Control of MarRAB operon in Escherichia coli via autoactivation and autorepression

Biophysical Journal

Volumn 109, Issue 7, 2015, Pages 1497-1508

  Prajapat, Mahendra Kumar ^a   Jain, Kirti ^a   Saini, Supreet ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY BOMBAY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; MARA PROTEIN, E COLI; MARR PROTEIN, E COLI; MULTIPLE ANTIBIOTIC RESISTANCE PROTEIN B; REPRESSOR PROTEIN;

BIOLOGICAL MODEL; COMPUTER SIMULATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; KINETICS; MARKOV CHAIN; METABOLISM; OPERON; REGULON;

BACTERIAL PROTEINS; COMPUTER SIMULATION; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; KINETICS; MODELS, GENETIC; OPERON; REGULON; REPRESSOR PROTEINS; STOCHASTIC PROCESSES;

EID: 84943618959     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.08.017     Document Type: Article

References (83)

1. D. Thieffry, and A.M. Huerta J. Collado-Vides From specific gene regulation to genomic networks: a global analysis of transcriptional regulation in Escherichia coli BioEssays 20 1998 433 440
2. S.S. Shen-Orr, and R. Milo U. Alon Network motifs in the transcriptional regulation network of Escherichia coli Nat. Genet. 31 2002 64 68
3. D.M. Wolf, and A.P. Arkin Motifs, modules and games in bacteria Curr. Opin. Microbiol. 6 2003 125 134
4. D. Nevozhay, and R.M. Adams G. Balázsi Negative autoregulation linearizes the dose-response and suppresses the heterogeneity of gene expression Proc. Natl. Acad. Sci. USA 106 2009 5123 5128
5. A. Becskei, and L. Serrano Engineering stability in gene networks by autoregulation Nature 405 2000 590 593
6. B. Novák, and J.J. Tyson Design principles of biochemical oscillators Nat. Rev. Mol. Cell Biol. 9 2008 981 991
7. A.Y. Mitrophanov, and E.A. Groisman Positive feedback in cellular control systems BioEssays 30 2008 542 555
8. Z. Cheng, and F. Liu W. Wang Robustness analysis of cellular memory in an autoactivating positive feedback system FEBS Lett. 582 2008 3776 3782
9. D. Kim, Y.K. Kwon, and K.H. Cho Coupled positive and negative feedback circuits form an essential building block of cellular signaling pathways BioEssays 29 2007 85 90
10. X.J. Tian, and X.P. Zhang W. Wang Interlinking positive and negative feedback loops creates a tunable motif in gene regulatory networks Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 80 2009 011926
11. S.A. Ramsey, and J.J. Smith J.D. Aitchison Dual feedback loops in the GAL regulon suppress cellular heterogeneity in yeast Nat. Genet. 38 2006 1082 1087
12. U.S. Bhalla, and R. Iyengar Robustness of the bistable behavior of a biological signaling feedback loop Chaos 11 2001 221 226
13. J.R. Pomerening, E.D. Sontag, and J.E. Ferrell Jr. Building a cell cycle oscillator: hysteresis and bistability in the activation of Cdc2 Nat. Cell Biol. 5 2003 346 351
14. L.P. Shearman, and S. Sriram S.M. Reppert Interacting molecular loops in the mammalian circadian clock Science 288 2000 1013 1019
15. L.P. Randall, and M.J. Woodward The multiple antibiotic resistance (mar) locus and its significance Res. Vet. Sci. 72 2002 87 93
16. A.M. George, and S.B. Levy Amplifiable resistance to tetracycline, chloramphenicol, and other antibiotics in Escherichia coli: involvement of a non-plasmid-determined efflux of tetracycline J. Bacteriol. 155 1983 531 540
17. A.M. George, and S.B. Levy Gene in the major cotransduction gap of the Escherichia coli K-12 linkage map required for the expression of chromosomal resistance to tetracycline and other antibiotics J. Bacteriol. 155 1983 541 548
