Discovery of Fur binding site clusters in Escherichia coli by information theory models

Nucleic Acids Research

Volumn 35, Issue 20, 2007, Pages 6762-6777

  Chen, Zehua ^a,h   Lewis, Karen A ^a,e   Shultzaberger, Ryan K ^a,f   Lyakhov, Ilya G ^a,b   Zheng, Ming ^c,g   Doan, Bernard ^c,d   Storz, Gisela ^c   Schneider, Thomas D ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g DUPONT COMPANY   (United States)

^h BOSTON COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; DIMER; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; FERRIC UPTAKE REGULATOR; REPRESSOR PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BINDING SITE; CLUSTER ANALYSIS; CONTROLLED STUDY; DNA FOOTPRINTING; DNA HELIX; ESCHERICHIA COLI; GENE ACTIVATION; GENETIC CONSERVATION; IRON METABOLISM; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA; SEQUENCE ANALYSIS; THEORETICAL MODEL;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; DNA FOOTPRINTING; ESCHERICHIA COLI; MODELS, BIOLOGICAL; PSEUDOMONAS AERUGINOSA; REPRESSOR PROTEINS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA;

EID: 36749031105     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm631     Document Type: Article

References (81)

1. Stojiljkovic,I., Baumler,A.J. and Hantke,K. (1994) Fur regulon in gram-negative bacteria. Identification and characterization of new iron-regulated Escherichia coli genes by a fur titration assay [published erratum appears in J. Mol. Biol. 1994 Jul 15;240(3):271]. J. Mol Biol., 236, 531-545.
2. Le Cam,E., Frechon,D., Barray,M., Fourcade,A. and Delain,E. (1994) Observation of binding and polymerization of Fur repressor onto operator-containing DNA with electron and atomic force microscopes. Proc. Natl Acad. Sci. USA, 91, 11816-11820.
3. Calderwood,S.B. and Mekalanos,J.J. (1987) Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus. J. Bacteriol., 169, 4759-4764.
4. Niederhoffer,E.C., Naranjo,C.M., Bradley,K.L. and Fee,J.A. (1990) Control of Escherichia coli superoxide dismutase (sodA and sodB) genes by the ferric uptake regulation (fur) locus. J. Bacteriol., 172, 1930-1938.
5. Escolar,L., Perez-Martin,J. and de Lorenzo,V. (1998) Binding of the Fur (Ferric Uptake Regulator) repressor of Escherichia coli to arrays of the GATAAT sequence. J. Mol. Biol., 283, 537-547.
6. Bagg,A. and Neilands,J.B. (1987) Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry, 26, 5471-5477.
7. de Lorenzo,V., Wee,S., Herrero,M. and Neilands,J.B. (1987) Operator sequences of the aerobactin operon of plasmid CoIV-K30 binding the ferric uptake regulation (fur) repressor. J. Bacteriol., 169, 2624-2630.
8. Althaus,E.W., Outten,C.E., Olson,K.E., Cao,H. and O'Halloran,T.V. (1999) The ferric uptake regulation (Fur) repressor is a zinc metalloprotein. Biochemistry, 38, 6559-6569.
9. Pohl,E., Haller,J.C., Mijovilovich,A., Meyer-Klaucke,W., Garman,E. and Vasil,M.L. (2003) Architecture of a protein central to iron homeostasis: crystal structure and spectroscopic analysis of the ferric uptake regulator. Mol. Microbiol., 47, 903-915.
10. Kammler,M., Schon,C. and Hantke,K. (1993) Characterization of the ferrous iron uptake system of Escherichia coli. J. Bacteriol., 175, 6212-6219.
11. Desai,P.J., Angerer,A. and Genco,C.A. (1996) Analysis of Fur binding to operator sequences within the Neisseria gonorrhoeae fbp A promoter. J. Bacteriol., 178, 5020-5023.
12. Heidrich,C., Hantke,K., Bierbaum,G. and Sahl,H.G. (1996) Identification and analysis of a gene encoding a Fur-like protein of Staphylococcus epidermidis. FEMS Microbiol. Lett., 140, 253-259.
