The hierarchic network of metal-response transcription factors in Escherichia coli

Bioscience, Biotechnology and Biochemistry

Volumn 78, Issue 5, 2014, Pages 737-747

  Yamamoto, Kaneyoshi ^a  

^a HOSEI UNIVERSITY   (Japan)

Author keywords

Escherichia coli; Hierarchic regulatory network; Metal sensing transcription factor regulon; Rna polymerase; Transcriptional regulation

Indexed keywords

ANIMALS; COMPLEX NETWORKS; ESCHERICHIA COLI; GENE EXPRESSION; GENES; METALS; PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

COMPREHENSIVE ANALYSIS; EXPRESSION PATTERNS; METAL SENSING; PROMOTER RECOGNITION; REGULATORY NETWORK; RNA POLYMERASE; SIGNAL TRANSDUCTION PATHWAYS; TRANSCRIPTIONAL REGULATION;

TRANSCRIPTION;

ANIMALIA; ENTEROBACTERIACEAE; ESCHERICHIA COLI;

BACTERIAL DNA; METAL; TRANSCRIPTION FACTOR;

ESCHERICHIA COLI; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

DNA, BACTERIAL; ESCHERICHIA COLI; GENE REGULATORY NETWORKS; METALS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84906888370     PISSN: 09168451     EISSN: 13476947     Source Type: Journal    
DOI: 10.1080/09168451.2014.915731     Document Type: Review

References (116)

