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Chapter 15 : The Regulon

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Abstract:

This chapter reviews the current understanding of the regulon, and focusing on some of the more interesting features of regulation. It highlights the considerable homology and cross-regulation that exists between MarA and the related transcriptional regulators SoxS and Rob. The extensive overlap observed in the regulons and phenotypes associated with these proteins is discussed in this chapter. The regulon consists of a large group of chromosomal genes directly or indirectly regulated by MarA. This regulon is also frequently referred to as the //regulon because the two MarA homologues, SoxS and Rob, recognize the same regulatory DNA element in the promoter of regulated genes. More recently, with the advent of genome-wide transcriptome analysis, two independent macroarray studies have provided new insights into the multitude of genes that constitute the transcriptional network of the regulon. Importantly, although multiple marboxes can be found in the promoter regions of regulon genes, in vivo studies have demonstrated that it is the one closest to the promoter signatures that plays the major role in transcriptional control. While understanding the molecular cross-talk that underlies regulon expression and how this is elicited by natural stresses remains an important goal for the future, the prevailing long-term objective is to understand the physiological relevance of the changes within the cell and to more accurately map the development of the phenotype. This will offer new possibilities for identifying targets for novel antimicrobial therapies to better deal with the growing problem of antimicrobial resistance.

Citation: Barbosa T, Pomposiello P. 2005. The Regulon, p 209-223. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch15

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Figure 1

MarA, SoxS, and Rob regulatory circuits. MarA, SoxS, and Rob can mediate a global cellular stress response to different toxic compounds by governing the expression of a common network of chromosomal genes, the regulon, which is involved in a variety of different cell functions. This includes active efflux of toxic compounds (e.g., through the activation of the AcrAB-TolC complex), reduction of cell permeability (e.g., through the decreased expression of porins, such as OmpF, and modulation of expression of other membrane proteins), detoxification (e.g., through the increased expression of cytoprotective and repair enzymes), and others. A multitude of external stresses are sensed by the MarRAB, SoxRS, and Rob systems, which ultimately result in the modulation through different pathways of the expression of the three transcriptional factors. Some of these stimuli result in the activation of more than one sensory system, while other stimuli display restricted activation of only one system. For example, MarA is produced when MarR is inactivated either by mutations or by interaction with inducing agents, such as phenolic compounds and certain oxidative stress agents. expression can also be induced by SoxS and Rob and enhanced by Fis. Additionally, MppA, in combination with mutations at an unknown locus in , is capable of influencing expression through what appears to be a MarR-independent pathway. In contrast, oxidative stress agents oxidize SoxR, which in turn activates expression of SoxS. No other signals are known to result in increased levels of SoxS. Rob is produced constitutively, but recently it has been shown that its expression can be repressed in a SoxS-dependent manner. Although Rob is known to accumulate to high concentrations in the cell, its activation in vivo is thought to be mediated by inducing agents that bind to the carboxyl-terminus effector-binding domain of this protein, such as 2,2′- and 4,4′- dipyridyl, bile salts, and fatty acids (represented as E in the figure).

Citation: Barbosa T, Pomposiello P. 2005. The Regulon, p 209-223. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch15
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Figure 2

Northern blotting reveals differential regulation of gene transcription by SoxS and MarA. The SoxS and MarA proteins were expressed in in the absence of stress from IPTG-inducible constructs. Total RNA was extracted, purified, separated by electrophoresis in an agarose gel, transferred to a Nytran membrane, and hybridized sequentially with gene-specific probes. The bottom panel shows the EtBr stain of a gel run in parallel with the same amounts of total RNA.

Citation: Barbosa T, Pomposiello P. 2005. The Regulon, p 209-223. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch15
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Figure 3

MarA, SoxS, and Rob recognition sequence within the promoter of controlled genes. (A) Comparison of the most recently defined consensus for the 20 bp degenerate marbox sequences in the forward orientation: “old consensus” ( ) and “new consensus” ( ); N, any base; R = A/G; W = A/T; Y = C/T; G = any base but G. The location of the most conserved recognition elements within the marbox sequence, RE1 and RE2, is indicated. (B) Location and orientation of the marbox in class I (backward), class I* (forward), and class II regulon-activated promoters ( ). (C) Location and orientation of the marbox in the promoters of down-regulated genes ( ). Arrows depict the marbox, while the direction of the arrow-head represents the functional orientation of the marbox relative to the −10 and −35 RNAP recognition sequences (gray rectangles). Distances between the marbox and the −10 hexamer are indicated.