18. M.N. Alekshun, and S.B. Levy Regulation of chromosomally mediated multiple antibiotic resistance: the mar regulon Antimicrob. Agents Chemother. 41 1997 2067 2075
19. R.G. Martin, P.S. Nyantakyi, and J.L. Rosner Regulation of the multiple antibiotic resistance (mar) regulon by marORA sequences in Escherichia coli J. Bacteriol. 177 1995 4176 4178
20. L. Vinué, L.M. McMurry, and S.B. Levy The 216-bp marB gene of the marRAB operon in Escherichia coli encodes a periplasmic protein which reduces the transcription rate of marA FEMS Microbiol. Lett. 345 2013 49 55
21. S.P. Cohen, H. Hächler, and S.B. Levy Genetic and functional analysis of the multiple antibiotic resistance (mar) locus in Escherichia coli J. Bacteriol. 175 1993 1484 1492
22. R.G. Martin, and J.L. Rosner Binding of purified multiple antibiotic-resistance repressor protein (MarR) to mar operator sequences Proc. Natl. Acad. Sci. USA 92 1995 5456 5460
23. M.N. Alekshun, and S.B. Levy Alteration of the repressor activity of MarR, the negative regulator of the Escherichia coli marRAB locus, by multiple chemicals in vitro J. Bacteriol. 181 1999 4669 4672
24. S.P. Cohen, and S.B. Levy J.L. Rosner Salicylate induction of antibiotic resistance in Escherichia coli: activation of the mar operon and a mar-independent pathway J. Bacteriol. 175 1993 7856 7862
25. R.G. Martin, and K.W. Jair J.L. Rosner Autoactivation of the marRAB multiple antibiotic resistance operon by the MarA transcriptional activator in Escherichia coli J. Bacteriol. 178 1996 2216 2223
26. M.C. Sulavik, L.F. Gambino, and P.F. Miller The MarR repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli: prototypic member of a family of bacterial regulatory proteins involved in sensing phenolic compounds Mol. Med. 1 1995 436 446
27. A.S. Seoane, and S.B. Levy Characterization of MarR, the repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli J. Bacteriol. 177 1995 3414 3419
28. R. Tobes, and J.L. Ramos AraC-XylS database: a family of positive transcriptional regulators in bacteria Nucleic Acids Res. 30 2002 318 321
29. S. Rhee, and R.G. Martin D.R. Davies A novel DNA-binding motif in MarA: the first structure for an AraC family transcriptional activator Proc. Natl. Acad. Sci. USA 95 1998 10413 10418
30. K.L. Griffith, I.M. Shah, and R.E. Wolf Jr. 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 2004 1801 1816
31. R.G. Martin, and W.K. Gillette J.L. Rosner 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 1999 431 441
32. H. Okusu, D. Ma, and H. Nikaido AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants J. Bacteriol. 178 1996 306 308
33. T. Schneiders, and T.M. Barbosa S.B. Levy The Escherichia coli transcriptional regulator MarA directly represses transcription of purA and hdeA J. Biol. Chem. 279 2004 9037 9042
34. J.A. Fralick Evidence that TolC is required for functioning of the Mar/AcrAB efflux pump of Escherichia coli J. Bacteriol. 178 1996 5803 5805
35. S. White, and F.E. Tuttle J.L. Slonczewski pH dependence and gene structure of inaA in Escherichia coli J. Bacteriol. 174 1992 1537 1543
36. K.W. Jair, and R.G. Martin R.E. Wolf Jr. Purification and regulatory properties of MarA protein, a transcriptional activator of Escherichia coli multiple antibiotic and superoxide resistance promoters J. Bacteriol. 177 1995 7100 7104
37. D.G. White, and J.D. Goldman S.B. Levy Role of the acrAB locus in organic solvent tolerance mediated by expression of marA, soxS, or robA in Escherichia coli J. Bacteriol. 179 1997 6122 6126