1. Ishihama A. Protein-protein communication within the transcription apparatus. J. Bacteriol. 1993;175:2483-2489.
2. Busby S, Ebright RH. Promoter structure, promoter recognition, and transcription activation in prokaryotes. Cell. 1994;79:743-746.
3. Ishihama A. Functional modulation of Escherichia coli RNA polymerase. Annu. Rev. Microbiol. 2000;54:499-518.
4. Brennan RG, Matthews BW. The helix-turn-helix DNA binding motif. J. Biol. Chem. 1989;264:1903-1906.
5. Aravind L, Anantharaman V, Balaji S, Babu MM, Iyer LM. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol. Rev. 2005;29:231-262.
6. Ishihama A. Prokaryotic genome regulation: multifactor promoters, multitarget regulators and hierarchic networks. FEMS Microbiol. Rev. 2010;34:628-645.
7. Ishihama A. Prokaryotic genome regulation: a revolutionary paradigm. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 2012; 88:485-508.
8. Aiba H, Kawamukai M, Ishihama A. Cloning and promoter analysis of the Escherichia coli adenylate cyclase gene. Nucleic Acids Res. 1983;11:3451-3465.
9. Ishizuka H, Hanamura A, Inada T, Aiba H. Mechanism of the down-regulation of cAMP receptor protein by glucose in Escherichia coli: role of autoregulation of the crp gene. EMBO J. 1994;13:3077-3082.
10. Choy HE, Park SW, Aki T, Parrack P, Fujita N, Ishihama A, Adhya S. Repression and activation of transcription by Gal and Lac repressors: involvement of alpha subunit of RNA polymerase. EMBO J. 1995;14:4523-4529.
11. Ishihama A. Promoter selectivity control of RNA polymerase. In: Eckstein F, Lilley D, editors. Nucleic acids and molecular biology. Vol. 11, Mechanism of Transcription. Heidelberg: Springer-Verlag; 1997. p. 53-70.
12. Igarashi K, Ishihama A. Bipartite functional map of the E. coli RNA polymerase alpha subunit: involvement of the C-terminal region in transcription activation by cAMP-CRP. Cell. 1991;65:1015-1022.
13. Igarashi K, Hanamura A, Makino K, Aiba H, Aiba H, Mizuno T, Nakata A, Ishihama A. Functional map of the alpha subunit of Escherichia coli RNA polymerase: two modes of transcription activation by positive factors. Proc. Natl. Acad. Sci. USA. 1991;88:8958-8962.
14. Weickert MJ, Adhya S. The galactose regulon of Escherichia coli. Mol. Microbiol. 1993;10:245-251.
15. Yamamoto K, Yata K, Fujita N, Ishihama A. Novel mode of transcription regulation by SdiA, an Escherichia coli homologue of the quorum-sensing regulator. Mol. Microbiol. 2001;41:1187-1198.
16. Yamamoto K, Ogasawara H, Fujita N, Utsumi R, Ishihama A. Novel mode of transcription regulation of divergently overlapping promoters by PhoP, the regulator of two-component system sensing external magnesium availability. Mol. Microbiol. 2002;45:423-438.
17. Müller-Hill B. Some repressors of bacterial transcription. Curr. Opin. Microbiol. 1998;1:145-151.
18. Yamamoto K, Ishihama A. Two different modes of transcription repression of the Escherichia coli acetate operon by IclR. Mol. Microbiol. 2003;47:183-194.
19. Hoch JA. Two-component and phosphorelay signal transduction. Curr. Opin. Microbiol. 2000;3:165-170.
20. Stock AM, Robinson VL, Goudreau PN. Two-component signal transduction. Annu. Rev. Biochem. 2000;69:183-215.
21. Igo MM, Slauch JM, Silhavy TJ. Signal transduction in bacteria: kinases that control gene expression. New Biol. 1990;2:5-9.
22. Mizuno T, Mizushima S. Signal transduction and gene regulation through the phosphorylation of two regulatory components: the molecular basis for the osmotic regulation of the porin genes. Mol. Microbiol. 1990;4:1077-1082.
23. Parkinson JS, Kofoid EC. Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 1992;26:71-112.
24. Egger LA, Park H, Inouye M. Signal transduction via the histidyl-aspartyl phosphorelay. Genes Cells. 1997;2:167-184.
25. Mizuno T. Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res. 1997;4:161-168.