Citation: Barbosa T, Pomposiello P. 2005. The Regulon, p 209-223. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch15
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References

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1. Alekshun, M. N.,, and S. B. Levy. 1999. Alteration of the repressor activity of MarR, the negative regulator of the Escherichia coli marRAB locus, by multiple chemicals in vitro. J. Bacteriol. 181: 4669 4672.
2. Alekshun, M. N.,, and S. B. Levy. 1999. Characterization of MarR superrepressor mutants. J. Bacteriol. 181: 3303 3306.
3. Alekshun, M. N.,, and S. B. Levy. 1999. The mar regulon: multiple resistance to antibiotics and other toxic chemicals. Trends Microbiol. 7: 410 413.
4. Alekshun, M. N.,, and S. B. Levy. 1997. Regulation of chromosomally mediated multiple antibiotic resistance: the mar regulon. Antimicrob. Agents Chemother. 41: 2067 2075.
5. Amabile-Cuevas, C. F.,, and B. Demple. 1991. Molecular characterization of the soxRS genes of Escherichia coli: two genes control a superoxide stress regulon. Nucleic Acids Res. 19: 4479 4484.
6. Aono, R.,, N. Tsukagoshi,, and M. Yamamoto. 1998. Involvement of outer membrane protein TolC, a possible member of the mar-sox regulon, in maintenance and improvement of organic solvent tolerance of Escherichia coli K-12. J. Bacteriol. 180: 938 944.
7. Ariza, R. R.,, Z. Li,, N. Ringstad,, and B. Demple. 1995. Activation of multiple antibiotic resistance and binding of stressinducible promoters by Escherichia coli Rob protein. J. Bacteriol. 177: 1655 1661.
8. Barbosa, T. M.,, and S. B. Levy. 2002. Activation of the Escherichia coli nfnB gene by MarA through a highly divergent marbox in a class II promoter. Mol. Microbiol. 45: 191 202.
9. Barbosa, T. M.,, and S. B. Levy. 2000. Differential expression of over 60 chromosomal genes in Escherichia coli by constitutive expression of MarA. J. Bacteriol. 182: 3467 3474.
10. Barbosa, T. M.,, and S. B. Levy. 1999. Presented at the 99th General Meeting of the American Society for Microbiology, Chicago, USA. Abstract A42, p 9.
11. Bennik, M. H.,, P. J. Pomposiello,, D. F. Thorne,, and B. Demple. 2000. Defining a rob regulon in Escherichia coli by using transposon mutagenesis. J. Bacteriol. 182: 3794 3801.
12. Bina, X.,, V. Perreten,, and S. B. Levy. 2003. The periplasmic protein MppA requires an additional mutated locus to repress marA expression in Escherichia coli. J. Bacteriol. 185: 1465 1469.
13. Chou, J. H.,, J. T. Greenberg,, and B. Demple. 1993. Posttranscriptional repression of Escherichia coli OmpF protein in response to redox stress: positive control of the micF antisense RNA by the soxRS locus. J. Bacteriol. 175: 1026 1031.
14. Cohen, S. P.,, H. Hachler,, and S. B. Levy. 1993. Genetic and functional analysis of the multiple antibiotic resistance ( mar) locus in Escherichia coli. J. Bacteriol. 175: 1484 1492.
15. Cohen, S. P.,, S. B. Levy,, J. Foulds,, and J. L. Rosner. 1993. Salicylate induction of antibiotic resistance in Escherichia coli: activation of the mar operon and a mar-independent pathway. J. Bacteriol. 175: 7856 7862.
16. Cohen, S. P.,, L. M. McMurry,, D. C. Hooper,, J. S. Wolfson,, and S. B. Levy. 1989. Cross-resistance to fluoroquinolones in multiple-antibiotic-resistant (Mar) Escherichia coli selected by tetracycline or chloramphenicol: decreased drug accumulation associated with membrane changes in addition to OmpF reduction. Antimicrob. Agents Chemother. 33: 1318 1325.
