The σE‐mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of σE

Peñas, Alejandro De Las; Connolly, Lynn; Gross, Carol A.

doi:10.1046/j.1365-2958.1997.3611718.x

Cited by 300 publications

(323 citation statements)

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“…5B) (Raivio and Silhavy, 2001;Alba and Gross, 2004). In that pathway, RseA is an anti-sigma factor with a central transmembrane segment whose N-terminal, cytoplasmic domain sequesters s E and represses its essential activity (De Las Penas et al, 1997;Missiakas et al, 1997;Ades et al, 1999;Campbell et al, 2003). When periplasmic protease…”

Section: Dicmentioning

confidence: 99%

A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant

Chen

Viollier

Shapiro

2005

Molecular Microbiology

123

143

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SummaryCaulobacter crescentus assembles many of its cellular machines at distinct times and locations during the cell cycle. PodJ provides the spatial cues for the biogenesis of several polar organelles, including the pili, adhesive holdfast and chemotactic apparatus, by recruiting structural and regulatory proteins, such as CpaE and PleC, to a specific cell pole. PodJ is a protein with a single transmembrane domain that exists in two forms, full-length (PodJ L ) and truncated (PodJ S ), each appearing during a specific time period of the cell cycle to control different aspects of polar organelle development. PodJ L is synthesized in the early predivisional cell and is later proteolytically converted to PodJ S . During the swarmer-to-stalked transition, PodJ S must be degraded to preserve asymmetry in the next cell cycle. We found that MmpA facilitates the degradation of PodJ S . MmpA belongs to the site-2 protease (S2P) family of membraneembedded zinc metalloproteases, which includes SpoIVFB and YluC of Bacillus subtilis and YaeL of Escherichia coli . MmpA appears to cleave within or near the transmembrane segment of PodJ S , releasing it into the cytoplasm for complete proteolysis. While PodJ S has a specific temporal and spatial address, MmpA is present throughout the cell cycle; furthermore, periplasmic fusion to mRFP1 suggested that MmpA is uniformly distributed around the cell. We also determined that mmpA and yaeL can complement each other in C. crescentus and E. coli , indicating functional conservation. Thus, the sequential degradation of PodJ appears to involve regulated intramembrane proteolysis (Rip) by MmpA.

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Section: Dicmentioning

confidence: 99%

A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant

Chen

Viollier

Shapiro

2005

Molecular Microbiology

123

143

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“…This fragment is easy to purify because it is stable in E. coli. It is also sufficient for antiactivity both in vivo and in vitro (De Las Penas et al 1997b;Missiakas et al 1997;Campbell et al 2003). We used fluorescence anisotropy to measure the dissociation of rhodamine-labeled RseA 1-100 from E .…”

Section: The Cytoplasmic Domain Of Rsea Binds Very Tightly To Ementioning

confidence: 99%

“…RseA, a membrane-spanning anti-factor, inhibits E activity. The cytoplasmic domain of RseA (RseA 1-108 ) binds to E and its periplasmic domain binds to RseB (De Las Penas et al 1997b;Missiakas et al 1997 …”

mentioning

confidence: 99%

Design principles of the proteolytic cascade governing the σ^E-mediated envelope stress response in Escherichia coli: keys to graded, buffered, and rapid signal transduction

Chaba¹,

Grigorova²,

Flynn³

et al. 2007

Genes Dev.

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104

119

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Proteolytic cascades often transduce signals between cellular compartments, but the features of these cascades that permit efficient conversion of a biological signal into a transcriptional output are not well elucidated. E mediates an envelope stress response in Escherichia coli, and its activity is controlled by regulated degradation of RseA, a membrane-spanning anti-factor. Examination of the individual steps in this protease cascade reveals that the initial, signal-sensing cleavage step is rate-limiting; that multiple ATP-dependent proteases degrade the cytoplasmic fragment of RseA and that dissociation of E from RseA is so slow that most free E must be generated by the active degradation of RseA. As a consequence, the degradation rate of RseA is set by the amount of inducing signal, and insulated from the "load" on and activity of the cytoplasmic proteases. Additionally, changes in RseA degradation rate are rapidly reflected in altered E activity. These design features are attractive as general components of signal transduction pathways governed by unstable negative regulators. Proteolytic cascades are widely used to transduce signals across membranes to enable cells to respond to environmental stress and coordinate processes in different cellular compartments. However, the molecular properties of these cascades that facilitate the desired outputs have rarely been examined. In this work, we examine the individual steps in the protease cascade governing the activity of the E -mediated envelope stress response in Escherichia coli to determine the construction features of this cascade that facilitate faithful transmission of signal and a rapid output.E directs RNA polymerase to transcribe genes encoding proteins that ensure the synthesis, assembly, and homeostasis of outer membrane porins and lipopolysaccharide, the two major components of the unique outer membrane of Gram-negative bacteria (Dartigalongue et al. 2001;Rezuchova et al. 2003;Rhodius et al. 2006). Envelope integrity is required under all growth conditions, and E is an essential transcription factor (De Las Penas et al. 1997a). Perturbations in the integrity and protein-folding state of the envelope caused by temperature upshift, chaperone depletion, or accumulation of unassembled porins increase E activity; conversely, temperature downshift and/or depletion of porins decrease E activity (Mecsas et al. 1993;Hiratsu et al. 1995;Raina et al. 1995;Rouviere et al. 1995;Missiakas et al. 1996;Rouviere and Gross 1996;Ades et al. 2003).The components of the signal transduction system that control E activity are shown in Figure 1. RseA, a membrane-spanning anti-factor, inhibits E activity. The cytoplasmic domain of RseA (RseA 1-108 ) binds to E and its periplasmic domain binds to RseB (De Las Penas et al. 1997b;Missiakas et al. 1997

