References (43)

1. Badis G., Chan E.T., van Bakel H., Pena-Castillo L., Tillo D., Tsui K., Carlson C.D., Gossett A.J., Hasinoff M.J., Warren C.L., et al. A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Mol. Cell 2008, 32:878-887.
2. Baker C.R., Tuch B.B., Johnson A.D. Extensive DNA-bindingspecificity divergence of a conserved transcription regulator. Proc. Natl. Acad. Sci. USA 2011, 108:7493-7498.
3. Beerli R.R., Segal D.J., Dreier B., Barbas C.F. Toward controlling gene expression at will: specific regulation of the erbB-2/HER-2 promoter by using polydactyl zinc finger proteins constructed from modular building blocks. Proc. Natl. Acad. Sci. USA 1998, 95:14628-14633.
4. Benos P.V., Lapedes A.S., Stormo G.D. Probabilistic code for DNA recognition by proteins of the EGR family. J.Mol. Biol. 2002, 323:701-727.
5. Berger M.F., Bulyk M.L. Protein binding microarrays (PBMs) for rapid, high-throughput characterization of the sequence specificities of DNA binding proteins. Methods Mol. Biol. 2006, 338:245-260.
6. Berger M.F., Bulyk M.L. Universal protein-binding microarrays forthe comprehensive characterization of the DNA-binding specificities of transcription factors. Nat. Protoc. 2009, 4:393-411.
7. Borneman A.R., Gianoulis T.A., Zhang Z.D., Yu H., Rozowsky J., Seringhaus M.R., Wang L.Y., Gerstein M., Snyder M. Divergence of transcription factor binding sites across related yeast species. Science 2007, 317:815-819.
8. Bradley R.K., Li X.Y., Trapnell C., Davidson S., Pachter L., Chu H.C., Tonkin L.A., Biggin M.D., Eisen M.B. Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species. PLoS Biol. 2010, 8:e1000343.
9. Choo Y., Klug A. Physical basis of a protein-DNA recognition code. Curr. Opin. Struct. Biol. 1997, 7:117-125.
10. Elrod-Erickson M., Rould M.A., Nekludova L., Pabo C.O. Zif268 protein-DNA complex refined at 1.6 A: a model system for understanding zinc finger-DNA interactions. Structure 1996, 4:1171-1180.
11. 2 zinc finger proteins reveals a multitude of novel recognition motifs and binding determinants. Genome Res. 2013, 23:928-940.
12. Gasch A.P., Moses A.M., Chiang D.Y., Fraser H.B., Berardini M., Eisen M.B. Conservation and evolution of cis-regulatory systems in ascomycete fungi. PLoS Biol. 2004, 2:e398.
13. 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.
14. Gupta A., Christensen R.G., Bell H.A., Goodwin M., Patel R.Y., Pandey M., Enuameh M.S., Rayla A.L., Zhu C., Thibodeau-Beganny S., et al. An improved predictive recognition model for Cys2-His2 zinc finger proteins. Nucleic Acids Res. 2014, 42:4800-4812.
15. Handel E.M., Alwin S., Cathomen T. Expanding or restricting thetarget site repertoire of zinc-finger nucleases: the inter-domain linker as a major determinant of target site selectivity. Mol. Ther. 2009, 17:104-111.
16. Isalan M., Choo Y., Klug A. Synergy between adjacent zinc fingers in sequence-specific DNA recognition. Proc. Natl. Acad. Sci. USA 1997, 94:5617-5621.
17. Jolma A., Yan J., Whitington T., Toivonen J., Nitta K.R., Rastas P., Morgunova E., Enge M., Taipale M., Wei G., et al. DNA-binding specificities of human transcription factors. Cell 2013, 152:327-339.
18. Kaplan T., Friedman N., Margalit H. Ab initio prediction of transcription factor targets using structural knowledge. PLoS Comput. Biol. 2005, 1:e1.
19. Klug A. The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu. Rev. Biochem. 2010, 79:213-231.
20. Lam K.N., van Bakel H., Cote A.G., van der Ven A., Hughes T.R. Sequence specificity is obtained from the majority of modular C2H2 zinc-finger arrays. Nucleic Acids Res. 2011, 39:4680-4690.
21. Liu J., Stormo G.D. Context-dependent DNA recognition code for C2H2 zinc-finger transcription factors. Bioinformatics 2008, 24:1850-1857.