38. K.W. Jair, and X. Yu R.E. Wolf Jr. 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 1996 2507 2513
39. Z. Li, and B. Demple SoxS, an activator of superoxide stress genes in Escherichia coli. Purification and interaction with DNA J. Biol. Chem. 269 1994 18371 18377
40. R.G. Martin, and E.S. Bartlett M.E. Wall Activation of the Escherichia coli marA/soxS/rob regulon in response to transcriptional activator concentration J. Mol. Biol. 380 2008 278 284
41. R.G. Martin, W.K. Gillette, and J.L. Rosner Promoter discrimination by the related transcriptional activators MarA and SoxS: differential regulation by differential binding Mol. Microbiol. 35 2000 623 634
42. R.G. Martin, and J.L. Rosner 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 2002 1611 1624
43. T.M. Barbosa, and S.B. Levy Differential expression of over 60 chromosomal genes in Escherichia coli by constitutive expression of MarA J. Bacteriol. 182 2000 3467 3474
44. L.M. Chubiz, G.D. Glekas, and C.V. Rao Transcriptional cross talk within the mar-sox-rob regulon in Escherichia coli is limited to the Rob and marRAB operons J. Bacteriol. 194 2012 4867 4875
45. L.M. McMurry, and S.B. Levy Evidence that regulatory protein MarA of Escherichia coli represses rob by steric hindrance J. Bacteriol. 192 2010 3977 3982
46. C. Michán, M. Manchado, and C. Pueyo SoxRS down-regulation of rob transcription J. Bacteriol. 184 2002 4733 4738
47. R.G. Martin, and J.L. Rosner Transcriptional and translational regulation of the marRAB multiple antibiotic resistance operon in Escherichia coli Mol. Microbiol. 53 2004 183 191
48. J. Garcia-Bernardo, and M.J. Dunlop Tunable stochastic pulsing in the Escherichia coli multiple antibiotic resistance network from interlinked positive and negative feedback loops PLOS Comput. Biol. 9 2013 e1003229
49. M.N. Alekshun, and S.B. Levy J.F. Head The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3 Å resolution Nat. Struct. Biol. 8 2001 710 714
50. R.R. Ariza, and S.P. Cohen B. Demple Repressor mutations in the marRAB operon that activate oxidative stress genes and multiple antibiotic resistance in Escherichia coli J. Bacteriol. 176 1994 143 148
51. S.P. Wilkinson, and A. Grove Ligand-responsive transcriptional regulation by members of the MarR family of winged helix proteins Curr. Issues Mol. Biol. 8 2006 51 62
52. D.T. Gillespie Exact stochastic simulation of coupled chemical reactions J. Phys. Chem. 81 1977 2340 2361
53. D.T. Gillespie A general method for numerically simulating the stochastic time evolution of coupled chemical reactions J. Comput. Phys. 22 1976 403 434
54. M.K. Prajapat, and S. Saini Role of feedback and network architecture in controlling virulence gene expression in Bordetella Mol. Biosyst. 9 2013 2635 2644
55. F.R. Blattner, and G. Plunkett 3rd Y. Shao The complete genome sequence of Escherichia coli K-12 Science 277 1997 1453 1462
56. S. Kalir, and J. McClure U. Alon Ordering genes in a flagella pathway by analysis of expression kinetics from living bacteria Science 292 2001 2080 2083
57. Prajapat, M. K., K. Jain,..., S. Saini. 2015. Revisiting demand rules for gene regulation. bioRxiv 01/2015.
58. H. Salgado, and M. Peralta-Gil J. Collado-Vides REGULONDB Ver. 8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more Nucleic Acids Res. 41 2013 D203 D213
59. M. Acar, A. Becskei, and A. van Oudenaarden Enhancement of cellular memory by reducing stochastic transitions Nature 435 2005 228 232
