Effects of Lipoprotein Overproduction on the Induction of DegP (HtrA) Involved in Quality Control in the Escherichia coli Periplasm

Miyadai, Hidenori; Tanaka-Masuda, Kimie; Matsuyama, Shin-ichi; Tokuda, Harukuni

doi:10.1074/jbc.m406390200

Cited by 59 publications

(66 citation statements)

References 32 publications

(51 reference statements)

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“…Consistent with the positive regulation of the rpoEP3 promoter by the Rcs system, its activation by overexpression of the lipoproteins is also Rcsdependent. Among the genes encoding lipoproteins identified in this work that induce the rpoEP3 transcription, yhdV, yghG, spr, and yceB were previously shown to induce the transcription of the rpoE-regulated degP promoter (58). Some of the lipoproteins are known to show significant genetic interactions with several components of LPS biosynthesis (59).…”

Section: Discussionmentioning

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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Section: Discussionmentioning

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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“…Despite the presence of DegP in wild-type cells, the three forms of Cal always seem to be present, indicating that the (610), and upon the overproduction of some outer membrane lipoproteins (459). Membrane anchoring of the lipoprotein NlpE is essential for degP induction, since the nonlipidated derivative of NlpE does not induce it (604).…”

Section: Structure-function Relationships Of Colicin Lysis Proteinsmentioning

confidence: 99%

Colicin Biology

Cascales

Buchanan

Duché

et al. 2007

Microbiol Mol Biol Rev

971

1,324

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SUMMARY Colicins are proteins produced by and toxic for some strains of Escherichia coli. They are produced by strains of E. coli carrying a colicinogenic plasmid that bears the genetic determinants for colicin synthesis, immunity, and release. Insights gained into each fundamental aspect of their biology are presented: their synthesis, which is under SOS regulation; their release into the extracellular medium, which involves the colicin lysis protein; and their uptake mechanisms and modes of action. Colicins are organized into three domains, each one involved in a different step of the process of killing sensitive bacteria. The structures of some colicins are known at the atomic level and are discussed. Colicins exert their lethal action by first binding to specific receptors, which are outer membrane proteins used for the entry of specific nutrients. They are then translocated through the outer membrane and transit through the periplasm by either the Tol or the TonB system. The components of each system are known, and their implication in the functioning of the system is described. Colicins then reach their lethal target and act either by forming a voltage-dependent channel into the inner membrane or by using their endonuclease activity on DNA, rRNA, or tRNA. The mechanisms of inhibition by specific and cognate immunity proteins are presented. Finally, the use of colicins as laboratory or biotechnological tools and their mode of evolution are discussed.

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“…T he chromosome of Escherichia coli encodes at least 90 species of lipoprotein precursors (1), which are translocated to the outer leaflet of the inner membrane by a Sec translocon and then processed to mature forms (2). Mature lipoproteins are next sorted to the outer membrane or retained in the inner membrane, depending on the lipoprotein-sorting signal located at position 2.…”

mentioning

confidence: 99%

Model of mouth-to-mouth transfer of bacterial lipoproteins through inner membrane LolC, periplasmic LolA, and outer membrane LolB

Okuda

Tokuda

2009

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

Self Cite

107

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Outer membrane-specific lipoproteins in Escherichia coli are released from the inner membrane by an ATP-binding cassette transporter, the LolCDE complex, which causes the formation of a soluble complex with a periplasmic molecular chaperone, LolA. LolA then transports lipoproteins to the outer membrane where an outer membrane receptor, LolB, incorporates lipoproteins into the outer membrane. The molecular mechanisms underlying the Loldependent lipoprotein sorting have been clarified in detail. However, it remained unclear how Lol factors interact with each other to conduct very efficient lipoprotein transfer in the periplasm where ATP is not available. To address this issue, a photo-reactive phenylalanine analogue, p-benzoyl-phenylalanine, was introduced at various positions of LolA and LolB, of which the overall structures are very similar and comprise an incomplete ␤-barrel with a hydrophobic cavity inside. Cells expressing LolA or LolB derivatives containing the above analogue were irradiated with UV for in vivo photo-cross-linking. These analyses revealed a hot area in the same region of LolA and LolB, through which LolA and LolB interact with each other. This area is located at the entrance of the hydrophobic cavity. Moreover, this area in LolA is involved in the interaction with a membrane subunit, LolC, whereas no cross-linking occurs between LolA and the other membrane subunit, LolE, or ATP-binding subunit LolD, despite the structural similarity between LolC and LolE. The hydrophobic cavities of LolA and LolB were both found to bind lipoproteins inside. These results indicate that the transfer of lipoproteins through Lol proteins occurs in a mouth-to-mouth manner.E. coli ͉ Lol proteins ͉ molecular chaperone ͉ photo-cross-link

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Effects of Lipoprotein Overproduction on the Induction of DegP (HtrA) Involved in Quality Control in the Escherichia coli Periplasm

Cited by 59 publications

References 32 publications

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

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

Colicin Biology

Model of mouth-to-mouth transfer of bacterial lipoproteins through inner membrane LolC, periplasmic LolA, and outer membrane LolB

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