22. Lynch V.J., Wagner G.P. Resurrecting the role of transcription factor change in developmental evolution. Evolution 2008, 62:2131-2154.
23. Mandel-Gutfreund Y., Margalit H. Quantitative parameters for amino acid-base interaction: implications for prediction of protein-DNA binding sites. Nucleic Acids Res. 1998, 26:2306-2312.
24. Martínez-Pastor M.T., Marchler G., Schüller C., Marchler-Bauer A., Ruis H., Estruch F. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J. 1996, 15:2227-2235.
25. Nakagawa, S., Gisselbrecht, S.S., Rogers, J.M., Hartl, D.L., and Bulyk, M.L. (2013). DNA-binding specificity changes in the evolution of forkhead transcription factors. Proceedings of the National Academy of Sciences of the United States of America. 110, 12349-12354.
26. Omichinski J.G., Pedone P.V., Felsenfeld G., Gronenborn A.M., Clore G.M. The solution structure of a specific GAGA factor-DNA complex reveals a modular binding mode. Nat. Struct. Biol. 1997, 4:122-132.
27. Persikov A.V., Singh M. An expanded binding model for Cys2His2 zinc finger protein-DNA interfaces. Phys. Biol. 2011, 8:035010.
28. Persikov A.V., Rowland E.F., Oakes B.L., Singh M., Noyes M.B. Deep sequencing of large library selections allows computational discovery of diverse sets of zinc fingers that bind common targets. Nucleic Acids Res. 2014, 42:1497-1508.
29. Ramirez C.L., Foley J.E., Wright D.A., Müller-Lerch F., Rahman S.H., Cornu T.I., Winfrey R.J., Sander J.D., Fu F., Townsend J.A., et al. Unexpected failure rates for modular assembly of engineered zinc fingers. Nat. Methods 2008, 5:374-375.
30. 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.
31. Schaufler L.E., Klevit R.E. Mechanism of DNA binding by the ADR1 zinc finger transcription factor as determined by SPR. J.Mol. Biol. 2003, 329:931-939.
32. Shiraishi Y., Imanishi M., Morisaki T., Sugiura Y. Swapping of thebeta-hairpin region between Sp1 and GLI zinc fingers: significant role of the beta-hairpin region in DNA binding properties of C2H2-type zinc finger peptides. Biochemistry 2005, 44:2523-2528.
33. Siggers T., Gordân R. Protein-DNA binding: complexities and multi-protein codes. Nucleic Acids Res. 2014, 42:2099-2111.
34. Siggers T.W., Honig B. Structure-based prediction of C2H2 zinc-finger binding specificity: sensitivity to docking geometry. Nucleic Acids Res. 2007, 35:1085-1097.
35. 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.
36. Thukral S.K., Morrison M.L., Young E.T. Alanine scanning site-directed mutagenesis of the zinc fingers of transcription factor ADR1: residues that contact DNA and that transactivate. Proc. Natl. Acad. Sci. USA 1991, 88:9188-9192.
37. Wang H., Mayhew D., Chen X., Johnston M., Mitra R.D. Calling Cards enable multiplexed identification of the genomic targets of DNA-binding proteins. Genome Res. 2011, 21:748-755.
38. Wapinski I., Pfeffer A., Friedman N., Regev A. Natural history and evolutionary principles of gene duplication in fungi. Nature 2007, 449:54-61.
39. Wilson M.D., Barbosa-Morais N.L., Schmidt D., Conboy C.M., Vanes L., Tybulewicz V.L., Fisher E.M., Tavaré S., Odom D.T. Species-specific transcription in mice carrying human chromosome 21. Science 2008, 322:434-438.
40. Wolfe S.A., Greisman H.A., Ramm E.I., Pabo C.O. Analysis of zinc fingers optimized via phage display: evaluating the utility of a recognition code. J.Mol. Biol. 1999, 285:1917-1934.
41. Wolfe S.A., Nekludova L., Pabo C.O. DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 2000, 29:183-212.
42. Zhao Y., Stormo G.D. Quantitative analysis demonstrates mosttranscription factors require only simple models of specificity. Nat. Biotechnol. 2011, 29:480-483.
43. 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-resolutionDNA-binding specificity analysis of yeast transcription factors. Genome Res. 2009, 19:556-566.