13. McHugh,J.P., Rodriguez-Quinones,F., Abdul-Tehrani,H., Svistunenko,D.A., Poole,R.K., Cooper,C.E. and Andrews,S.C. (2003) Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. J. Biol Chem., 278, 29478-29486.
14. Shannon,C.E. (1948) A mathematical theory of communication. Bell Syst. Tech. J., 27, 379-423, 623-656. http://cm.bell-labs.com/ cm/ms/what/shannonday/paper.html
15. Pierce,J.R. (1980) An Introduction to Information Theory: Symbols, Signals and Noise, 2nd edn Dover Publications, Inc., New York.
16. Schneider,T.D., Stormo,G.D., Gold,L. and Ehrenfeucht,A. (1986) Information content of binding sites on nucleotide sequences. J. Mol. Biol., 188, 415-431. http://www.ccmp.ncifcrf.gov/~toms/paper/ schneider1986/
17. Schneider,T.D. and Mastronarde,D. (1996) Fast multiple alignment of ungapped DNA sequences using information theory and a relaxation method. Discrete Appli. Math., 71, 259-268. http://www.ccmp.ncifcrf.gov/~toms/paper/malign
18. Schneider,T.D. and Stephens,R.M. (1990) Sequence logos: A new way to display consensus sequences. Nucleic Acids Res., 18, 6097-6100. http://www.ccrnp.ncifcrf.gov/~toms/paper/logopaper/
19. Schneider,T.D. (1997) Information content of individual genetic sequences. J. Theor Biol., 189, 427-441. http://www.ccrnp.ncifcrf.gov/~toms/paper/ri/
20. Schneider,T.D. (1997) Sequence walkers: A graphical method to display how binding proteins interact with DNA or RNA sequences. Nucleic Acids Res., 25, 4408-4415. http://www.ccrnp.ncifcrf.gov/~toms/ paper/walker/, erratum: NAR 26(4): 1135, 1998.
21. Panina,E.M., Mironov,A.A. and Gelfand,M.S. (2001) Comparative analysis of FUR regulons in gamma-proteobacteria. Nucleic Acids Res., 29 5195-5206.
22. Schneider,T.D. (2000) Evolution of biological information. Nucleic Acids Res., 28, 2794-2799. http://www.ccrnp.ncifcrf.gov/~toms/ paper/ev/
23. Vyhlidal,C.A., Rogan,P.K. and Leeder,J.S. (2004) Development and refinement of pregnane X receptor (PXR) DNA binding site model using information theory: Insights into PXR-mediated gene regulation. J. Biol Chem., 279, 46779-46786.
24. Zheng,M., Doan,B., Schneider,T.D. and Storz,G. (1999) OxyR and SoxRS regulation of fur. J. Bacteriol., 181, 4639-4643. http://www.ccrnp.ncifcrf.gov/~toms/paper/oxyrfur/
25. Hengen,P.N., Bartram,S.L., Stewart,L.E. and Schneider,T.D. (1997) Information analysis of Fis binding sites. Nucleic Acids Res., 25, 4994-5002. http://www.ccrnp.ncifcrf.gov/~toms/paper/fisinfo/
26. Wood,T.I., Griffith,K.L., Fawcett,W.P., Jair, K.-W., Schneider,T.D. and Wolf,R.E. (1999) Interdependence of the position and orientation of SoxS binding sites in the transcriptional activation of the class I subset of Escherichia coli superoxide-inducible promoters. Mol. Microbiol., 34, 414-430.
27. Zheng,M., Wang,X., Doan,B., Lewis,K.A., Schneider,T.D. and Storz,G. (2001) Computation-directed identification of OxyR-DNA binding sites in Escherichia coli. J. Bacteriol., 183, 4571-4579.
