Engineering transcription factors with novel DNA-binding specificity using comparative genomics

Nucleic Acids Research

Volumn 37, Issue 8, 2009, Pages 2493-2503

  Desai, Tasha A ^a   Rodionov, Dmitry A ^b,c   Gelfand, Mikhail S ^c,d   Alm, Eric J ^e   Rao, Christopher V ^a  

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

^b BURNHAM INSTITUTE   (United States)

^c INSTITUTE FOR INFORMATION TRANSMISSION PROBLEMS   (Russian Federation)

^d MOSCOW STATE UNIVERSITY   (Russian Federation)

^e Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ARGININE; BETA GALACTOSIDASE; CYCLIC AMP RECEPTOR; FUMARATE NITRATE REDUCTASE REGULATORY PROTEIN; FUMARATE REDUCTASE; GLUTAMINE; GREEN FLUORESCENT PROTEIN; NITRATE REDUCTASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BINDING SITE; CLOSTRIDIUM; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; DESULFOVIBRIO; DNA TEMPLATE; ESCHERICHIA COLI; GENE MUTATION; GENETIC ENGINEERING; MUTAGENESIS; NONHUMAN; OPERATOR GENE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; REPORTER GENE; SEQUENCE ALIGNMENT; TREPONEMA;

AMINO ACID SUBSTITUTION; CYCLIC AMP RECEPTOR PROTEIN; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; GENES, REPORTER; GENOMICS; IRON-SULFUR PROTEINS; MUTATION; OPERATOR REGIONS, GENETIC; PROTEIN ENGINEERING; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 65849228838     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp079     Document Type: Article

References (63)

