Repression of photosynthesis gene expression by formation of a disulfide bond in CrtJ

Masuda, Shinji; Dong, Chen; Swem, Danielle L.; Setterdahl, Aaron T.; Knaff, David B.; Bauer, Carl E.

doi:10.1073/pnas.102013099

Cited by 82 publications

(98 citation statements)

References 21 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Despite that the cytosol of both prokaryotic and eukaryotic cells provides a highly reducing environment, which is almost untenable for disulfide bond formation (30,31), a number of cytoplasmic proteins that are regulated by reversible disulfide bond formation are known. Some examples include the transcriptional factors Yap1p in Saccharomyces cerevisiae, OxyR and the chaperone Hsp33 in E. coli, and the CtrJ and the membrane-bound kinase RegB in Rhodobacter capsulatus (31)(32)(33)(34)(35)(36). However, our in vivo and in vitro analyses indicate that disulfide bond formation in ArcB may differ from that of the other redox regulators in that it appears to respond specifically to the oxidized forms of quinones rather than to molecular oxygen or to reactive-oxygen species such as H 2 O 2 .…”

Section: Discussionmentioning

confidence: 99%

Identification of a quinone-sensitive redox switch in the ArcB sensor kinase

Malpica

Franco

Rodríguez

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

263

254

View full text Add to dashboard Cite

Escherichia coli senses and signals anoxic or low redox conditions in its growth environment by the Arc two-component system. Under anaerobic conditions, the ArcB sensor kinase autophosphorylates and transphosphorylates ArcA, a global transcriptional regulator that controls the expression of numerous operons involved in respiratory or fermentative metabolism. Under aerobic conditions, the kinase activity of ArcB is inhibited by the quinone electron carriers that act as direct negative signals. Here, we show that the molecular mechanism of kinase silencing involves the oxidation of two cytosol-located redox-active cysteine residues that participate in intermolecular disulfide bond formation, a reaction in which the quinones provide the source of oxidative power. Thus, a pivotal link in the Arc signal transduction pathway connecting the redox state of the quinone pool to the transcriptional apparatus is elucidated.T wo-component signal transduction systems are widespread in prokaryotes and play extensive roles in adaptation to environmental changes (1, 2). The Arc (anoxic redox control) two-component system is an important element in the complex transcriptional regulatory network that allows facultative anaerobic bacteria, such as Escherichia coli, to sense various respiratory growth conditions and adapt their gene expression accordingly (3). This system comprises the cytoplasmic response regulator ArcA and the transmembrane sensor kinase ArcB (4, 5). ArcA is a typical response regulator possessing an N-terminal receiver domain with a conserved Asp residue at position 54 and a C-terminal helix-turn-helix DNA binding domain. In contrast, ArcB is an unorthodox sensor kinase as manifested by its unusually elaborate architecture. As a sensor, ArcB is deviant because in contrast to typical sensor kinases that have a substantial periplasmic domain for environmental sensing, ArcB has a very short periplasmic sequence of only 16 amino acid residues delimited by two canonical transmembrane segments. Interestingly, the ArcB transmembrane domain (amino acids 22-77) does not directly participate in signal sensing but rather serves as an anchor that keeps the protein close to the source of the signal (6). As a kinase, ArcB is atypical because it contains three catalytic domains: an N-terminal transmitter domain with a conserved His-292 residue, a central receiver domain with a conserved Asp-576 residue, and a C-terminal phosphotransfer domain with a conserved His-717 residue (5, 7). Moreover, in the linker that is the region connecting the catalytic domains with the transmembrane domain, there are a putative leucine zipper (8) and a Per-Arnt-Sim (PAS) domain (9).Under reducing conditions, ArcB undergoes ATP-dependent autophosphorylation, a process shown to be enhanced by certain anaerobic metabolites such as D-lactate, acetate, and pyruvate (10, 11), and transphosphorylates ArcA via a His-292 3 Asp-576 3 His-717 3 Asp-54 phosphorelay (12, 13). Phosphorylated ArcA (ArcA-P), in turn, represses the expression of many operons invo...