26. Yamamoto K, Hirao K, Oshima T, Aiba H, Utsumi R, Ishihama A. Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem. 2005;280:1448-1456.
27. DeRisi JL, Iyer VR, Brown PO. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science. 1997;278:680-686.
28. de Saizieu A, Certa U, Warrington J, Gray C, Keck W, Mous J. Bacterial transcript imaging by hybridization of total RNA to oligonucleotide arrays. Nat. Biotechnol. 1998;16:45-48.
29. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science. 2008;320:1344-1349.
30. Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, Goodhead I, Penkett CJ, Rogers J, Bahler J. Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature. 2008;453:1239-1243.
31. Passalacqua KD, Varadarajan A, Ondov BD, Okou DT, Zwick ME, Bergman NH. Structure and complexity of a bacterial transcriptome. J. Bacteriol. 2009;191:3203-3211.
32. Richmond CS, Glasner JD, Mau R, Jin H, Blattner FR. Genome-wide expression profiling in Escherichia coli K-12. Nucleic Acids Res. 1999;27:3821-3835.
33. Arnold CN, McElhanon J, Lee A, Leonhart R, Siegele DA. Global analysis of Escherichia coli gene expression during the acetate-induced acid tolerance response. J. Bacteriol. 2001;183:2178-2186.
34. Salmon K, Hung SP, Mekjian K, Baldi P, Hatfield GW, Gunsalus RP. Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. J. Biol. Chem. 2003;278:29837-29855.
35. Tuerk C, Gold L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science. 1990;249:505-510.
36. Shimada T, Fujita N, Maeda M, Ishihama A. Systematic search for the Cra-binding promoters using genomic SELEX system. Genes Cells. 2005;10:907-918.
37. Ren B, Robert F, Wyrick JJ, Aparicio O, Jennings EG, Simon I, Zeitlinger J, Schreiber J, Hannett N, Kanin E, Volkert TL, Wilson CJ, Bell SP, Young RA. Genome-wide location and function of DNA binding proteins. Science. 2000;290:2306-2309.
38. Katou Y, Kaneshiro K, Aburatani H, Shirahige K. Genomic approach for the understanding of dynamic aspect of chromosome behavior. Methods Enzymol. 2006;409:389-410.
39. Wackett LP, Dodge AG, Ellis LB. Microbial genomics and the periodic table. Appl. Environ. Microbiol. 2004;70:647-655.
40. Nies DH. Microbial heavy-metal resistance. Appl. Microbiol. Biotechnol. 1999;51:730-750.
41. Nies DH. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 2003;27:313-339.
42. Hobman JL, Yamamoto K, Oshima T. Transcriptomic responses of bacterial cells to sublethal metal ion stress. In: Nies DH, Simon S, editors. Microbiology monographs. Vol. 6, Molecular microbiology of heavy metals. Berlin: Springer-Verlag; 2007. p. 77-116.
43. Rahav-Manor O, Carmel O, Karpel R, Taglicht D, Glaser G, Schuldiner S, Padan E. NhaR, a protein homologous to a family of bacterial regulatory proteins (LysR), regulates nhaA, the sodium proton antiporter gene in Escherichia coli. J. Biol. Chem. 1992;267:10433-10438.
44. + antiporter gene in Escherichia coli. EMBO J. 1994;13:1981-1989.
45. Toesca I, Perard C, Bouvier J, Gutierrez C, Conter A. The transcriptional activator NhaR is responsible for the osmotic induction of osmC(p1), a promoter of the stress-inducible gene osmC in Escherichia coli. Microbiology. 2001;147:2795-2803.
46. Goller C, Wang X, Itoh Y, Romeo T. The cation-responsive protein NhaR of Escherichia coli activates pgaABCD transcription, required for production of the biofilm adhesin poly-beta-1, 6-N-acetyl-D-glucosamine. J. Bacteriol. 2006;188:8022-8032.
47. + and ionic strength directly influence the autophosphorylation activity of the putative turgor sensor KdpD of Escherichia coli. J. Biol. Chem. 2000;275:40142-40147.
48. Sugiura A, Nakashima K, Tanaka K, Mizuno T. Clarification of the structural and functional features of the osmoregulated kdp operon of Escherichia coli. Mol. Microbiol. 1992;6:1769-1776.
49. Walderhaug MO, Polarek JW, Voelkner P, Daniel JM, Hesse JE, Altendorf K, Epstein W. KdpD and KdpE proteins that control expression of the kdpABC operon, are members of the two-component sensor-effector class of regulators. J. Bacteriol. 1992;174:2152-2159.
