Regulated intramembrane proteolysis of FtsL protein and the control of cell division in <i>Bacillus subtilis</i>

Bramkamp, Marc; Weston, Louise; Daniel, Richard A.; Errington, Jeff

doi:10.1111/j.1365-2958.2006.05402.x

Cited by 67 publications

(91 citation statements)

References 50 publications

(84 reference statements)

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“…Both enzymes have been implicated in the cellular response to the stresses caused by high-level production of secretory proteins or heat, but whether this involves a sheddase activity of HtrA or HtrB is not known (30,62,187). Interestingly, the cellular levels of HtrA and HtrB seem to be controlled by RasP, the RseP homologue of B. subtilis, suggesting that they are subject to intramembrane cleavage (19,199). This would explain why fragments of HtrA and HtrB are detectable in the growth medium of B. subtilis.…”

Section: Degsmentioning

confidence: 99%

“…In the enteric pathogen Vibrio cholerae, the causative agent of cholera, DegS is implicated in sigma E-mediated resistance to membrane-acting, host gut-derived antimicrobial peptides (103). In B. subtilis, the DegS homologue proteases HtrA and HtrB are both membrane bound by an N-terminal membrane anchor like E. coli DegS (7,19,62,198,199). Both enzymes have been implicated in the cellular response to the stresses caused by high-level production of secretory proteins or heat, but whether this involves a sheddase activity of HtrA or HtrB is not known (30,62,187).…”

Section: Degsmentioning

confidence: 99%

“…RseP and certain signal peptide hydrolases are highly intriguing enzymes because they catalyze hydrolytic reactions within the membrane plane. Moreover, in the Gram-positive bacterium Bacillus subtilis, the S2P RasP (YluC) plays an important role in the regulation of cell division (19,199). RasP is responsible for the rapid turnover of FtsL, a small bitopic membrane protein, which is an essential part of the cell division machinery.…”

mentioning

confidence: 99%

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Membrane Proteases in the Bacterial Protein Secretion and Quality Control Pathway

Dalbey

Wang

Dijl

2012

Microbiol Mol Biol Rev

128

129

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SUMMARY Proteolytic cleavage of proteins that are permanently or transiently associated with the cytoplasmic membrane is crucially important for a wide range of essential processes in bacteria. This applies in particular to the secretion of proteins and to membrane protein quality control. Major progress has been made in elucidating the structure-function relationships of many of the responsible membrane proteases, including signal peptidases, signal peptide hydrolases, FtsH, the rhomboid protease GlpG, and the site 1 protease DegS. These enzymes employ very different mechanisms to cleave substrates at the cytoplasmic and extracytoplasmic membrane surfaces or within the plane of the membrane. This review highlights the different ways that bacterial membrane proteases degrade their substrates, with special emphasis on catalytic mechanisms and substrate delivery to the respective active sites.

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Section: Degsmentioning

confidence: 99%

Section: Degsmentioning

confidence: 99%

mentioning

confidence: 99%

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Membrane Proteases in the Bacterial Protein Secretion and Quality Control Pathway

Dalbey

Wang

Dijl

2012

Microbiol Mol Biol Rev

128

129

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“…They are also involved in the endoplasmic reticulum stress responses (6 -8). Recent studies revealed that the prokaryotic S2P homologs function in membranebased events such as stress response (9), sporulation (10), cell division (11), and cell differentiation (12). In Escherichia coli, the S2P homolog RseP is an essential player in the transmembrane signaling involved in the E pathway of extracytoplasmic stress responses (13)(14)(15).…”

Section: I-clipsmentioning

confidence: 99%

Substrate Recognition and Binding by RseP, an Escherichia coli Intramembrane Protease

Koide

Ito

Akiyama

2008

Journal of Biological Chemistry

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Escherichia coli RseP belongs to the S2P family of intramembrane cleaving proteases. RseP catalyzes proteolytic cleavage of the membrane-bound anti-E protein RseA as an essential step in transmembrane signal transduction in the E extracytoplasmic stress response pathway. RseP cleaves transmembrane segments of membrane proteins, but the molecular mechanisms of its substrate recognition and proteolytic action remain largely unknown. Here we analyzed interaction between RseP and substrate membrane proteins. Co-immunoprecipitation assays showed that helix-destabilizing residues in a substrate transmembrane segment, which were previously shown to be required for efficient proteolysis of the substrate by RseP, stabilize the substrate-RseP interaction. Substitutions of certain amino acid residues, including those evolutionarily conserved, in the third transmembrane region (TM3) of RseP weakened the RseP-substrate interaction. Specific combinations of Cys substitutions in RseP TM3 and in the RseA transmembrane segment led to the formation of disulfide bonds upon oxidation, suggesting that TM3 of RseP directly binds the substrate. These results provide insights into the mechanism of membrane protein proteolysis by RseP. I-CLiPs2 are a class of membrane proteases that are widely distributed from bacteria to higher eukaryotes and play pivotal roles in a variety of biological processes (1, 2). These proteases generally catalyze cleavage of target membrane proteins within or around their transmembrane segments, leading to a release of the soluble domains into the secretory compartments and/or cytoplasm. The soluble domains that are liberated from the membrane act as biologically active molecules such as transcription factors and growth factors. I-CLiPs can be classified into three groups based on their catalytic residues: the S2P (metalloprotease) family, the rhomboid (serine protease) family, and the ␥-secretase and signal peptide peptidase (aspartyl protease) family (1, 2).The S2P proteases regulate sterol and lipid metabolism in eukaryotic cells (3-5). They are also involved in the endoplasmic reticulum stress responses (6 -8). Recent studies revealed that the prokaryotic S2P homologs function in membranebased events such as stress response (9), sporulation (10), cell division (11), and cell differentiation (12). In Escherichia coli, the S2P homolog RseP is an essential player in the transmembrane signaling involved in the E pathway of extracytoplasmic stress responses (13-15).E is a sigma factor dedicated to the transcription of genes that encode proteases, chaperones, and folding catalysts in the cell envelop, and it is activated by a cascade of intracellular proteolysis of its inhibitor (16,17). Under resting conditions, E is kept inactive through its tight association with the N-terminal cytoplasmic domain of the membrane-bound anti-E protein, RseA, which has a type II (N IN -C OUT ) topology. When cells are exposed to extracytoplasmic stresses, stress signals such as unassembled outer membrane proteins directly activ...

