Transcription profile of Escherichia coli: Genomic SELEX search for regulatory targets of transcription factors

Nucleic Acids Research

Volumn 44, Issue 5, 2016, Pages 2058-2074

  Ishihama, Akira ^a   Shimada, Tomohiro ^b   Yamazaki, Yukiko ^c  

^a HOSEI UNIVERSITY   (Japan)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANOXIC REDOX CONTROL; BACTERIAL PROTEIN; BETAINE INHIBITOR; CYCLIC AMP BINDING PROTEIN; FERRIC UPTAKE REGULATOR; FUMARATE AND NITRATE REDUCTION; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; LEUCINE REGULATOR PROTEIN; LEUCINE RESPONSIVE REGULATORY PROTEIN; LIGAND; MULTI TARGET TRANSCRIPTION FACTOR; N ACETYLNEURAMINIC ACID; N ACETYLNEURAMINIC ACID ACID REGULATOR; NITRATE NITRITE RESPONSE REGULATOR; NUCLEOID TRANSCRIPTION FACTOR; REGULATOR PROTEIN; SIGMA FACTOR; SINGLE TARGET TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; UTILIZATION OF L ASCORBATE OPERON REGULATOR; BACTERIAL DNA; DNA DIRECTED RNA POLYMERASE; ESCHERICHIA COLI PROTEIN; LEUO PROTEIN, E COLI; LRP PROTEIN, E COLI; PROTEIN BINDING;

ARTICLE; BACTERIAL GENOME; BINDING SITE; CONSENSUS SEQUENCE; CONTROLLED STUDY; DATA BASE; DNA SEQUENCE; ESCHERICHIA COLI; GENE REGULATORY NETWORK; GENE SILENCING; GENE TARGETING; GENETIC DATABASE; GENETIC SCREENING; MULTI FACTOR OPERON; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN BINDING; SELEX DATABASE; TRANSCRIPTION REGULATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROMOTER REGION; SYSTEMATIC EVOLUTION OF LIGANDS BY EXPONENTIAL ENRICHMENT APTAMER TECHNIQUE;

BINDING SITES; CYCLIC AMP RECEPTOR PROTEIN; DNA, BACTERIAL; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; LEUCINE-RESPONSIVE REGULATORY PROTEIN; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SELEX APTAMER TECHNIQUE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84963800566     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw051     Document Type: Article

References (94)

1. Ishihama, A. (2010) Prokaryotic genome regulation: multi-factor promoters, multi-target regulators and hierarchic networks. FEMS Microbiol. Rev., 34, 628-645.
2. Ishihama, A. (2012) Prokaryotic genome regulation: a revolutionary paradigm. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci., 88, 485-508.
3. Helmann, J. and Chamberlin, M. (1988) Structure and function of bacterial sigma factors. Annu. Rev. Biochem., 57, 839-872.
4. Gross, C.A., Lonetto, M. and Losick, R. (1992) Bacterial sigma factors. In: McKnight, SL and Yamamoto, KR (eds). Transcriptional Regulation, Cold Spring Harbour Press, NY, pp. 129-176.
5. Ishihama, A. (2000) Functional modulation of Escherichia coli RNA polymerase. Annu. Rev. Microbiol., 54, 499-518.
6. Gruber, T.M. and Gross, C.A. (2003) Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol., 57, 441-466.
7. Paget, M.S. and Helmann, J.D. (2003) The sigma 70 family of sigma factors. Genome Biol., 4, 203.
8. Gourse, R.L., Ross, W. and Rutherford, S.T. (2006) General pathway for turning on promoters transcribed by RNA polymerase containing alternative sigma factors. J. Bacteriol., 188, 4589-4591.
9. Shimada, T., Yamazaki, Y., Tanaka, K. and Ishihama, A. (2014) The whole set of constitutive promoters recognized by RNA polymerase RpoD holoenzyme in Escherichia coli. PLoS One, 9, e90447.