28. Rogan,P.K., Faux,B.M. and Schneider,T.D. (1998) Information analysis of human splice site mutations. Hum. Mutat., 12, 153-171. Erratum in: Hum Mutat 1999;13(1):82. http://www.ccrnp.ncifcrf.gov/~toms/ paper/rfs/
29. Chen,Z. and Schneider,T.D. (2005) Information theory based T7-like promoter models: Classification of bacteriophages and differential evolution of promoters and their polymerases. Nucleic Acids Res., 33, 6172-6187. http://www.ccrnp.ncifcrf.gov/~toms/papers/t7like/
30. Chen,Z. and Schneider,T.D. (2006) Comparative analysis of tandem T7-like promoter containing regions in enterobacterial genomes reveals a novel group of genetic islands. Nucleic Acids Res., 34, 1133-1147. http://www.ccmp.ncifcrf.gov/~toms/papers/t7island/
31. Schneider,T.D. (1996) Reading of DNA sequence logos: Prediction of major groove binding by information theory. Meth. Enzymol, 274, 445-455. http://www.ccrnp.ncifcrf.gov/~toms/paper/oxyr/
32. Griggs,D.W. and Konisky,J. (1989) Mechanism for iron-regulated transcription of the Escherichia coli cir gene: Metal-dependent binding of Fur protein to the promoters. J. Bacteriol., 171, 1048-1052.
33. Angerer,A. and Braun,V. (1998) Iron regulates transcription of the Escherichia coli ferric citrate transport genes directly and through the transcription initiation proteins. Arch. Microbiol., 169 483-490.
34. de Lorenzo,V., Herrero,M., Giovannini,F. and Neilands,J.B. (1988) Fur (ferric uptake regulation) protein and CAP (catabolite-activator protein) modulate transcription of fur gene in Escherichia coli. Eur. J. Biochem., 173, 537-546.
35. Hunt,M.D., Pettis,G.S. and McIntosh,M.A. (1994) Promoter and operator determinants for fur-mediated iron regulation in the bidirectional fepA-fes control region of the Escherichia coli enterobactin gene system. J. Bacteriol., 176, 3944-3955.
36. Tardat,B. and Touati,D. (1993) Iron and oxygen regulation of Escherichia coli MnSOD expression: Competition between the global regulators Fur and ArcA for binding to DNA. Mol. Microbiol., 9 53-63.
37. Escolar,L., Perez-Martin,J. and de Lorenzo,V. (2000) Evidence of an unusually long operator for the fur repressor in the aerobactin promoter of Escherichia coli. J. Biol. Chem., 275, 24709-24714.
38. Young,G.M. and Postle,K. (1994) Repression of tonB transcription during anaerobic growth requires Fur binding at the promoter and a second factor binding upstream. Mol. Microbiol., 11, 943-954.
39. Brickman,T.J., Ozenberger,B.A. and McIntosh,M.A. (1990) Regulation of divergent transcription from the iron-responsive fepB-entC promoter-operator regions in Escherichia coli. J. Mol. Biol., 212, 669-682.
40. Baichoo,N. and Helmann,J.D. (2002) Recognition of DNA by Fur: A reinterpretation of the Fur box consensus sequence. J. Bacteriol., 184, 5826-5832.
41. Ochsner,U.A. and Vasil,M.L. (1996) Gene repression by the ferric uptake regulator in Pseudomonas aeruginosa: Cycle selection of iron-regulated genes. Proc. Natl Acad. Sci. USA, 93, 4409-4414.
42. Baichoo,N., Wang,T., Ye,R. and Helmann,J.D. (2002) Global analysis of the Bacillus subtilis Fur regulon and the iron starvation stimulon. Mol. Microbiol., 45, 1613-1629.
43. Christoffersen,C.A., Brickman,T.J., Hook-Barnard,I. and McIntosh,M.A. (2001) Regulatory architecture of the iron-regulated fepD-ybdA bidirectional promoter region in Escherichia coli. J. Bacteriol., 183, 2059-2070.
44. Chai,S., Welch,T.J. and Crosa,J.H. (1998) Characterization of the interaction between Fur and the iron transport promoter of the virulence plasmid in Vibrio anguillarum. J. Biol. Chem., 273, 33841-33847.
45. Escolar,L., Perez-Martin,J. and de Lorenzo,V. (1998) Coordinated repression in vitro of the divergent fepA-fes promoters of Escherichia coli by the iron uptake regulation (Fur) protein. J. Bacteriol., 180, 2579-2582.