17. Cohen, S. P.,, L. M. McMurry,, and S. B. Levy. 1988. marA locus causes decreased expression of OmpF porin in multipleantibiotic- resistant (Mar) mutants of Escherichia coli. J. Bacteriol. 170: 5416 5422.
18. Dangi, B.,, P. Pelupessey,, R. G. Martin,, J. L. Rosner,, J. M. Louis,, and A. M. Gronenborn. 2001. Structure and dynamics of MarADNA complexes: an NMR investigation. J. Mol. Biol. 314: 113 127.
19. Delihas, N.,, and S. Forst. 2001. MicF: an antisense RNA gene involved in response of Escherichia coli to global stress factors. J. Mol. Biol. 313: 1 12.
20. Ding, H.,, and B. Demple. 2000. Direct nitric oxide signal transduction via nitrosylation of iron-sulfur centers in the SoxR transcription activator. Proc. Natl. Acad. Sci. USA 97: 5146 5150.
21. Ding, H.,, E. Hidalgo,, and B. Demple. 1996. The redox state of the [2Fe-2S] clusters in SoxR protein regulates its activity as a transcription factor. J. Biol. Chem. 271: 33173 33175.
22. Ding, H. G.,, and B. Demple. 1997. In vivo kinetics of a redoxregulated transcriptional switch. Proc. Natl. Acad. Sci. USA 94: 8445 8449.
23. Egan, S. M.,, A. J. Pease,, J. Lang,, X. Li,, V. Rao,, W. K. Gillette,, R. Ruiz,, J. L. Ramos,, and R. E. Wolf, Jr. 2000. Transcription activation by a variety of AraC/XylS family activators does not depend on the class II-specific activation determinant in the Nterminal domain of the RNA polymerase alpha subunit. J. Bacteriol. 182: 7075 7077.
24. Fralick, J. A. 1996. Evidence that TolC is required for functioning of the Mar/AcrAB efflux pump of Escherichia coli. J. Bacteriol. 178: 5803 5805.
25. Gajiwala, K. S.,, and S. K. Burley. 2000. HDEA, a periplasmic protein that supports acid resistance in pathogenic enteric bacteria. J. Mol. Biol. 295: 605 612.
26. Gallegos, M. T.,, R. Schleif,, A. Bairoch,, K. Hofmann,, and J. L. Ramos. 1997. Arac/XylS family of transcriptional regulators. Microbiol. Mol. Biol. Rev. 61: 393 410.
27. Gaudu, P.,, and B. Weiss. 2000. Flavodoxin mutants of Escherichia coli K-12. J. Bacteriol. 182: 1788 1793.
28. Gaudu, P.,, and B. Weiss. 1996. SoxR, a [2Fe-2S] transcription factor, is active only in its oxidized form. Proc. Natl. Acad. Sci. USA 93: 10094 10098.
29. Gillette, W. K.,, R. G. Martin,, and J. L. Rosner. 2000. Probing the Escherichia coli transcriptional activator MarA using alanine- scanning mutagenesis: residues important for DNA binding and activation. J. Mol. Biol. 299: 1245 1255.
30. Godon, C.,, G. Lagniel,, J. Lee,, J. M. Buhler,, S. Kieffer,, M. Perrot,, H. Boucherie,, M. B. Toledano,, and J. Labarre. 1998. The H2O2 stimulon in Saccharomyces cerevisiae. J. Biol. Chem. 273: 22480 22489.
31. Gralla, J. D.,, and J. Collado-Vides,. 1996. Organization and function of transcriptional regulatory elements, p. 1232 1245. In F. C. Neidhardt (ed.), Escherichia coli and Salmonella: Cellular and Molecular Biology. ASM Press, Washington, D.C.
32. Gralnick, J.,, and D. Downs. 2001. Protection from superoxide damage associated with an increased level of the YggX protein in Salmonella enterica. Proc. Natl. Acad. Sci. USA 98: 8030 8035.
33. Gralnick, J. A.,, and D. M. Downs. 2003. The YggX protein of Salmonella enterica is involved in Fe(II) trafficking and minimizes the DNA damage caused by hydroxyl radicals: residue CYS-7 is essential for YggX function. J. Biol. Chem. 278: 20708 20715.