10. Perez-Rueda, E. and Collado-Vides, J. (2000) The repertoire of DNA-binding transcription regulators in Escherichia coli K-12. Nucleic Acids Res., 28, 1838-1847.
11. Babu, M.M. and Teichmann, S.A. (2003) Evolution of transcription factors and the gene regulatory network in Escherichia coli. Nucleic Acids Res., 31, 1234-1244.
12. Ishihama, A. (2009) The nucleoid: an overview. In: Böck, A, Curtiss, R III, Kaper, JB, Karp, PD, Neidhardt, FC, Nystrom, T, Slauch, JM, Squires, CL and Ussery, D (eds). EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology. ASM Press, Washington.
13. Ishihama, A. (1992) Role of the RNA polymerase alpha subunit in tanscription activation. Mol. Microbiol., 6, 3283-3288.
14. Ishihama, A. (1993) Protein-protein communication within the transcription apparatus. J. Bacteriol., 175, 2483-2489.
15. Busby, S. and Ebright, R.H. (1999) Transcription activation by catabolite activator protein (CAP). J. Mol. Biol., 293, 199-213.
16. Shimada, T., Fujita, N., Maeda, M. and Ishihama, A. (2005) Systematic search for the Cra-binding promoters using genomic SELEX systems. Genes Cells, 10, 907-918.
17. Ellington, A.D. and Szostak, J.W. (1990) In vitro selection of RNA molecules that bind specific ligands. Nature, 346, 818-822.
18. Tuerk, C. and Gold, L. (1990) Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science, 249, 505-510.
19. Gold, L., Brown, D., He, Y., Shtatland, T., Singer, B.S. and Wu, Y. (1997) From oligonucleotides shapes to genomic SELEX: novel biological regulatory loops. Proc. Natl. Acad. Sci. U.S.A., 94, 59-64.
20. Singer, B.S., Shtatland, T., Brown, D. and Gold, L. (1997) Libraries for genomic SELEX. Nucleic Acids Res., 25, 781-786.
21. Teramoto, J., Yoshimura, S. H., Takeyasu, K. and Ishihama, A. (2010) A novel nucleoid protein of Escherichia coli induced under anaerobiotic growth conditions. Nucleic Acids Res., 38, 3605-3618.
22. Umezawa, Y., Ogasawara, H., Shimada, T., Kori, A. and Ishihama, A. (2008) The uncharacterized YdhM is the regulator of the nemA gene, coding N-ethylmaleimide reductase. J. Bacteriol., 190, 5890-5897.
23. Ogasawara, H., Ohe, S. and Ishihama, A. (2015) Role of transcription factor NimR (YeaM) in sensitivity control of Escherichia coli to 2-nitroimidazole. FEMS Microbiol. Lett., 362, 1-8.
24. Shimada, T., Yamazaki, K. and Ishihama, A. (2013) Novel regulator PgrR for switch control of peptidoglycan recycling in Escherichia coli. Genes Cells, 18, 123-134.
25. Shimada, T., Katayama, Y., Kawakita, S., Ogasawara, H., Nakano, M., Yamamoto, K. and Ishihama, A. (2012) A novel regulator RcdA of the csgD gene encoding the master regulator of biofilm formation in Escherichia coli. Microbiologyopen, 1, 381-394.
26. Shimada, T., Hirao, K., Kori, A., Yamamoto, K. and Ishihama, A. (2007) RutR is the uracil/thymine-sensing master regulator of a set of genes for synthesis and degradation of pyrimdines. Mol. Microbiol., 66, 744-757.
27. Shimada, T., Ishihama, A., Busby, S.J. and Grainger, D.C. (2008) The Escherichia coli RutR transcription factor binds at targets within genes as well as intergenic regions. Nucleic Acids Res., 36, 3950-3955.