46. Escolar,L., de Lorenzo,V. and Perez-Martin,J. (1997) Metalloregulation in vitro of the aerobactin promoter of Escherichia coli by the Fur (ferric uptake regulation) protein. Mol. Microbiol., 26, 799-808.
47. 70 promoters. Nucleic Acids Res., 35, 771-788. http://www.ccrnp.ncifcrf.gov/~toms/paper/flexprom/
48. Shultzaberger,R.K., Bucheimer,R.E., Rudd,K.E. and Schneider,T.D. (2001) Anatomy of Escherichia coli ribosome binding sites. J. Mol Biol., 313, 215-228. http://www.ccrnp.ncifcrf.gov/~toms/ paper/flexrbs/
49. Hirao,I., Kawai,G., Yoshizawa,S., Nishimura,Y., Ishido,Y., Watanabe,K. and Miura,K. (1994) Most compact hairpin-turn structure exerted by a short DNA fragment, d(GCGAAGC) in solution: An extraordinarily stable structure resistant-to nucleases and heat. Nucleic Acids Res., 22, 576-582.
50. Eick-Helmerich,K. and Braun,V. (1989) Import of biopolymers into Escherichia coli: Nucleotide sequences of the exbB and exbD genes are homologous to those of the tolQ and tolR genes, respectively. J. Bacteriol., 171, 5117-5126.
51. Vassinova,N. and Kozyrev,D. (2000) A method for direct cloning of Fur-regulated genes: Identification of seven new Fur-regulated loci in Escherichia coli. Microbiology, 146, 3171-3182.
52. Toledano,M.B., Kullik,I., Trinh,F., Baird,P.T., Schneider,T.D. and Storz,G. (1994) Redox-dependent shift of OxyR-DNA contacts along an extended DNA binding site: A mechanism for differential promoter selection. Cell, 78, 897-909.
53. Blattner,F.R., Plunkett,G. III, Bloch,C.A., Perna,N.T., Burland,V., Riley,M., Collado-Vides,J., Glasner,J.D., Rode,C.K. et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277, 1453-1474.
54. Bagg,A. and Neilands,J.B. (1987) Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol. Rev., 51, 509-518.
55. Lavrrar,J.L. and McIntosh,M.A. (2003) Architecture of a Fur binding site: A comparative analysis. J. Bacteriol., 185, 2194-2202.
56. Orchard,K. and May,G.E. (1993) An EMSA-based method for determining the molecular weight of a protein - DNA complex. Nucleic Acids Res., 21, 3335-3336.
57. Masse,E. and Gottesman,S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl Acad. Sci USA, 99, 4620-4625.
58. Lavrrar,J.L., Christoffersen,C.A. and McIntosh,M.A. (2002) Fur-DNA interactions at the bidirectional fepDGC-entS promoter region in Escherichia coli. J. Mol. Biol., 322, 983-995.
59. Delany,I., Rappuoli,R. and Scarlato,V. (2004) Fur functions as an activator and as a repressor of putative virulence genes in Neisseria meningitidis. Mol. Microbiol., 52, 1081-1090.
60. Masse,E., Vanderpool,C.K. and Gottesman,S. (2005) Effect of RyhB small RNA on global iron use in Escherichia coli. J. Bacteriol., 187 6962-6971.
61. Argaman,L., Hershberg,R., Vogel,J., Bejerano,G., Wagner,E.G., Margalit,H. and Altuvia,S. (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr. Biol., 11, 941-950.
62. Wassarman,K.M., Repoila,F., Rosenow,C., Storz,G. and Gottesman,S. (2001) Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev., 15, 1637-1651.
63. Robison,K., McGuire,A.M. and Church,G.M. (1998) A comprehensive library of DNA-binding site matrices for 55 proteins applied to the complete Escherichia coli K-12 genome. J. Mol. Biol., 284, 241-254.
64. Salgado,H., Santos-Zavaleta,A., Gama-Castro,S., Milian-Zarate,D., Diaz-Peredo,E., Sanchez-Solano,F., Perez-Rueda,E., Bonavides-Martinez,C. and Collado-Vides,J. (2001) RegulonDB (version 3.2): Transcriptional regulation and operon organization in Escherichia coli K-12. Nucleic Acids Res., 29, 72-74.