34. Greenberg, J. T.,, P. Monach,, J. H. Chou,, P. D. Josephy,, and B. Demple. 1990. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc. Natl. Acad. Sci. USA 87: 6181 6185.
35. Griffith, K. L.,, I. M. Shah,, T. E. Myers,, M. C. O’Neill,, and R. E. Wolf, Jr. 2002. Evidence for “pre-recruitment” as a new mechanism of transcription activation in Escherichia coli: the large excess of SoxS binding sites per cell relative to the number of SoxS molecules per cell. Biochem. Biophys. Res. Commun. 291: 979 986.
36. Griffith, K. L.,, I. M. Shah,, and R. E. Wolf, Jr. 2004. Proteolytic degradation of Escherichia coli transcription activators SoxS and MarA as the mechanism for reversing the induction of the superoxide (SoxRS) and multiple antibiotic resistance (Mar) regulons. Mol. Microbiol. 51: 1801 1816.
37. Griffith, K. L.,, and R. E. Wolf, Jr. 2001. Systematic mutagenesis of the DNA binding sites for SoxS in the Escherichia coli zwf and fpr promoters: identifying nucleotides required for DNA binding and transcription activation. Mol. Microbiol. 40: 1141 1154.
38. Gruer, M. J.,, and J. R. Guest. 1994. Two genetically-distinct and differentially-regulated aconitases (AcnA and AcnB) in Escherichia coli. Microbiology 140: 2531 2541.
39. Hidalgo, E.,, and B. Demple. 1994. An iron-sulfur center essential for transcriptional activation by the redox-sensing SoxR protein. EMBO J. 13: 138 146.
40. Hidalgo, E.,, V. Leautaud,, and B. Demple. 1998. The redoxregulated SoxR protein acts from a single DNA site as a repressor and an allosteric activator. EMBO J. 17: 2629 2636.
41. Jair, K. W.,, W. P. Fawcett,, N. Fujita,, A. Ishihama,, and R. E. Wolf, Jr. 1996. Ambidextrous transcriptional activation by SoxS: requirement for the C-terminal domain of the RNA polymerase alpha subunit in a subset of Escherichia coli superoxide- inducible genes. Mol. Microbiol. 19: 307 317.
42. Jair, K. W.,, R. G. Martin,, J. L. Rosner,, N. Fujita,, A. Ishihama,, and R. E. Wolf, Jr. 1995. Purification and regulatory properties of MarA protein, a transcriptional activator of Escherichia coli multiple antibiotic and superoxide resistance promoters. J. Bacteriol. 177: 7100 7104.
43. Jair, K. W.,, X. Yu,, K. Skarstad,, B. Thony,, N. Fujita,, A. Ishihama,, and R. E. Wolf, Jr. 1996. Transcriptional activation of promoters of the superoxide and multiple antibiotic resistance regulons by Rob, a binding protein of the Escherichia coli origin of chromosomal replication. J. Bacteriol. 178: 2507 2513.
44. Koh, Y. S.,, J. Choih,, J. H. Lee,, and J. H. Roe. 1996. Regulation of the ribA gene encoding GTP cyclohydrolase II by the soxRS locus in Escherichia coli. Mol. Gen. Genet. 251: 591 598.
45. Koo, M. S.,, J. H. Lee,, S. Y. Rah,, W. S. Yeo,, J. W. Lee,, K. L. Lee,, Y. S. Koh,, S. O. Kang,, and J. H. Roe. 2003. A reducing system of the superoxide sensor SoxR in Escherichia coli. EMBO J. 22: 2614 2622.
46. Kwon, H. J.,, M. H. Bennik,, B. Demple,, and T. Ellenberger. 2000. Crystal structure of the Escherichia coli Rob transcription factor in complex with DNA. Nat. Struct. Biol. 7: 424 430.
47. Li, Z.,, and B. Demple. 1996. Sequence specificity for DNA binding by Escherichia coli SoxS and Rob proteins. Mol. Microbiol. 20: 937 945.
48. Li, Z.,, and B. Demple. 1994. SoxS, an activator of superoxide stress genes in Escherichia coli. Purification and interaction with DNA. J. Biol. Chem. 269: 18371 18377.
49. Liochev, S. I.,, and I. Fridovich. 1992. Fumarase C, the stable fumarase of Escherichia coli, is controlled by the soxRS regulon. Proc. Natl. Acad. Sci. USA 89: 5892 5896.