28. Yamamoto, K., Nakano, M. and Ishihama, A. (2015) Regulatory role of transcription factor SutR (YdcN) in sulfur utilization in Escherichia coli. Microbiology, 161, 99-111.
29. Keseler, I.M., Collado-Vides, J., Gama-Castro, S., Ingraham, S., Paley, S., Paulsen, I.T., Peralta-Gil, M. and Karp, P.D. (2005) EcoCyc: a compehensive database resource for Escherichia coli. Nucleic Acids Res., 44, D334-D337.
30. Karp, P.D., Weaver, D., Paley, S., Fulcher, C., Kubo, A., Kothari, A., Krummenacker, M., Subharaveti, P., Weerasinghe, D., Cama-Castro, S. et al. (2014) The EcoCyc database. Ecosal Plus, doi:10.1128/ecosalplus.ESP-0009-2103.
31. Salgado, H., Gama-Castro, S., Martinez-Flores, I., Diaz-Peredo, E., Sanchez-Solano, F., Peralta-Gil, M., Garcita-Alonso, D., Jimenez-Jacinto, V., Santos- Zavaleta, A., Bonavides-Martinez, C. et al. (2006) RegulonDB (version 4.0): transcriptional regulation, operon organization and growth conditions. Nucleic Acids Res., 32, D303-D306.
32. Salgado, H., Peralta-Gil, M., Gama-Castro, S., Santos-Zavaleta, A., Muniz-Raccado, L., Garcia-Sotelo, J.S., Weiss, V., Solano-Lira, H., Martinez-Flores, I., Medina-Revira, A. et al. (2013) RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards an dmore. Nucleic Acids Res., 41, D203-D213.
33. Jishage, M. and Ishihama, A. (1997) Variation in RNA polymerase sigma subunit composition within different stocks of Escherichia coli W3110. J. Bacteriol., 179, 959-963.
34. Bleibtreu, A., Clermont, O., Darlu, P., Glodt, J., Branger, C., Picard, B. and Denamur, E. (2014) The rpoS gene is predominantly inactivated during laboratory storage and undergoes source-sink evolution in Escherichia coli species. J. Bacteriol., 196, 4276-4284.
35. Cook, H. and Ussery, D.W. (2013) Sigma factors in a thousand E. coli genomes. Environ. Microbiol., 15, 3121-3129.
36. Conway, T., Creecy, J.P., Maddox, S.M., Grissom, J.E., Conkle, T.L., Shadid, T.M., Teramoto, J., Miguet, P.S., Shimada, T., Ishihama, A. et al. (2014) Unprecedented high-resolution view of bacterial operon architecture revealed by RNA sequencing. MBio, 5, doi:10.1128/mBio.01442-14.
37. Shimada, T., Takada, H., Yamamoto, K. and Ishihama, A. (2015) Expanded roles of the two-component response regulator OmpR in Escherichia coli: Genomic SELEX search for novel regulation targets. Genes Cells, 20, 915-931.
38. Mizuno, T. (1997) Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res., 4, 161-168.
39. Yamamoto, K., Hirao, K., Oshima, T., Aiba, H., Utsumi, R. and Ishihama, A. (2005) Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem., 280, 1448-1456.
40. Laishram, R.S. and Gowrishankar, J. (2007) Envirornmental regulation operating at the promoter clearance step of bacterial transcription. Genes Dev., 21, 1258-1272.
41. Shimada, T., Shimada, K., Matsui, M., Kitai, Y., Igarashi, J., Suga, H. and Ishihama, A. (2014) Roles of cell division control factor SdiA: recognition of quorum sensing signals and modulation of transcription regulation targets. Genes Cells, 19, 405-418.
42. Nieto, J.M., Madrid, C., Miquelay, E., Parra, J.L., Rodriguez, S. and Juaraz, A. (2002) Evidence for direct protein-protein interaction between members of the enterobacterial Hha/YmoA and H-NS families of proteins. J. Bacteriol., 184, 629-635.