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“…1) (3,(11)(12)(13)(14)(15)(16). There is an intricate link between the LPS assembly, its non-stoichiometric modifications, and the RpoE-mediated control exerted via its regulon members (17,18).…”

mentioning

confidence: 99%

Multiple Transcriptional Factors Regulate Transcription of the rpoE Gene in Escherichia coli under Different Growth Conditions and When the Lipopolysaccharide Biosynthesis Is Defective

Klein

Stupak

Biernacka

et al. 2016

Journal of Biological Chemistry

107

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The RpoE factor is essential for the viability of Escherichia coli. RpoE regulates extracytoplasmic functions including lipopolysaccharide (LPS) translocation and some of its non-stoichiometric modifications. Transcription of the rpoE gene is positively autoregulated by E E and by unknown mechanisms that control the expression of its distally located promoter(s). Mapping of 5 ends of rpoE mRNA identified five new transcriptional initiation sites (P1 to P5) located distal to E E -regulated promoter. These promoters are activated in response to unique signals. Of these P2, P3, and P4 defined major promoters, recognized by RpoN, RpoD, and RpoS factors, respectively. Isolation of trans-acting factors, in vitro transcriptional and gel retardation assays revealed that the RpoN-recognized P2 promoter is positively regulated by a QseE/F two-component system and NtrC activator, whereas the RpoD-regulated P3 promoter is positively regulated by a Rcs system in response to defects in LPS core biosynthesis, overproduction of certain lipoproteins, and the global regulator CRP. Strains synthesizing Kdo 2 -LA LPS caused up to 7-fold increase in the rpoEP3 activity, which was abrogated in ⌬(waaC rcsB). Overexpression of a novel 73-nucleotide sRNA rirA (RfaH interacting RNA) generated by the processing of 5 UTR of the waaQ mRNA induces the rpoEP3 promoter activity concomitant with a decrease in LPS content and defects in the O-antigen incorporation. In the presence of RNA polymerase, RirA binds LPS regulator RfaH known to prevent premature transcriptional termination of waaQ and rfb operons. RirA in excess could titrate out RfaH causing LPS defects and the activation of rpoE transcription.The cell envelope of Gram-negative bacteria, including Escherichia coli, contains two distinct membranes, an inner (IM) 3 and an outer (OM) membrane separated by the periplasm, a hydrophilic compartment that includes a layer of peptidoglycan. The OM is an asymmetric lipid bilayer with phospholipids forming the inner leaflet and LPS forming the outer leaflet. LPSs are highly heterogeneous in composition. However, they share a common architecture composed of a membrane-anchored phosphorylated and acylated ␤(136)-linked GlcN disaccharide, termed lipid A, to which a carbohydrate moiety of varying size is attached (1, 2).During the analyses of signals that induce the RpoE-dependent extracytoplasmic stress response, we showed that strains synthesizing heptoseless LPS due to the absence of either GmhD (RfaD/HtrM) or WaaC exhibited a constitutive induction of RpoE (3-6). Such strains also display constitutive synthesis of exopolysaccharide that is regulated by the Rcs twocomponent system (5,7,8). Subsequently, we showed that strains synthesizing the minimal LPS structure composed of either Kdo 2 -lipid IV A or only free lipid IV A exhibited hyperelevated levels of the RpoE activity (6). The activity of RpoE is highly induced when the LPS assembly is severely compromised or when there is an imbalance between LPS and phospholipids (9). Lack of many LPS co...

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The σ^E‐mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of σ^E

Cited by 300 publications

References 44 publications

A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant

A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant

Design principles of the proteolytic cascade governing the σ^E-mediated envelope stress response in Escherichia coli: keys to graded, buffered, and rapid signal transduction

Multiple Transcriptional Factors Regulate Transcription of the rpoE Gene in Escherichia coli under Different Growth Conditions and When the Lipopolysaccharide Biosynthesis Is Defective

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The σE‐mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of σE

Cited by 300 publications

References 44 publications

A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant

A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant

Design principles of the proteolytic cascade governing the σE-mediated envelope stress response in Escherichia coli: keys to graded, buffered, and rapid signal transduction

Multiple Transcriptional Factors Regulate Transcription of the rpoE Gene in Escherichia coli under Different Growth Conditions and When the Lipopolysaccharide Biosynthesis Is Defective

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The σ^E‐mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of σ^E

Design principles of the proteolytic cascade governing the σ^E-mediated envelope stress response in Escherichia coli: keys to graded, buffered, and rapid signal transduction