50. Liochev, S. I.,, A. Hausladen,, W. F. Beyer, Jr.,, and I. Fridovich. 1994. NADPH: ferredoxin oxidoreductase acts as a paraquat diaphorase and is a member of the soxRS regulon. Proc. Natl. Acad. Sci. USA 91: 1328 1331.
51. Liochev, S. I.,, A. Hausladen,, and I. Fridovich. 1999. Nitroreductase A is regulated as a member of the soxRS regulon of Escherichia coli. Proc. Natl. Acad. Sci. USA 96: 3537 3579.
52. Ma, D.,, M. Alberti,, C. Lynch,, H. Nikaido,, and J. E. Hearst. 1996. The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol. Microbiol. 19: 101 112.
53. Maneewannakul, K.,, and S. B. Levy. 1996. Identification for mar mutants among quinolone-resistant clinical isolates of Escherichia coli. Antimicrob. Agents Chemother. 40: 1695 1698.
54. Martin, R. G.,, W. K. Gillette,, N. I. Martin,, and J. L. Rosner. 2002. Complex formation between activator and RNA polymerase as the basis for transcriptional activation by MarA and SoxS in Escherichia coli. Mol. Microbiol. 43: 355 370.
55. Martin, R. G.,, W. K. Gillette,, S. Rhee,, and J. L. Rosner. 1999. Structural requirements for marbox function in transcriptional activation of mar/sox/rob regulon promoters in Escherichia coli: sequence, orientation and spatial relationship to the core promoter. Mol. Microbiol. 34: 431 441.
56. Martin, R. G.,, W. K. Gillette,, and J. L. Rosner. 2000. Promoter discrimination by the related transcriptional activators MarA and SoxS: differential regulation by differential binding. Mol. Microbiol. 35: 623 634.
57. Martin, R. G.,, K. W. Jair,, R. E. Wolf, Jr.,, and J. L. Rosner. 1996. Autoactivation of the marRAB multiple antibiotic resistance operon by the MarA transcriptional activator in Escherichia coli. J. Bacteriol. 178: 2216 2223.
58. Martin, R. G.,, and J. L. Rosner. 2003. Analysis of microarray data for the marA, soxS, and rob regulons of Escherichia coli. Methods Enzymol. 370: 278 280.
59. Martin, R. G.,, and J. L. Rosner. 2001. The AraC transcriptional activators. Curr. Opin. Microbiol. 4: 132 137.
60. Martin, R. G.,, and J. L. Rosner. 1997. Fis, an accessorial factor for transcriptional activation of the mar (multiple antibiotic resistance) promoter of Escherichia coli in the presence of the activator MarA, SoxS, or Rob. J. Bacteriol. 179: 7410 7419.
61. Martin, R. G.,, and J. L. Rosner. 2002. Genomics of the marA/soxS/rob regulon of Escherichia coli: identification of directly activated promoters by application of molecular genetics and informatics to microarray data. Mol. Microbiol. 44: 1611 1624.
62. McMurry, L. M.,, M. Oethinger,, and S. B. Levy. 1998. Overexpression of marA, soxS or acrAB produces resistance to triclosan in Escherichia coli. FEMS Microbiol. Lett. 166: 305 309.
63. Michan, C.,, M. Manchado,, and C. Pueyo. 2002. SoxRS downregulation of rob transcription. J. Bacteriol. 184: 4733 4738.
64. Miller, P. F.,, L. F. Gambino,, M. C. Sulavik,, and S. J. Gracheck. 1994. Genetic relationship between soxRS and mar loci in promoting multiple antibiotic resistance in Escherichia coli. Antimicrob. Agents Chemother. 38: 1773 1779.
65. Moken, M. C.,, L. M. McMurry,, and S. B. Levy. 1997. Selection of multiple-antibiotic-resistant ( mar) mutants of Escherichia coli by using the disinfectant pine oil: roles of the mar and acrAB loci. Antimicrob. Agents Chemother. 41: 2770 2772.