show abstract

Section: Discussionmentioning

confidence: 99%

Identification of a quinone-sensitive redox switch in the ArcB sensor kinase

Malpica

Franco

Rodríguez

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

263

254

View full text Add to dashboard Cite

show abstract

“…Active FLP from Lactobacillus casei contains an intramolecular disulfide bridge (14). In CrtJ homologues, two cysteine residues are conserved (Cys249 and Cys420) that form a disulfide bridge in the active CrtJ protein characterized from Rhodobacter capsulatus (30). OxyR from E. coli is a well-studied regulator of genes involved in antioxidative response (1).…”

Section: Vol 188 2006 Regulation Of Halorespiration By Cprk1 2609mentioning

confidence: 99%

Characterization of CprK1, a CRP/FNR-Type Transcriptional Regulator of Halorespiration from Desulfitobacterium hafniense

et al. 2006

View full text Add to dashboard Cite

The recently identified CprK branch of the CRP (cyclic AMP receptor protein)-FNR (fumarate and nitrate reduction regulator) family of transcriptional regulators includes proteins that activate the transcription of genes encoding proteins involved in reductive dehalogenation of chlorinated aromatic compounds. Here we report the characterization of the CprK1 protein from Desulfitobacterium hafniense, an anaerobic low-G؉C gram-positive bacterium that is capable of reductive dechlorination of 3-chloro-4-hydroxyphenylacetic acid (Cl-OHPA). The gene encoding CprK1 was cloned and functionally overexpressed in Escherichia coli, and the protein was subsequently purified to homogeneity. To investigate the interaction of CprK1 with three of its predicted binding sequences (dehaloboxes), we performed in vitro DNA-binding assays (electrophoretic mobility shift assays) as well as in vivo promoter probe assays. Our results show that CprK1 binds its target dehaloboxes with high affinity (dissociation constant, 90 nM) in the presence of Cl-OHPA and that transcriptional initiation by CprK1 is influenced by deviations in the dehaloboxes from the consensus TTAAT----ATTAA sequence. A mutant CprK1 protein was created by a Val3Glu substitution at a conserved position in the recognition ␣-helix that gained FNR-type DNA-binding specificity, recognizing the TTGAT----ATCAA sequence (FNR box) instead of the dehaloboxes. CprK1 was subject to oxidative inactivation in vitro, most likely caused by the formation of an intermolecular disulfide bridge between Cys11 and Cys200. The possibility of redox regulation of CprK1 by a thiol-disulfide exchange reaction was investigated by using two Cys3Ser mutants. Our results indicate that a Cys11-Cys200 disulfide bridge does not appear to play a physiological role in the regulation of CprK1.Transcriptional regulators of the CRP (cyclic AMP [cAMP] receptor protein)-FNR (fumarate and nitrate reduction regulator) family play an important role in modulating the expression of numerous metabolic genes in many facultatively or strictly anaerobic bacteria. These structurally related regulators evolved to enable an efficient response to a wide range of environmental signals in organisms that are often phylogenetically distinct. In Escherichia coli, CRP is a positive regulator of catabolite repression, directly sensing elevated cAMP levels caused by glucose starvation and activating the expression of genes involved in the utilization of alternative carbon sources (26). E. coli FNR senses the changes in redox state (e.g., the decreasing availability of oxygen) through a polynuclear ironsulfur center whose presence enhances DNA binding, resulting in transcriptional activation of genes involved in anaerobic respiration (38). Apart from these archetypes of the CRP-FNR superfamily, there are several members that use other effector molecules that can stimulate or repress the expression of metabolic genes by causing structural changes in the DNA-binding domain of the corresponding regulator (18,27). Binding of carbon ...