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“…Recently, it has been demonstrated that FtsL, a transmembrane protein of the B. subtilis cell division machinery, is attacked by RasP (Bramkamp et al, 2006). Therefore, in analogy to the GFP-RsiW reporter, a GFP-FtsL fusion was constructed and expressed in different genetic backgrounds.…”

Section: Mutations In B Subtilis Ecsab Prevent Induction Of S W -Conmentioning

confidence: 99%

The Bacillus subtilis ABC transporter EcsAB influences intramembrane proteolysis through RasP

et al. 2008

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The Bacillus subtilis s W regulon is induced by different stresses that most probably affect integrity of the cell envelope. The activity of the extracytoplasmic function (ECF) sigma factor s W is modulated by the transmembrane anti-sigma factor RsiW, which undergoes stress-induced degradation in a process known as regulated intramembrane proteolysis, finally resulting in the release of s W and the transcription of s W -controlled genes. Mutations in the ecsA gene, which encodes an ATP binding cassette (ABC) of an ABC transporter of unknown function, block site-2 proteolysis of RsiW by the intramembrane cleaving protease RasP (YluC). In addition, degradation of the cell division protein FtsL, which represents a second RasP substrate, is blocked in an ecsA-negative strain. The defect in s W induction of an ecsA-knockout strain could be partly suppressed by overproducing RasP. A B. subtilis rasP-knockout strain displayed the same pleiotropic phenotype as an ecsA knockout, namely defects in processing a-amylase, in competence development, and in formation of multicellular structures known as biofilms. INTRODUCTIONGenes of Bacillus subtilis controlled by the alternative extracytoplasmic function (ECF) sigma factor s W constitute an antibiosis regulon (Helmann, 2002(Helmann, , 2006 that responds to a variety of envelope stresses such as certain antibiotics (Cao et al., 2002) and antimicrobial peptides (Pietiäinen et al., 2005;Butcher & Helmann, 2006), and also alkaline shock and phage infection . Its activity is modulated by RsiW, a transmembrane anti-sigma factor that sequesters and inactivates s W . Upon a stress signal, RsiW is degraded by the mechanism of regulated intramembrane proteolysis (RIP). In a concerted action, at least three proteases in three different compartments of the cell degrade the RsiW anti-sigma factor in a sequential manner, finally resulting in the release of s W and the transcription of s Wcontrolled genes. The first protease that has been identified to be involved in that process is RasP (regulating anti-sigma factor protease; formerly YluC). RasP belongs to the group of zinc-dependent intramembrane cleaving proteases (iClips) and cleaves RsiW in its transmembrane domain after the extracytoplasmic part of the anti-sigma factor has been removed by a site-1 protease (Schöbel et al., 2004). The site-2 degradation step catalysed by RasP uncovers a cryptic proteolytic tag that ensures further degradation of the RsiW remnant by cytoplasmic proteases, mainly ClpXP (Zellmeier et al., 2006). These two steps are related to RIP of the s E anti-sigma factor RseA of Escherichia coli (Ades, 2004;Alba & Gross, 2004). RasP is an orthologue of E. coli RseP, and the concept of a cryptic proteolytic tag recognized by ClpXP was first described for that system (Akiyama et al., 2004;Flynn et al., 2004). However, there is a marked difference in the site-1 proteolytic step, because no dependency on B. subtilis Deg (Htr) proteases was found and the inducing stress is apparently different. The probable site-1 prot...

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Regulated intramembrane proteolysis of FtsL protein and the control of cell division in Bacillus subtilis

Cited by 67 publications

References 50 publications

Membrane Proteases in the Bacterial Protein Secretion and Quality Control Pathway

Membrane Proteases in the Bacterial Protein Secretion and Quality Control Pathway

Substrate Recognition and Binding by RseP, an Escherichia coli Intramembrane Protease

The Bacillus subtilis ABC transporter EcsAB influences intramembrane proteolysis through RasP

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