1. Browning,D.F. and Busby,S.J. (2004) The regulation of bacterial transcription initiation. Nat. Rev. Microbiol., 2, 57-65.
2. Pabo,C.O. and Sauer,R.T. (1992) Transcription factors: Structural families and principles of DNA recognition. Annu. Rev. Biochem., 61, 1053-1095.
3. Rhodes,D., Schwabe,J.W., Chapman,L. and Fairall,L. (1996) Towards an understanding of protein-DNA recognition. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 351, 501-509.
4. Sarai,A. and Kono,H. (2005) Protein-DNA recognition patterns and predictions. Annu. Rev. Biophys. Biomol. Struct., 34, 379-398.
5. Kaern,M., Blake,W.J. and Collins,J.J. (2003) The engineering of gene regulatory networks. Annu. Rev. Biomed. Eng., 5, 179-206.
6. Haseltine,E.L. and Arnold,F.H. (2007) Synthetic gene circuits: Design with directed evolution. Annu. Rev. Biophys. Biomol. Struct., 36, 1-19.
7. Voigt,C.A. (2006) Genetic parts to program bacteria. Curr. Opin. Biotechnol., 17, 548-557.
8. Khosla,C. and Keasling,J.D. (2003) Metabolic engineering for drug discovery and development. Nat. Rev. Drug Discov., 2, 1019-1025.
9. Isalan,M., Lemerle,C., Michalodimitrakis,K., Horn,C., Beltrao,P., Raineri,E., Garriga-Canut,M. and Serrano,L. (2008) Evolvability and hierarchy in rewired bacterial gene networks. Nature, 452, 840-845.
10. Gardner,T.S., Cantor,C.R. and Collins,J.J. (2000) Construction of a genetic toggle switch in Escherichia coli. Nature, 403, 339-342.
11. Kobayashi,H., Kaern,M., Araki,M., Chung,K., Gardner,T.S., Cantor,C.R. and Collins,J.J. (2004) Programmable cells: Interfacing natural and engineered gene networks. Proc. Natl Acad. Sci. USA, 101, 8414-8419.
12. Collins,C.H., Yokobayashi,Y., Umeno,D. and Arnold,F.H. (2003) Engineering proteins that bind, move, make and break DNA. Curr. Opin. Biotechnol., 14, 665.
13. Wharton,R.P., Brown,E.L. and Ptashne,M. (1984) Substituting an alpha-helix switches the sequence-specific DNA interactions of a repressor. Cell, 38, 361-369.
14. Wharton,R.P. and Ptashne,M. (1985) Changing the binding specificity of a repressor by redesigning an alpha-helix. Nature, 316, 601-605.
15. Youderian,P., Vershon,A., Bouvier,S., Sauer,R.T. and Susskind,M.M. (1983) Changing the DNA-binding specificity of a repressor. Cell, 35, 777-783.
16. Ebright,R.H., Cossart,P., Gicquel-Sanzey,B. and Beckwith,J. (1984) Mutations that alter the DNA sequence specificity of the catabolite gene activator protein of E. coli. Nature, 311, 232-235.
17. Beerli,R.R. and Barbas,C.F.3rd. (2002) Engineering polydactyl zinc-finger transcription factors. Nat. Biotechnol., 20, 135-141.
18. Liolios,K., Mavromatis,K., Tavernarakis,N. and Kyrpides,N.C. (2008) The Genomes On Line Database (GOLD) in 2007: Status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res., 36, D475-D479.
19. Pabo,C.O. and Nekludova,L. (2000) Geometric analysis and comparison of protein-DNA interfaces: Why is there no simple code for recognition? J. Mol. Biol., 301, 597-624.
20. Rodionov,D.A., Dubchak,I.L., Arkin,A.P., Alm,E.J. and Gelfand,M.S. (2005) Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. PLoS Comput. Biol., 1, e55.
21. Korner,H., Sofia,H.J. and Zumft,W.G. (2003) Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: Exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol. Rev., 27, 559-592.
22. Lawson,C.L., Swigon,D., Murakami,K.S., Darst,S.A., Berman,H.M. and Ebright,R.H. (2004) Catabolite activator protein: DNA binding and transcription activation. Curr. Opin. Struct. Biol., 14, 10-20.
23. Siggers,T.W., Silkov,A. and Honig,B. (2005) Structural alignment of protein-DNA interfaces: Insights into the determinants of binding specificity. J. Mol. Biol., 345, 1027-1045.
24. Morozov,A.V. and Siggia,E.D. (2007) Connecting protein structure with predictions of regulatory sites. Proc. Natl Acad. Sci. USA, 104 7068-7073.
25. Mandel-Gutfreund,Y., Baron,A. and Margalit,H. (2001) A structure-based approach for prediction of protein binding sites in gene upstream regions. Pac. Symp. Biocomput., 139-150
26. Datsenko,K.A. and Wanner,B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA, 97, 6640-6645.
27. Stemmer,W.P. and Morris,S.K. (1992) Enzymatic inverse PCR: A restriction site independent, single-fragment method for high-efficiency, site-directed mutagenesis. Biotechniques, 13, 214-220.
28. Kazakov,A.E., Cipriano,M.J., Novichkov,P.S., Minovitsky,S., Vinogradov,D.V., Arkin,A., Mironov,A.A., Gelfand,M.S. and Dubchak,I. (2007) RegTransBase - a database of regulatory sequences and interactions in a wide range of prokaryotic genomes. Nucleic Acids Res., 35, D407-D412.
29. Rodionov,D.A., Dubchak,I., Arkin,A., Alm,E. and Gelfand,M.S. (2004) Reconstruction of regulatory and metabolic pathways in metal-reducing delta-proteobacteria. Genome Biol., 5, R90.
30. Busby,S. and Ebright,R.H. (1999) Transcription activation by catabolite activator protein (CAP). J. Mol. Biol., 293, 199-213.
31. Zhang,X.P. and Ebright,R.H. (1990) Identification of a contact between arginine-180 of the catabolite gene activator protein (CAP) and base pair 5 of the DNA site in the CAP-DNA complex. Proc. Natl Acad. Sci. USA, 87, 4717-4721.
32. Ebright,R.H., Kolb,A., Buc,H., Kunkel,T.A., Krakow,J.S. and Beckwith,J. (1987) Role of glutamic acid-181 in DNA-sequence recognition by the catabolite gene activator protein (CAP) of Escherichia coli: Altered DNA-sequence-recognition properties of [Val181]CAP and [Leu181]CAP. Proc. Natl Acad. Sci. USA, 84, 6083-6087.
33. Livingstone,C.D. and Barton,G.J. (1996) Identification of functional residues and secondary structure from protein multiple sequence alignment. Methods Enzymol., 266, 497-512.