50. Nakashima K, Sugiura A, Momoi H, Mizuno T. Phosphotransfer signal transduction between two regulatory factors involved in the osmoregulated kdp operon in Escherichia coli. Mol. Microbiol. 1992;6:1777-1784.
51. Nakashima K, Sugiura A, Kanamaru K, Mizuno T. Signal transduction between the two regulatory components involved in the regulation of the kdpABC operon in Escherichia coli: phosphorylation-dependent functioning of the positive regulator, KdpE. Mol. Microbiol. 1993;7:109-116.
52. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell. 1996;84:165-174.
53. 2+-responsive promoters. J. Bacteriol. 1999;181:5516-5520.
54. 2+ stimulon of Escherichia coli. J. Bacteriol. 2003;185:3696-3702.
55. Patzer SI, Hantke K. The zinc-responsive regulator Zur and its control of the znu gene cluster encoding the ZnuABC zinc uptake system in Escherichia coli. J. Biol. Chem. 2000;275:24321-24332.
56. Waters LS, Sandoval M, Storz G. The Escherichia coli MntR miniregulon includes genes encoding a small protein and an efflux pump required for manganese homeostasis. J. Bacteriol. 2011;193:5887-5897.
57. Yamamoto K, Ishihama A, Busby SJ, Grainger DC. The Escherichia coli K-12 MntR miniregulon includes dps, which encodes the major stationary-phase DNA-binding protein. J. Bacteriol. 2011;193:1477-1480.
58. Chivers PT, Sauer RT. NikR is a ribbon-helix-helix DNA-binding protein. Protein Sci. 1999;8:2494-2500.
59. Schreiter ER, Sintchak MD, Guo Y, Chivers PT, Sauer RT, Drennan CL. Crystal structure of the nickel-responsive transcription factor NikR. Nat. Struct. Biol. 2003;10:794-799.
60. Schreiter ER, Wang SC, Zamble DB, Drennan CL. NikR-operator complex structure and the mechanism of repressor activation by metal ions. Proc. Natl. Acad. Sci. USA. 2006;103:13676-13681.
61. Phillips CM, Schreiter ER, Guo Y, Wang SC, Zamble DB, Drennan CL. Structural basis of the metal specificity for nickel regulatory protein NikR. Biochemistry. 2008;47:1938-1946.
62. 2+-Dependent interaction of NikR with wild-type and mutant operator sites. J. Biol. Chem. 2000;275:19735-19741.
63. Yamamoto K, Ishihama A. Transcriptional response of Escherichia coli to external zinc. J. Bacteriol. 2005;187:6333-6340.
64. Beard SJ, Hashim R, Membrillo-Hernandez J, Hughes MN, Poole RK. Zinc(II) tolerance in Escherichia coli K-12: evidence that the zntA gene (o732) encodes a cation transport ATPase. Mol. Microbiol. 1997;25:883-891.
65. Rensing C, Mitra B, Rosen BP. The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc. Natl. Acad. Sci. USA. 1997;94:14326-14331.
66. Grass G, Fan B, Rosen BP, Franke S, Nies DH, Rensing C. ZitB (YbgR), a member of the cation diffusion facilitator family, is an additional zinc transporter in Escherichia coli. J. Bacteriol. 2001;183:4664-4667.
67. Patzer SI, Hantke K. The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol. Microbiol. 1998;28:1199-1210.
68. Grass G, Wong MD, Rosen BP, Smith RL, Rensing C. ZupT is a Zn(II) uptake system in Escherichia coli. J. Bacteriol. 2002;184:864-866.
69. Brocklehurst KR, Hobman JL, Lawley B, Blank L, Marshall SJ, Brown NL, Morby AP. ZntR is a Zn(II)-responsive MerR-like transcriptional regulator of zntA in Escherichia coli. Mol. Microbiol. 1999;31:893-902.
70. Outten CE, Outten FW, O'Halloran TV. DNA distortion mechanism for transcriptional activation by ZntR, a Zn(II)-responsive MerR homologue in Escherichia coli. J. Biol. Chem. 1999;274:37517-37524.
71. Changela A, Chen K, Xue Y, Holschen J, Outten CE, O'Halloran TV, Mondragon A. Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science. 2003;301:1383-1387.
72. Outten CE, O'Halloran TV. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science. 2001;292:2488-2492.
