Abstract
SoxR is a transcription activator governing a cellular response to superoxide and nitric oxide in Escherichia coli. SoxR protein is a homodimer, and each monomer has a redox-active [2Fe-2S] cluster. Oxidation and reduction of the [2Fe-2S] clusters can reversibly activate and inactivate SoxR transcriptional activity. Here, we use electron paramagnetic resonance spectroscopy to follow the redox-switching process of SoxR protein in vivo. SoxR [2Fe-2S] clusters were in the fully reduced state during normal aerobic growth, but were completely oxidized after only 2-min aerobic exposure of the cells to superoxide-generating agents such as paraquat. The oxidized SoxR [2Fe-2S] clusters were rapidly re-reduced in vivo once the oxidative stress was removed. The in vivo kinetics of SoxR [2Fe-2S] cluster oxidation and reduction exactly paralleled the increase and decrease of transcription of soxS, the target gene for SoxR. The kinetic analysis also revealed that an oxidative stress-linked decrease in soxS mRNA stability contributes to the rapid attainment of a new steady state after SoxR activation. Such a redox stress-related change in soxS mRNA stability may represent a new level of biological control.
MeSH Terms
Bacterial Proteins/genetics,metabolism
Escherichia coli/genetics,metabolism
Gene Expression Regulation, Bacterial
Magnetic Resonance Spectroscopy
Oxidation-Reduction
Transcription Factors/genetics,metabolism
Transcription, Genetic
Chemicals
Bacterial Proteins
Transcription Factors
SoxR protein, Bacteria
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Ding H
Department of Molecular and Cellular Toxicology, School of Public Health, Harvard University, 665 Huntington Avenue, Boston, MA 02115-6021, USA.
Demple B
References (27)
27 references, click to expand
-
Superoxide radical: an endogenous toxicant.
Annu Rev Pharmacol Toxicol. 1983;23:239-57
PMID: 6307121
-
Spacing of promoter elements regulates the basal expression of the soxS gene and converts SoxR from a transcriptional activator into a repressor.
EMBO J. 1997 Mar 3;16(5):1056-65
PMID: 9118944
-
Effects of paraquat on Escherichia coli: differences between B and K-12 strains.
J Bacteriol. 1990 Feb;172(2):686-90
PMID: 2404951
-
Molecular characterization of the soxRS genes of Escherichia coli: two genes control a superoxide stress regulon.
Nucleic Acids Res. 1991 Aug 25;19(16):4479-84
PMID: 1653416
-
Two-stage induction of the soxRS (superoxide response) regulon of Escherichia coli.
J Bacteriol. 1992 Jun;174(12):3915-20
PMID: 1317841
-
Decay of ompA mRNA and processing of 9S RNA are immediately affected by shifts in growth rate, but in opposite manners.
J Bacteriol. 1992 Aug;174(16):5382-90
PMID: 1644765
-
Two-stage control of an oxidative stress regulon: the Escherichia coli SoxR protein triggers redox-inducible expression of the soxS regulatory gene.
J Bacteriol. 1992 Oct;174(19):6054-60
PMID: 1400156
-
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. 1993 Feb;175(4):1026-31
PMID: 7679383
-
SoxS, an activator of superoxide stress genes in Escherichia coli. Purification and interaction with DNA.
J Biol Chem. 1994 Jul 15;269(28):18371-7
PMID: 8034583
-
A cluster of constitutive mutations affecting the C-terminus of the redox-sensitive SoxR transcriptional activator.
Nucleic Acids Res. 1994 Aug 11;22(15):2958-62
PMID: 8065907
-
Regulation of bacterial gene expression in response to oxidative stress.
Methods Enzymol. 1994;236:196-207
PMID: 7968610
-
Roles of nitric oxide in inducible resistance of Escherichia coli to activated murine macrophages.
Infect Immun. 1995 Mar;63(3):794-8
PMID: 7532626
-
Purification of a MalE-SoxS fusion protein and identification of the control sites of Escherichia coli superoxide-inducible genes.
Mol Microbiol. 1994 Nov;14(4):669-79
PMID: 7891555
-
Overproduction and physical characterization of SoxR, a [2Fe-2S] protein that governs an oxidative response regulon in Escherichia coli.
J Biol Chem. 1995 Apr 28;270(17):10323-7
PMID: 7730338
-
soxRS gene increased the level of organic solvent tolerance in Escherichia coli.
Biosci Biotechnol Biochem. 1995 Jul;59(7):1323-5
PMID: 7670195
-
Binuclear [2Fe-2S] clusters in the Escherichia coli SoxR protein and role of the metal centers in transcription.
J Biol Chem. 1995 Sep 8;270(36):20908-14
PMID: 7673113
-
Redox control of gene expression involving iron-sulfur proteins. Change of oxidation-state or assembly/disassembly of Fe-S clusters?
FEBS Lett. 1996 Mar 11;382(1-2):218-9; discussion 220-1
PMID: 8612757
-
Iron-sulphur clusters as genetic regulatory switches: the bifunctional iron regulatory protein-1.
FEBS Lett. 1996 Jun 24;389(1):40-3
PMID: 8682202
-
Glutathione-mediated destabilization in vitro of [2Fe-2S] centers in the SoxR regulatory protein.
Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9449-53
PMID: 8790350
-
Nitrosative stress: activation of the transcription factor OxyR.
Cell. 1996 Sep 6;86(5):719-29
PMID: 8797819
-
SoxR, a [2Fe-2S] transcription factor, is active only in its oxidized form.
Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10094-8
PMID: 8816757
-
Iron-sulfur clusters as biosensors of oxidants and iron.
Trends Biochem Sci. 1996 May;21(5):174-7
PMID: 8871401
-
Redox signaling and gene control in the Escherichia coli soxRS oxidative stress regulon--a review.
Gene. 1996 Nov 7;179(1):53-7
PMID: 8955629
-
The redox state of the [2Fe-2S] clusters in SoxR protein regulates its activity as a transcription factor.
J Biol Chem. 1996 Dec 27;271(52):33173-5
PMID: 8969171
-
Redox signal transduction: mutations shifting [2Fe-2S] centers of the SoxR sensor-regulator to the oxidized form.
Cell. 1997 Jan 10;88(1):121-9
PMID: 9019397
-
Regulation of the soxRS oxidative stress regulon. Reversible oxidation of the Fe-S centers of SoxR in vivo.
J Biol Chem. 1997 Feb 21;272(8):5082-6
PMID: 9030573
-
Biochemistry of oxygen toxicity.
Annu Rev Biochem. 1989;58:79-110
PMID: 2673022