43. Reznikoff, W.S. (1992) The lactose operon controlling elements: a complex paradigm. Mol. Microbiol., 6, 2419-2422.
44. Martinez-Antonio, A. and Collado-Vides, J. (2003) Identifying global regulators in transcriptional regulatory networks in bacteria. Curr. Opin. Microbiol., 6, 482-489.
45. Wei, G.H., Liu, D.P. and Lian, C.C. (2004) Charting gene regulatory networks: strategies, challenges and perspectives. Biochem. J., 381, 1-12.
46. Gottesman, S. (1984) Bacterial regulation: global regulatory nework. Ann. Rev. Genet., 18, 415-441.
47. Gutierrez-Rois, R.M., Rosenblueth, D.A., Loza, J.A., Huerta, A.M., Glasner, J.D., Blattner, F.R. and Collado-Vides, J. (2003) Regulatory network of Escherichia coli: consistency between literature and knowledge and microarray profiles. Genome Res., 13, 2435-2443.
48. Balderas-Martinez, Y.I., Savageau, M., Saldago, H., Perez-Rueda, E., Morett, E. and Collado-Vides, J. (2013) Transcription factors in Escherichia coli prefer the holo conformation. PLoS One, 8, e65723.
49. Lamark, T., Rokenes, T.P., McDougall, J. and Strom, A.R. (1996) The complex bet promoters of Escherichia coli: regulation by oxygen (ArcA), choline (BetI), and osmotic stress. J. Bacteriol., 178, 1655-1662.
50. Rkenes, T.P., Lamark, T. and Strom, A.R. (1996) DNA-binding properties of the BetI repressor protein of Escherichia coli: the inducer choline stimulates BetI-DNA complex formation. J. Bacterol., 178, 1663-1670.
51. Kalivoda, K.A., Steenbergen, S.M., Vimr, E.R. and Plumbridge, J. (2003) Regulation of sialic acid catabolism by the DNA binding protein NanR in Escherichia coli. J. Bacteriol., 185, 4806-4815.
52. Sohanpal, B.K., El-Labany, S., Lahooti, M., Plumbridge, J.A. and Blomfield, I.C. (2004) Integrated regulatory responses of fimB to N-acetylneuraminic (sialic) acid and GlcNAc in Escherichia coli K-12. Proc. Natl. Acad. Sci. U.S.A., 101, 16322-16327.
53. Campos, E., Baldoma, L., Aguilar, J. and Badia, J. (2004) Regulation of expression of the divergent ulaG and ulaABCDEF operons involved in L-ascorbate dissimilation in Escherichia coli. J. Bacteriol., 186, 1720-1728.
54. Kolb, A., Busby, S., Buc, H., Garges, S. and Adhya, S. (1993) Transcriptional regulation by cAMP and its receptor protein. Annu. Rev. Biochem., 62, 749-795.
55. Harman, J.G. (2001) Allosteric regulation of the cAMP receptor protein. Biochim. Biophys. Acta, 1547, 1-17.
56. Krueger, S., Gregurick, S., Shi, Y., Wang, S., Wladkowski, B.D. and Schwarz, F.P. (2003) Entropic nature of the interaction between promoter and bound CRP mutants and RNA polymerase. Biochemistry, 42, 1958-1968.
57. Shimada, T., Fujita, N., Yamamoto, K. and Ishihama, A. (2011) Novel roles of cAMP receptor protein (CRP) in regulation of transport and metabolism of carbon sources. PLoS One, 6, e20081.
58. Shimada, T., Yamamoto, K. and Ishihama, A. (2011) Novel members of the Cra regulon involved in carbon metabolism in Escherichia coli. J. Bacteriol., 193, 649-659.
59. Hertzberg, K.M., Gemmill, R., Jones, J. and Calvo, J.M. (1980) Cloning of an EcoR1-generated fragment of the leucine operon of Salmonella typhimurium. Gene, 8, 135-152.