show abstract

“…Here, the importance of intramolecular disulfide bond formation as redox-sensing mechanism is somewhat controversial. Masuda et al (23) determined the midpoint potential (E m ) for the disulfide bond formation of CrtJ to be Ϫ180 mV (at pH 7.0) by redox titration with GSH/ GSSG and also demonstrated that the intramolecular disulfide bond occurs only in aerobic and not in anaerobic cells. In contrast, however, Cho et al (4) reported that in R. sphaeroides cells, both critical cysteines of PpsR constantly exist in the reduced thiol form irrespective of the oxygen and light conditions.…”

mentioning

confidence: 99%

A Glutathione Redox Effect on Photosynthetic Membrane Expression in Rhodospirillum rubrum

Carius¹,

Henkel²,

Grammel³

2011

J Bacteriol

View full text Add to dashboard Cite

The formation of intracytoplasmic photosynthetic membranes by facultative anoxygenic photosynthetic bacteria has become a prime example for exploring redox control of gene expression in response to oxygen and light. Although a number of redox-responsive sensor proteins and transcription factors have been characterized in several species during the last several years in some detail, the overall understanding of the metabolic events that determine the cellular redox environment and initiate redox signaling is still poor. In the present study we demonstrate that in Rhodospirillum rubrum, the amount of photosynthetic membranes can be drastically elevated by external supplementation of the growth medium with the low-molecular-weight thiol glutathione. Neither the widely used reductant dithiothreitol nor oxidized glutathione caused the same response, suggesting that the effect was specific for reduced glutathione. By determination of the extracellular and intracellular glutathione levels, we correlate the GSH/GSSG redox potential to the expression level of photosynthetic membranes. Possible regulatory interactions with periplasmic, membrane, and cytosolic proteins are discussed. Furthermore, we found that R. rubrum cultures excrete substantial amounts of glutathione to the environment.It is well established that the thiol-containing tripeptide glutathione (␥-Glu-Cys-Gly [GSH]) is the most abundant redox buffer in all eukaryotic and in many prokaryotic cells and that GSH is critically important for the defense of oxidative stress which inevitably is associated with respiratory life. Various functions and mechanisms where GSH is involved in bacteria are summarized in a recent review (22). During many of these reactions, two molecules of GSH are oxidized to glutathione disulfide (GSSG), and the reduced form has to be recycled by the enzyme glutathione reductase at the expense of NADPH. A signaling role for GSH, however, is thus far not readily established. In bacteria, the reversible formation of intramolecular or intermolecular disulfide bonds of cysteines of regulatory proteins appears to be a common motif in molecular redox switches. For example, the ArcB sensor of Escherichia coli or the PpsR-and RegB-type regulators in facultative anoxygenic photosynthetic bacteria undergo reversible thiol/disulfide switches when exposed to different redox conditions in vitro (21, 32). The latter group of bacteria (Rhodospirillaceae) has contributed significantly to the recent paradigms of redox signaling and control of gene expression due to its facultative phototrophic lifestyle, which allows these bacteria to adapt their energy metabolism to the redox conditions of the environment. Under conditions of limiting oxygen, the Rhodospirillaceae induce the biosynthesis of an extensive system of pigmented intracytoplasmic membranes (ICM) which harbor photosynthetic reaction centers and light-harvesting complexes. The major environmental factor that determines the amount of ICM is the availability of oxygen, since aerobic growth conditio...

show abstract

Repression of photosynthesis gene expression by formation of a disulfide bond in CrtJ

Cited by 82 publications

References 21 publications

Identification of a quinone-sensitive redox switch in the ArcB sensor kinase

Identification of a quinone-sensitive redox switch in the ArcB sensor kinase

Characterization of CprK1, a CRP/FNR-Type Transcriptional Regulator of Halorespiration from Desulfitobacterium hafniense

A Glutathione Redox Effect on Photosynthetic Membrane Expression in Rhodospirillum rubrum

Contact Info

Product

Resources

About