60. H.A. Mohamed, and W. Yao J.H. Byrne cAMP-response elements in Aplysia creb1, creb2, and Ap-uch promoters: implications for feedback loops modulating long term memory J. Biol. Chem. 280 2005 27035 27043
61. X.P. Zhang, and Z. Cheng W. Wang Linking fast and slow positive feedback loops creates an optimal bistable switch in cell signaling Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 76 2007 031924
62. O. Brandman, and J.E. Ferrell Jr. T. Meyer Interlinked fast and slow positive feedback loops drive reliable cell decisions Science 310 2005 496 498
63. M.M. Babu, and N.M. Luscombe S.A. Teichmann Structure and evolution of transcriptional regulatory networks Curr. Opin. Struct. Biol. 14 2004 283 291
64. M.N. Price, P.S. Dehal, and A.P. Arkin Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli Genome Biol. 9 2008 R4
65. M. Cosentino Lagomarsino, and P. Jona H. Isambert Hierarchy and feedback in the evolution of the Escherichia coli transcription network Proc. Natl. Acad. Sci. USA 104 2007 5516 5520
66. S.A. Teichmann, and M.M. Babu Gene regulatory network growth by duplication Nat. Genet. 36 2004 492 496
67. N. Rajewsky, and N.D. Socci E.D. Siggia The evolution of DNA regulatory regions for proteo-γ bacteria by interspecies comparisons Genome Res. 12 2002 298 308
68. I. Lozada-Chávez, S.C. Janga, and J. Collado-Vides Bacterial regulatory networks are extremely flexible in evolution Nucleic Acids Res. 34 2006 3434 3445
69. M.S. Gelfand Evolution of transcriptional regulatory networks in microbial genomes Curr. Opin. Struct. Biol. 16 2006 420 429
70. K.S. Zaret Stability and evolution of transcriptional regulatory networks Mol. Syst. Biol. 2 2006 2006-0021
71. I. Cases, and V. de Lorenzo Promoters in the environment: transcriptional regulation in its natural context Nat. Rev. Microbiol. 3 2005 105 118
72. D. Angeli, J.E. Ferrell Jr., and E.D. Sontag Detection of multistability, bifurcations, and hysteresis in a large class of biological positive-feedback systems Proc. Natl. Acad. Sci. USA 101 2004 1822 1827
73. J.R. Kim, Y. Yoon, and K.H. Cho Coupled feedback loops form dynamic motifs of cellular networks Biophys. J. 94 2008 359 365
74. N. Rosenfeld, M.B. Elowitz, and U. Alon Negative autoregulation speeds the response times of transcription networks J. Mol. Biol. 323 2002 785 793
75. A.L. Koch The protein burden of lac operon products J. Mol. Evol. 19 1983 455 462
76. C.G. Kurland, and H. Dong Bacterial growth inhibition by overproduction of protein Mol. Microbiol. 21 1996 1 4
77. I. Shachrai, and A. Zaslaver E. Dekel Cost of unneeded proteins in E. coli is reduced after several generations in exponential growth Mol. Cell 38 2010 758 767
78. W. Xiong, and J.E. Ferrell Jr. A positive-feedback-based bistable 'memory module' that governs a cell fate decision Nature 426 2003 460 465
79. S. Saini, and J.R. Ellermeier C.V. Rao The role of coupled positive feedback in the expression of the SPI1 type three secretion system in Salmonella PLoS Pathog. 6 2010 e1001025
80. P. Paszek, and S. Ryan M.R. White Population robustness arising from cellular heterogeneity Proc. Natl. Acad. Sci. USA 107 2010 11644 11649
81. H.J. Beaumont, and J. Gallie P.B. Rainey Experimental evolution of bet hedging Nature 462 2009 90 93
82. A.J. Grimbergen, and J. Siebring O.P. Kuipers Microbial bet-hedging: the power of being different Curr. Opin. Microbiol. 25 2015 67 72
83. J.W. Veening, W.K. Smits, and O.P. Kuipers Bistability, epigenetics, and bet-hedging in bacteria Annu. Rev. Microbiol. 62 2008 193 210