65. Andrews,S.C., Robinson,A.K. and Rodriguez-Quinones,F. (2003) Bacterial iron homeostasis. FEMS Microbiol. Rev., 27, 215-237.
66. Schneider,T.D. (2002) Consensus Sequence Zen. Appl. Bioinformatics 1, 111-119. http://www.ccrnp.ncifcrf.gov/~toms/papers/zen/
67. Rudd,K.E. and Schneider,T.D. (1992) Compilation of E. coli ribosome binding sites. In Miller,J.H. (ed.), A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, Cold Spring Harbor Laboratory Press, New York, pp. 17.19-17.45.
68. Hengen,P.N., Lyakhov,I.G., Stewart,L.E. and Schneider,T.D. (2003) Molecular flip-flops formed by overlapping Fis sites. Nucleic Acids Res., 31, 6663-6673.
69. Fee,J.A. (1991) Regulation of sod genes in Escherichia coli: relevance to superoxide dismutase function. Mol. Microbiol., 5 2599-2610.
70. Igarashi,K., Saisho,T., Yuguchi,M. and Kashiwagi,K. (1997) Molecular mechanism of polyamine stimulation of the synthesis of oligopeptide-binding protein. J. Biol. Chem., 272, 4058-4064.
71. Yoshida,M., Meksuriyen,D., Kashiwagi,K., Kawai,G. and Igarashi,K. (1999) Polyamine stimulation of the synthesis of oligopeptide-binding protein (OppA). Involvement of a structural change of the Shine-Dalgarno sequence and the initiation codon aug in oppa mRNA. J. Biol. Chem. 274, 22723-22728.
72. Litwin,C.M. and Calderwood,S.B. (1993) Role of iron in regulation of virulence genes. Clin. Microbiol. Rev., 6, 137-149.
73. Makui,H., Roig,E., Cole,S.T., Helmann,J.D., Gros,P. and Cellier,M.F. (2000) Identification of the Escherichia coli K-12 Nramp, orthologue (MntH) as a selective divalent metal ion transporter. Mol. Microbiol., 35, 1065-1078.
74. Patzer,S.I. and Hantke,K. (2001) Dual repression by Fe(2+)-Fur and Mn(2 +)-MntR of the mntH gene, encoding an NRAMP-like Mn(2+) transporter in Escherichia coli. J. Bacteriol., 183, 4806-4813.
75. Furrer,J.L., Sanders,D.N., Hook-Barnard,I.G. and McIntosh,M.A. (2002) Export of the siderophore enterobactin in Escherichia coli: involvement of a 43 kDa membrane exporter. Mol. Microbiol., 44 1225-1234.
76. Cunningham,L., Gruer,M.J. and Guest,J.R. (1997) Transcriptional regulation of the aconitase genes (acnA and acnB) of Escherichia coli. Microbiology, 143 (Pt 12), 3795-3805.
77. Fuentes,A.M., Diaz-Mejia,J.J., Maldonado-Rodriguez,R. and Amabile-Cuevas,C.F. (2001) Differential activities of the SoxR protein of Escherichia coli: SoxS is not required for gene activation under iron deprivation. FEMS Microbiol. Lett., 201 271-275.
78. Varghese,S., Tang,Y. and Imlay,J.A. (2003) Contrasting sensitivities of Escherichia coli aconitases A and B to oxidation and iron depletion. J. Bacteriol., 185, 221-230.
79. Zavitz,K.H., DiGate,R.J. and Marians,K.J. (1991) The PriB and PriC replication proteins of Escherichia coli. Genes, DNA sequence, overexpression, and purification. J. Biol. Chem., 266, 13988-13995.
80. Sandler,S.J. (2005) Requirements for replication restart proteins during constitutive stable DNA replication in Escherichia coli K-12. Genetics, 169, 1799-1806.
81. Schneider,T.D. (2001) Strong minor groove base conservation in sequence logos implies DNA distortion or base flipping during replication and transcription initiation. Nucleic Acids Res., 29, 4881-4891. http://www.cemp.ncifcrf.gov/~toms/paper/baseflip/