73. Leonhartsberger S, Huber A, Lottspeich F, Bock A. The hydH/G genes from Escherichia coli code for a zinc and lead responsive two-component regulatory system. J. Mol. Biol. 2001;307:93-105.
74. Rensing C, Grass G. Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol. Rev. 2003;27:197-213.
75. Brown NL, Lee BTO, Silver S. Bacterial transport of and resistance to copper. In: Sigel H, Sigel A, editors. Metal ions in biological systems. New York (NY): Dekker; 1994. p. 405-434.
76. Outten FW, Outten CE, Hale J, O'Halloran TV. Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homologue, cueR. J. Biol. Chem. 2000;275:31024-31029.
77. Stoyanov JV, Hobman JL, Brown NL. CueR (YbbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Mol. Microbiol. 2001;39:502-511.
78. Yamamoto K, Ishihama A. Transcriptional response of Escherichia coli to external copper. Mol. Microbiol. 2005;56:215-227.
79. Munson GP, Lam DL, Outten FW, O'Halloran TV. Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. J. Bacteriol. 2000;182:5864-5871.
80. Franke S, Grass G, Rensing C, Nies DH. Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J. Bacteriol. 2003;185:3804-3812.
81. Braun V, Braun M. Iron transport and signaling in Escherichia coli. FEBS Lett. 2002;529:78-85.
82. Wandersman C, Delepelaire P. Haemophore functions revisited. Mol. Microbiol. 2012;85:618-631.
83. Braun V, Hantke K. Recent insights into iron import by bacteria. Curr. Opin. Chem. Biol. 2011;15:328-334.
84. Braun V, Mahren S, Ogierman M. Regulation of the FecI-type ECF sigma factor by transmembrane signalling. Curr. Opin. Microbiol. 2003;6:173-180.
85. Baichoo N, Helmann JD. Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J. Bacteriol. 2002;184:5826-5832.
86. Lee JW, Helmann JD. Functional specialization within the Fur family of metalloregulators. Biometals. 2007;20:485-499.
87. Nagasawa S, Ishige K, Mizuno T. Novel members of the two-component signal transduction genes in Escherichia coli. J. Biochem. 1993;114:350-357.
88. Hagiwara D, Yamashino T, Mizuno T. A genome-wide view of the Escherichia coli BasS-BasR two-component system implicated in iron-responses. Biosci. Biotechnol. Biochem. 2004;68:1758-1767.
89. Froelich JM, Tran K, Wall D. A pmrA constitutive mutant sensitizes Escherichia coli to deoxycholic acid. J. Bacteriol. 2006;188:1180-1183.
90. Herrera CM, Hankins JV, Trent MS. Activation of PmrA inhibits LpxT-dependent phosphorylation of lipid A promoting resistance to antimicrobial peptides. Mol. Microbiol. 2010;76:1444-1460.
91. Ogasawara H, Shinohara S, Yamamoto K, Ishihama A. Novel regulation targets of the metal-response BasS-BasR two-component system of Escherichia coli. Microbiology. 2012;158:1482-1492.
92. Grunden AM, Ray RM, Rosentel JK, Healy FG, Shanmugam KT. Repression of the Escherichia coli modABCD (molybdate transport) operon by ModE. J. Bacteriol. 1996;178:735-744.
93. Hall DR, Gourley DG, Leonard GA, Duke EM, Anderson LA, Boxer DH, Hunter WN. The high-resolution crystal structure of the molybdate-dependent transcriptional regulator (ModE) from Escherichia coli: a novel combination of domain folds. EMBO J. 1999;18:1435-1446.
94. Kurata T, Katayama A, Hiramatsu M, Kiguchi Y, Takeuchi M, Watanabe T, Ogasawara H, Ishihama A, Yamamoto K. Identification of the set of genes, including nonannotated morA, under the direct control of ModE in Escherichia coli. J. Bacteriol. 2013;195:4496-4505.
95. Binet MR, Poole RK. Cd(II), Pb(II) and Zn(II) ions regulate expression of the metal-transporting P-type ATPase ZntA in Escherichia coli. FEBS Lett. 2000;473:67-70.
96. Stoyanov JV, Brown NL. The Escherichia coli copper-responsive copA promoter is activated by gold. J. Biol. Chem. 2003;278:1407-1410.
97. Shimada K, Ogasawara H, Yamada K, Shimura M, Kori A, Shimada T, Yamanaka Y, Yamamoto K, Ishihama A. Screening of promoter-specific transcription factors: multiple regulators for the sdiA gene involved in cell division control and quorum sensing. Microbiology. 2013;159:2501-2512.