34. Kalinina,O.V., Mironov,A.A., Gelfand,M.S. and Rakhmaninova,A.B. (2004) Automated selection of positions determining functional specificity of proteins by comparative analysis of orthologous groups in protein families. Protein Sci., 13, 443-456.
35. Mirny,L.A. and Gelfand,M.S. (2002) Using orthologous and paralogous proteins to identify specificity-determining residues in bacterial transcription factors. J. Mol. Biol., 321, 7-20.
36. Szurmant,H., Bobay,B.G., White,R.A., Sullivan,D.M., Thompson,R.J., Hwa,T., Hoch,J.A. and Cavanagh,J. (2008) Co-evolving motions at protein-protein interfaces of two-component signaling systems identified by covariance analysis. Biochemistry., 47, 7782-7784.
37. White,R.A., Szurmant,H., Hoch,J.A. and Hwa,T. (2007) Features of protein-protein interactions in two-component signaling deduced from genomic libraries. Methods Enzymol., 422, 75-101.
38. Skerker,J.M., Perchuk,B.S., Siryaporn,A., Lubin,E.A., Ashenberg,O., Goulian,M. and Laub,M.T. (2008) Rewiring the specificity of two-component signal transduction systems. Cell, 133, 1043-1054.
39. Li,L., Shakhnovich,E.I. and Mirny,L.A. (2003) Amino acids determining enzyme-substrate specificity in prokaryotic and eukaryotic protein kinases. Proc. Natl Acad. Sci. USA, 100, 4463-4468.
40. Skerker,J.M., Prasol,M.S., Perchuk,B.S., Biondi,E.G. and Laub,M.T. (2005) Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: A system-level analysis. PLoS Biol., 3, e334.
41. Zheng,D., Constantinidou,C., Hobman,J.L. and Minchin,S.D. (2004) Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res., 32, 5874-5893.
42. Lozada-Chavez,I., Angarica,V.E., Collado-Vides,J. and Contreras-Moreira,B. (2008) The role of DNA-binding specificity in the evolution of bacterial regulatory networks. J. Mol. Biol., 379 627-643.
43. Lassig,M. (2007) From biophysics to evolutionary genetics: Statistical aspects of gene regulation. BMC Bioinformatics, 8(Suppl. 6 , S7.
44. Mustonen,V. and Lassig,M. (2005) Evolutionary population genetics of promoters: Predicting binding sites and functional phylogenies. Proc. Natl Acad. Sci. USA, 102, 15936-15941.
45. Arkin,A.P. and Fletcher,D.A. (2006) Fast, cheap and somewhat in control. Genome Biol., 7, 114.
46. Channon,K., Bromley,E.H. and Woolfson,D.N. (2008) Synthetic biology through biomolecular design and engineering. Curr. Opin. Struct. Biol., 18, 491-498.
47. Chin,J.W. (2006) Modular approaches to expanding the functions of living matter. Nat. Chem. Biol., 2, 304-311.
48. Aiba,H. (1983) Autoregulation of the Escherichia coli crp gene: CRP is a transcriptional repressor for its own gene. Cell, 32, 141-149.
49. Polayes,D.A., Rice,P.W., Garner,M.M. and Dahlberg,J.E. (1988) Cyclic AMP-cyclic AMP receptor protein as a repressor of transcription of the spf gene of Escherichia coli. J. Bacteriol., 170, 3110-3114.
50. Teichmann,S.A. and Babu,M.M. (2004) Gene regulatory network growth by duplication. Nat. Genet., 36, 492-496.
51. Price,M.N., Dehal,P.S. and Arkin,A.P. (2008) Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli. Genome Biol., 9, R4.
52. Rodionov,D.A., Gelfand,M.S., Todd,J.D., Curson,A.R. and Johnston,A.W. (2006) Computational reconstruction of iron- and manganese-responsive transcriptional networks in alpha-proteobacteria. PLoS Comput. Biol. 2, e163.
53. Berg,J., Willmann,S. and Lassig,M. (2004) Adaptive evolution of transcription factor binding sites. BMC Evol. Biol., 4, 42.
54. Price,M.N., Dehal,P.S. and Arkin,A.P. (2007) Orthologous transcription factors in bacteria have different functions and regulate different genes. PLoS Comput. Biol., 3, 1739-1750.
55. Ravcheev,D.A., Gerasimova,A.V., Mironov,A.A. and Gelfand,M.S. (2007) Comparative genomic analysis of regulation of anaerobic respiration in ten genomes from three families of gamma-proteobacteria (Enterobacteriaceae, Pasteurellaceae, Vibrionaceae). BMC Genomics, 8, 54.
56. Ritzenthaler,P., Blanco,C. and Mata-Gilsinger,M. (1983) Interchangeability of repressors for the control of the uxu and uid operons in E. coli K12. Mol. Gen. Genet., 191, 263-270.
57. Rodionov,D.A., Mironov,A.A., Rakhmaninova,A.B. and Gelfand,M.S. (2000) Transcriptional regulation of transport and utilization systems for hexuronides, hexuronates and hexonates in gamma purple bacteria. Mol. Microbiol., 38, 673-683.
58. Geanacopoulos,M. and Adhya,S. (1997) Functional characterization of roles of GalR and GalS as regulators of the gal regulon. J. Bacteriol., 179, 228-234.
59. Semsey,S., Krishna,S., Sneppen,K. and Adhya,S. (2007) Signal integration in the galactose network of Escherichia coli. Mol. Microbiol., 65, 465-476.
60. Darwin,A.J., Tyson,K.L., Busby,S.J. and Stewart,V. (1997) Differential regulation by the homologous response regulators NarL and NarP of Escherichia coli K-12 depends on DNA binding site arrangement. Mol. Microbiol., 25, 583-595.
61. Stewart,V. and Bledsoe,P.J. (2003) Synthetic lac operator substitutions for studying the nitrate- and nitrite-responsive NarX-NarL and NarQ-NarP two-component regulatory systems of Escherichia coli K-12. J. Bacteriol., 185, 2104-2111.
62. Wang,H. and Gunsalus,R.P. (2000) The nrfA and nirB nitrite reductase operons in Escherichia coli are expressed differently in response to nitrate than to nitrite. J. Bacteriol., 182, 5813-5822.
63. Wang,H. and Gunsalus,R.P. (2003) Coordinate regulation of the Escherichia coli formate dehydrogenase fdnGHI and fdhF genes in response to nitrate, nitrite, and formate: Roles for NarL and NarP. J. Bacteriol., 185, 5076-5085.