60. Shimada, T., Bridier, A., Briandet, R. and Ishihama, A. (2011) Novel roles of LeuO in transcription regulation in E. coli: Antagonistic interplay with the universal silencer H-NS. Mol. Microbiol., 82, 378-397.
61. Ernsting, B.R., Atkinson, M.R., Ninfa, A.J. and Matthews, R.G. (1992) Characterization of the regulon controlled by the leucine-responsive regulatory prootein in Escherichia coli. J. Bacteriol., 174, 1109-1118.
62. Calvo, J.M. and Matthews, R.G. (1994) The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol. Rev., 58, 466-490.
63. Shimada, T., Saito, N., Maeda, M., Tanaka, K. and Ishihama, A. (2015) Expanded roles of Lrp in transcription regulation of the Eschericia coli genome: Genomic SELEX screening of the regulation targets. Microbial. Genomics, doi:10.1099/mgen.0.000001.
64. Ishihama, A. (1999) Modulation of the nucleoid, the transcription apparatus, and the translation machinery in bacteria for stationary phase survival. Genes Cells, 4, 135-143.
65. Dorman, C.J. (2004) H-NS: a universal regulator for a dynamic genome. Nat. Rev. Microbiol., 2, 391-400.
66. Macvanin, M. and Adhya, S. (2012) Architectural organization in E. coli nucleoid. Biochim. Biophys. Acta, 1819, 830-835.
67. Azam, T.A., Iwata, A., Nishimura, A., Ueda, S. and Ishihama, A. (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J. Bacteriol., 181, 6361-6370.
68. Ishihama, A., Kori, A., Koshio, E., Yamada, K., Maeda, H., Shimada, T., Makinoshima, H., Iwata, A. and Fujita, N. (2014) Intracellular concentrations of 65 species of transcription factors with known regulatory functions in Escherichia coli. J. Bacteriol., 196, 2718-2727.
69. Freundlich, M., Ramani, N., Mathew, E., Sirko, A. and Tsui, P. (1992) The role of integration host factor in gene expression in Escherichia coli. Mol. Microbiol., 6, 2557-2563.
70. Swinger, K.K. and Rice, P.A. (2007) Structure based analysis of HU-DNA binding. J. Mol. Biol., 365, 1005-1016.
71. Tending, C. and Bertin, P.N. (2003) H-NS in Gram-negative bacteria: a family of mutitfaceted proteins. Trends Microbiol., 11, 511-518.
72. Atlung, T. and Ingmer, H. (1997) H-NS: a modulator of environmentally regulated gene expression. Mol. Microbiol., 24, 7-17.
73. Hengge-Aronis, R. (1999) Interplay of global regulators and cell physiology in the general stress response of Escherichia coli. Curr. Opin. Microbiol., 2, 148-152.
74. Oshima, T. and Biville, F. (2006) Functional identification of ygiP as a positive regulator of the ttdA-ttdB-ygjE operon. Microbiology, 152, 2129-2135.
75. Bradley, M.D., Beach, M.B., de Koning, P.J., Pratt, T.S. and Osuna, R. (2007) Effects of Fis on Escherichia coli gene expression during different growth stages. Microbiology, 153, 2922-2940.
76. Ogasawara, H., Yamada, K., Kori, A., Yamamoto, K. and Ishihama, A. (2010) The E. coli csgD promoter: interplay between eight transcription factors. Microbiology, 156, 2470-2483.
77. Ogasawara, H., Yamamoto, K. and Ishihama, A. (2010) Regulatory role of MlrA in transcription activation of csgD, the master regulator of biofilm formation in Escherichia coli. FEMS Microbiol. Lett., 312, 160-168.
78. Dudlin, O., Gelselmann, J., Ogasawara, H., Ishihama, A. and Lacour, S. (2013). Repression of flagella genes in exponential phase by CsgD and CpxR, two crucial modulators of Escherichia coli biofilm formation. J. Bacteriol., 196, 707-715.
