Contribution of proteomics toward solving the fascinating mysteries of the biogenesis of the envelope of <i>Escherichia coli</i>

Leverrier, Pauline; Vertommen, Didier; Collet, Jean-François

doi:10.1002/pmic.200900461

Cited by 21 publications

(18 citation statements)

References 127 publications

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“…Integral OM proteins typically span the OM as β-sheets folded in a barrel conformation. Their folding and insertion into the OM is catalyzed by the Bam complex (16)(17)(18)(19)(20)(21) in conjunction with periplasmic chaperones (22). However, because of the extra complexity in their biogenesis, it remains unclear how OM proteins are oxidized.…”

mentioning

confidence: 99%

Nonconsecutive disulfide bond formation in an essential integral outer membrane protein

Ruiz

Chng

Hiniker

et al. 2010

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

102

174

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The Gram-negative bacterial envelope is bounded by two membranes. Disulfide bond formation and isomerization in this oxidizing environment are catalyzed by DsbA and DsbC, respectively. It remains unknown when and how the Dsb proteins participate in the biogenesis of outer membrane proteins, which are transported across the cell envelope after their synthesis. The Escherichia coli protein LptD is an integral outer membrane protein that forms an essential complex with the lipoprotein LptE. We show that oxidation of LptD is not required for the formation of the LptD/E complex but it is essential for function. Remarkably, none of the cysteines in LptD are essential because either of two nonconsecutive disulfide bonds suffices for function. Oxidation of LptD, which is efficiently catalyzed by DsbA, does not involve the isomerase DsbC, but it requires LptE. Thus, oxidation is completed only after LptD interacts with LptE, an interaction that occurs at the outer membrane and seems necessary for LptD folding.β-barrel protein | lipoprotein | protein folding

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mentioning

confidence: 99%

Nonconsecutive disulfide bond formation in an essential integral outer membrane protein

Ruiz

Chng

Hiniker

et al. 2010

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

102

174

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“…Recently, Zhao and coworkers have shown that unfolded OMPs interact with SurA and Skp with much faster kinetics than with DegP, suggesting that SurA and Skp function at the early stage of OMP biogenesis while DegP acts subsequently (5). Depletion of SurA leads to drastically decreased density of OMPs in the outer membrane, but deletion of Skp or DegP does not have a similar effect (6)(7)(8). Two explanations have been proposed for the drastic change of OMP density in the absence of SurA.…”

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confidence: 99%

“…They share redundant chaperone activities. SurA is the primary chaperone that facilitates membrane insertion of most OMPs, while Skp and DegP scavenge OMP folding intermediates that fall off the SurA pathway and either break them down or prepare them for membrane insertion (5)(6)(7). Recently, Zhao and coworkers have shown that unfolded OMPs interact with SurA and Skp with much faster kinetics than with DegP, suggesting that SurA and Skp function at the early stage of OMP biogenesis while DegP acts subsequently (5).…”

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confidence: 99%

“…Two explanations have been proposed for the drastic change of OMP density in the absence of SurA. First, in a SurA-deficient strain, E transcription factor is induced, which subsequently downregulates the mRNA level of several OMPs and leads to a decrease of OMP synthesis rate (6,(8)(9)(10). Second, without the SurA chaperone activity, nascent OMPs in the periplasm aggregate and fail to reach the outer membrane (7,11).…”

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confidence: 99%

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Insights into the Function and Structural Flexibility of the Periplasmic Molecular Chaperone SurA

Zhong

Ferrell

et al. 2012

Journal of Bacteriology

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SurA is the primary periplasmic molecular chaperone that facilitates the folding and assembling of outer membrane proteins (OMPs) in Gram-negative bacteria. Deletion of the surA gene in Escherichia coli leads to a decrease in outer membrane density and an increase in bacterial drug susceptibility. Here, we conducted mutational studies on SurA to identify residues that are critical for function. One mutant, SurA V37G , significantly reduced the activity of SurA. Further characterization indicated that SurA V37G was structurally similar to, but less stable than, the wild-type protein. The loss of activity in SurA V37G could be restored through the introduction of a pair of Cys residues and the subsequent formation of a disulfide bond. Inspired by this success, we created three additional SurA constructs, each containing a disulfide bond at different regions of the protein between two rigid secondary structural elements. The formation of disulfide bond in these mutants has no observable detrimental effect on protein activity, indicating that SurA does not undergo large-scale conformational change while performing its function.

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“…In Escherichia coli and related enteric bacteria, five periplasmic PPIases have been described: SurA, PpiD, PpiA, FkpA, and FklB (14,15,16). Among these proteins, SurA is particularly well studied.…”

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confidence: 99%

Demarcating SurA Activities Required for Outer Membrane Targeting of Yersinia pseudotuberculosis Adhesins

Obi

Francis

2013

Infect Immun

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SurA is a periplasmic protein folding factor involved in chaperoning and trafficking of outer membrane proteins across the Gram-negative bacterial periplasm. In addition, SurA also possesses peptidyl-prolyl cis/trans isomerase activity. We have previously reported that in enteropathogenic Yersinia pseudotuberculosis, SurA is needed for bacterial virulence and envelope integrity. In this study, we investigated the role of SurA in the assembly of important Yersinia adhesins. Using genetic mutation, biochemical characterization, and an in vitro-based bacterial host cell association assay, we confirmed that surface localization of the invasin adhesin is dependent on SurA. As a surA deletion also has some impact on the levels of individual components of the BAM complex in the Yersinia outer membrane, abolished invasin surface assembly could reflect both a direct loss of SurA-dependent periplasmic targeting and a potentially compromised BAM complex assembly platform in the outer membrane. To various degrees, the assembly of two other adhesins, Ail and the pH 6 antigen fibrillum PsaA, also depends on SurA. Consequently, loss of SurA leads to a dramatic reduction in Yersinia attachment to eukaryotic host cells. Genetic complementation of surA deletion mutants indicated a prominent role for SurA chaperone function in outer membrane protein assembly. Significantly, the N terminus of SurA contributed most of this SurA chaperone function. Despite a dominant chaperoning role, it was also evident that SurA isomerization activity did make a modest contribution to this assembly process.

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Contribution of proteomics toward solving the fascinating mysteries of the biogenesis of the envelope of Escherichia coli

Cited by 21 publications

References 127 publications

Nonconsecutive disulfide bond formation in an essential integral outer membrane protein

Nonconsecutive disulfide bond formation in an essential integral outer membrane protein

Insights into the Function and Structural Flexibility of the Periplasmic Molecular Chaperone SurA

Demarcating SurA Activities Required for Outer Membrane Targeting of Yersinia pseudotuberculosis Adhesins

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