66. Nakajima, H.,, K. Kobayashi,, M. Kobayashi,, H. Asako,, and R. Aono. 1995. Overexpression of the robA gene increases organic solvent tolerance and multiple antibiotic and heavy metal ion resistance in Escherichia coli. Appl. Environ. Microbiol. 61: 2302 2307.
67. Nikaido, H.,, M. Basina,, V. Nguyen,, and E. Y. Rosenberg. 1998. Multidrug efflux pump AcrAB of Salmonella typhimurium excretes only those beta-lactam antibiotics containing lipophilic side chains. J. Bacteriol. 180: 4686 4692.
68. Nunoshiba, T.,, T. de Rojas-Walker,, J. S. Wishnok,, S. R. Tannenbaum,, and B. Demple. 1993. Activation by nitric oxide of an oxidative-stress response that defends Escherichia coli against activated macrophages. Proc. Natl. Acad. Sci. USA 90: 9993 9997.
69. Nunoshiba, T.,, E. Hidalgo,, Z. Li,, and B. Demple. 1993. Negative autoregulation by the Escherichia coli SoxS protein: a dampening mechanism for the soxRS redox stress response. J. Bacteriol. 175: 7492 7494.
70. Okusu, H.,, D. Ma,, and H. Nikaido. 1996. AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants. J. Bacteriol. 178: 306 308.
71. Park, S. J.,, and R. P. Gunsalus. 1995. Oxygen, iron, carbon, and superoxide control of the fumarase fumA and fumC genes of Escherichia coli: role of the arcA, fnr, and soxR gene products. J. Bacteriol. 177: 6255 6262.
72. Paterson, E. S.,, S. E. Boucher,, and I. B. Lambert. 2002. Regulation of the nfsA gene in Escherichia coli by SoxS. J. Bacteriol. 184: 51 58.
73. Pomposiello, P. J.,, M. H. Bennik,, and B. Demple. 2001. Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J. Bacteriol. 183: 3890 3902.
74. Pomposiello, P. J.,, and B. Demple. 2002. Global adjustment of microbial physiology during free radical stress. Adv. Microb. Physiol. 46: 319 341.
75. Pomposiello, P. J.,, and B. Demple. 2000. Identification of SoxSregulated genes in Salmonella enterica serovar typhimurium. J. Bacteriol. 182: 23 29.
76. Pomposiello, P. J.,, and B. Demple. 2001. Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol. 19: 109 114.
77. Pomposiello, P. J.,, A. Koutsolioutsou,, D. Carrasco,, and B. Demple. 2003. SoxRS-regulated expression and genetic analysis of the yggX gene of Escherichia coli. J. Bacteriol. 185: 6624 6632.
78. Rhee, S.,, R. G. Martin,, J. L. Rosner,, and D. R. Davies. 1998. A novel DNA-binding motif in MarA: the first structure for an AraC family transcriptional activator. Proc. Natl. Acad. Sci. USA 95: 10413 10418.
79. Rhodius, V. A.,, and R. A. LaRossa. 2003. Uses and pitfalls of microarrays for studying transcriptional regulation. Curr. Opin. Microbiol. 6: 114 119.
80. Richmond, C. S.,, J. D. Glasner,, R. Mau,, H. Jin,, and F. R. Blattner. 1999. Genome-wide expression profiling in Escherichia coli K-12. Nucleic Acids Res. 27: 3821 3835.
81. Rosenberg, E. Y.,, D. Bertenthal,, M. L. Nilles,, K. P. Bertrand,, and H. Nikaido. 2003. Bile salts and fatty acids induce the expression of Escherichia coli AcrAB multidrug efflux pump through their interaction with Rob regulatory protein. Mol. Microbiol. 48: 1609 1619.
82. Rosner, J. L.,, B. Dangi,, A. M. Gronenborn,, and R. G. Martin. 2002. Posttranscriptional activation of the transcriptional activator Rob by dipyridyl in Escherichia coli. J. Bacteriol. 184: 1407 1416.
83. Rosner, J. L.,, and J. L. Slonczewski. 1994. Dual regulation of inaA by the multiple antibiotic resistance ( mar) and superoxide ( soxRS) stress response systems of Escherichia coli. J. Bacteriol. 176: 6262 6269.