79. Ma, Z., Zong, S., Richard, H., Tucker, D.L., Conway, T. and Foster, J.W. (2003) GadE activates glutamate decarboxylase-dependent acid resistance in Escherichia coli. Mol. Microbiol., 49, 130-1320.
80. Seo, S.W., Kim, D., O'Brien, E.J., Szubin, R. and Palsson, B.O. (2015) Decoding genome-wide GadEWX-transcriptional regulatory networks reveals multifaceted cellular responses to acid stress in Escherichia coli. Nat. Commun., 6, 7970.
81. Soutourina, O.A. and Bertin, P.N. (2003) Regulation of flagella expression in Gram-negative bacteria. FEMS Microbiol. Rev., 27, 505-523.
82. Park, S.J., Chao, G. and Gunsalus, R.P. (1997) Aerobic regulation of the sucABCD genes of Escherichia coli, which encode alpha-ketogkutarate dehydrogenase and succinyl coenzyme A synthetase: roles of ArcA, Fnr, and the upstream sdhCDAB promoter. J. Bacteriol., 179, 4138-4142.
83. Bongaerts, J., Zoske, S., Weldner, U. and Unden, G. (1995) Transcriptional regulation of the proton translocating NADH dehydrogenase genes (nuoA-N) of Escherichia coli by electron acceptors, electron donors and gene regulators. Mol. Microbiol., 16, 521-534.
84. Stoebel, D.M., Free, A. and Dorman, C.J. (2008) Anti-silencing: overcoming H-NS-mediated repression of transcription in Gram-negative enteric bacteria. Microbiology, 154, 2533-2545.
85. Lucchini, S., Rowley, G., Goldberg, M.D., Hurd, D., Harrison, M. and Hinton, J.C. (2006) H-NS mediates the silencing of laterally acquired genes in bacteria. PLoS Pathog., 2, e81.
86. Erill, I. (2015) Every site counts: submitting transcription factor-biding site information through the CollectTF portal. J. Bacteriol., 197, 2454-2457.
87. Richmond, C.S., Glasner, J.D., Mau, R. and Blattner, F.R. (1999) Genome-wide expression profiling in Escherichia coli K-12. Nucleic Acids Res., 27, 3821-3835.
88. Tao, H., Bausch, C., Richmond, C., Blattner, F.R. and Conway, T. (1999) Functional genomics: expression analysis of Escherichia coli growing on minimal and rich media. J. Bacteriol., 181, 6425-6440.
89. Bulyk, M.L. (2006) DNA microarray technologies for measuring protein-DNA interactions. Curr. Opin. Biotechnol., 17, 422-430.
90. Wade, J.T., Struhl, K., Busby, S.J.W. and Grainger, D.C. (2007) Genomic analysis of protein-DNA interactions in bacteria: insights into transcription and chromosome organization. Mol. Microbiol., 65, 21-26.
91. Ishida, Y., Kori, A. and Ishihama, A. (2009) Participation of regulator AscG of theβ-glucoside utilization operon in regulation of the propionate catabolism operon. J. Bacteriol., 191, 6136-6144.
92. Ogasawara, H., Shinohara, S. and Ishihama, A. (2012) Regulation targets of metal-response BasS-BasR two-component system in Escherichia coli: Modification of cell membrane. Microbiology, 158, 1482-1492.
93. Yamamoto, K., Matsumoto, F., Minagawa, S., Oshima, T., Fujita, N., Ogasawara, N. and Ishihama, A. (2009) Characterization of CitA-CitB signal transduction activating genes involved in anaerobic citrate catabolism in Escherichia coli. Biosci. Biotechnonl. Biochem., 73, 346-350.
94. Shimada, T., Kori, A. and Ishihama, A. (2013) Involvement of the ribose operon repressor RbsR in regulation of purine nucleotide synthesis in Escherichia coli. FEMS Microbiol. Lett., 344, 159-165.