98. McNicholas PM, Rech SA, Gunsalus RP. Characterization of the ModE DNA-binding sites in the control regions of modABCD and moaABCDE of Escherichia coli. Mol. Microbiol. 1997;23:515-524.
99. McNicholas PM, Chiang RC, Gunsalus RP. Anaerobic regulation of the Escherichia coli dmsABC operon requires the molybdate-responsive regulator ModE. Mol. Microbiol. 1998;27:197-208.
100. McNicholas PM, Gunsalus RP. The molybdate-responsive Escherichia coli ModE transcriptional regulator coordinates periplasmic nitrate reductase (napFDAGHBC) operon expression with nitrate and molybdate availability. J. Bacteriol. 2002;184:3253-3259.
101. Xu M, Busby SJ, Browning DF. Activation and repression at the Escherichia coli ynfEFGHI operon promoter. J. Bacteriol. 2009;191:3172-3176.
102. Ogasawara H, Hasegawa A, Kanda E, Miki T, Yamamoto K, Ishihama A. Genomic SELEX search for target promoters under the control of the PhoQP-RstBA signal relay cascade. J. Bacteriol. 2007;189:4791-4799.
103. Guckes KR, Kostakioti M, Breland EJ, Gu AP, Shaffer CL, Martinez CR 3rd, Hultgren SJ, Hadjifrangiskou M. Strong cross-system interactions drive the activation of the QseB response regulator in the absence of its cognate sensor. Proc. Natl. Acad. Sci. USA. 2013;110:16592-16597.
104. Clarke MB, Hughes DT, Zhu C, Boedeker EC, Sperandio V. The QseC sensor kinase: a bacterial adrenergic receptor. Proc. Natl. Acad. Sci. USA. 2006;103:10420-10425.
105. Sperandio V, Torres AG, Kaper JB. Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol. Microbiol. 2002;43:809-821.
106. Zwir I, Shin D, Kato A, Nishino K, Latifi T, Solomon F, Hare JM, Huang H, Groisman EA. Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc. Natl. Acad. Sci. USA. 2005;102:2862-2867.
107. Eguchi Y, Itou J, Yamane M, Demizu R, Yamato F, Okada A, Mori H, Kato A, Utsumi R. B1500, a small membrane protein, connects the two-component systems EvgS/EvgA and PhoQ/PhoP in Escherichia coli. Proc. Natl. Acad. Sci. USA. 2007;104:18712-18717.
108. Yamanaka Y, Ishihama A, Yamamoto K. Induction of YdeO, a regulator for acid resistance genes, by ultraviolet irradiation in Escherichia coli. Biosci. Biotechnol. Biochem. 2012;76:1236-1238.
109. Oshima T, Aiba H, Masuda Y, Kanaya S, Sugiura M, Wanner BL, Mori H, Mizuno T. Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol. Microbiol. 2002;46:281-291.
110. Yamamoto K, Matsumoto F, Oshima T, Fujita N, Ogasawara N, Ishihama A. Anaerobic regulation of citrate fermentation by CitAB in Escherichia coli. Biosci. Biotechnol. Biochem. 2008;72:3011-3014.
111. Yamamoto K, Matsumoto F, Minagawa S, Oshima T, Fujita N, Ogasawara N, Ishihama A. Characterization of CitA-CitB signal transduction activating genes involved in anaerobic citrate catabolism in Escherichia coli. Biosci. Biotechnol. Biochem. 2009;73:346-350.
112. Cariss SJ, Tayler AE, Avison MB. Defining the growth conditions and promoter-proximal DNA sequences required for activation of gene expression by CreBC in Escherichia coli. J. Bacteriol. 2008;190:3930-3939.
113. Reading NC, Torres AG, Kendall MM, Hughes DT, Yamamoto K, Sperandio V. A novel two-component signaling system that activates transcription of an enterohemorrhagic Escherichia coli effector involved in remodeling of host actin. J. Bacteriol. 2007;189:2468-2476.
114. Reichenbach B, Göpel Y, Görke B. Dual control by perfectly overlapping sigma 54- and sigma 70- promoters adjusts small RNA GlmY expression to different environmental signals. Mol. Microbiol. 2009;74:1054-1070.
115. Kraxenberger T, Fried L, Behr S, Jung K. First insights into the unexplored two-component system YehU/YehT in Escherichia coli. J. Bacteriol. 2012;194:4272-4284.
116. Fried L, Behr S, Jung K. Identification of a target gene and activating stimulus for the YpdA/YpdB histidine kinase/response regulator system in Escherichia coli. J. Bacteriol. 2013;195:807-815.