84. Schneiders, T.,, T. M. Barbosa,, L. M. McMurry,, and S. B. Levy. 2004. The Escherichia coli transcriptional regulator MarA directly represses transcription of purA and hdeA. J. Biol. Chem. 279: 9037 9042.
85. Seoane, A. S.,, and S. B. Levy. 1995. Characterization of MarR, the repressor of the multiple antibiotic resistance ( mar) operon in Escherichia coli. J. Bacteriol. 177: 3414 3419.
86. Seoane, A. S.,, and S. B. Levy. 1995. Identification of new genes regulated by the marRAB operon in Escherichia coli. J. Bacteriol. 177: 530 535.
87. Sulavik, M. C.,, M. Dazer,, and P. F. Miller. 1997. The Salmonella typhimurium mar locus: molecular and genetic analyses and assessment of its role in virulence. J. Bacteriol. 179: 1857 1866.
88. Tsaneva, I. R.,, and B. Weiss. 1990. soxR, a locus governing a superoxide response regulon in Escherichia coli K-12. J. Bacteriol. 172: 4197 4205.
89. Van Dyk, T. K.,, B. L. Ayers,, R. W. Morgan,, and R. A. Larossa. 1998. Constricted flux through the branched-chain amino acid biosynthetic enzymes acetolactate synthase triggers elevated expression of genes reglated by rpoS and internal acidification. J. Bacteriol. 180: 785 792.
90. Varghese, S.,, Y. Tang,, and J. A. Imlay. 2003. Contrasting sensitivities of Escherichia coli Aconitases A and B to oxidation and iron depletion. J. Bacteriol. 185: 221 230.
91. Waterman, S. R.,, and P. L. Small. 1996. Identification of sigma S-dependent genes associated with the stationary-phase acidresistance phenotype of Shigella flexneri. Mol. Microbiol. 21: 925 940.
92. White, D. G.,, J. D. Goldman,, B. Demple,, and S. B. Levy. 1997. Role of the acrAB locus in organic solvent tolerance mediated by expression of marA, soxS, or robA in Escherichia coli. J. Bacteriol. 179: 6122 6126.
93. Wood, T. I.,, K. L. Griffith,, W. P. Fawcett,, K. W. Jair,, T. D. Schneider,, and R. E. Wolf, Jr. 1999. Interdependence of the position and orientation of SoxS binding sites in the tran scriptional activation of the class I subset of Escherichia coli superoxide- inducible promoters. Mol. Microbiol. 34: 414 430.
94. Woods, S. A.,, S. D. Schwartzbach,, and J. R. Guest. 1988. Two biochemically distinct classes of fumarase in Escherichia coli. Biochem. Biophys. Acta 954: 14 26.
95. Wu, J.,, and B. Weiss. 1991. Two divergently transcribed genes, soxR and soxS, control a superoxide response regulon of Escherichia coli. J. Bacteriol. 173: 2864 2871.
96. Zheng, M.,, B. Doan,, T. D. Schneider,, and G. Storz. 1999. OxyR and SoxRS regulation of fur. J. Bacteriol. 181: 4639 4643.
97. Zheng, M.,, and G. Storz. 2000. Redox sensing by prokaryotic transcription factors. Biochem. Pharmacol. 59: 1 6.

Tables

Generic image for table
Table 1

Bona fide regulon genes

Regulon members whose differential expression by MarA and/or SoxS has been confirmed by more than one experimental approach.

For specific marbox sequences and respective configurations, see references 8, 55, and 61 and references therein. ND, not determined; NA, not applied, indirect regulation.

+, activation; ++, relatively larger degree of activation; −, repression; ?, no available comparative data.

Due to space restriction, we are only able to refer to selected publications. The reader is strongly advised to consult original research studies referenced therein.

Citation: Barbosa T, Pomposiello P. 2005. The Regulon, p 209-223. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch15

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