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Chapter 3 : Assembly of Integral Membrane Proteins from the Periplasm into the Outer Membrane

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Abstract:

Integral membrane proteins facilitate transport, for example, of nutrients, across a hydrophobic barrier. This chapter summarizes the current knowledge about the transport of outer membrane proteins (OMPs) through the periplasm and about their assembly into membranes. How insertion and folding of OMPs into the outer membrane (OM) takes place is largely unknown, and the chapter gives an overview about our current knowledge on the insertion and folding of OMPs from the periplasm into the OM. Therefore, some of the structures and properties of OMPs are described in the chapter, followed by an overview of the currently known periplasmic folding factors of OMPs. The chapter focuses on membrane insertion and assembly of the porins that form single-chain transmembrane β-barrels. It is now clear that periplasmic chaperones, such as Skp and SurA, help to keep OMPs unfolded in the periplasm and prevent their aggregation without requiring ATP as an energy source. The identification of the integral OMP YaeT and outer membrane lipoproteins as factors involved in targeting and/or insertion of OMPs into the OM on one side and the spontaneous assembly of OMPs into lipid bilayers in vitro on the other side raises several interesting questions. Furthermore, the accumulation of misfolded OMPs in the periplasm upon deletion of yaeT (omp85) suggests that the properties of the OM lipid bilayer differ from the properties of the phospholipid bilayers into which OMPs successfully fold in vitro.

Citation: Kleinschmidt J. 2007. Assembly of Integral Membrane Proteins from the Periplasm into the Outer Membrane, p 30-66. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch3

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Image of FIGURE 1
FIGURE 1

Export of integral membrane proteins through the periplasm to the OM. The OMP traverses the inner membrane through the SecY/G/E translocon in an unfolded form. A leader peptidase (SPase), anchored to the inner membrane, cleaves the signal sequence in the periplasm. The OMP then traverses the periplasm bound to a periplasmic chaperone. Among the periplasmic proteins that were either reported or likely to bind unfolded OMPs are Skp, SurA, DegP, and FkpA. All of the currently discovered soluble periplasmic folding factors are bi-functional. Skp binds unfolded OMPs and LPS; SurA and FkpA have chaperone function and—independent of the chaperone function—PPIase activity. DegP is a protease and a chaperone. From the periplasm, OMPs are targeted to or assembled into the outer membrane by membrane-bound proteins, namely YaeT (Omp85) and the lipopro-teins YfiO, YfgL, and NlpB. This process has not been investigated yet. Misfolded proteins in the periplasm are degraded by proteases such as DegP and DegS. DegS is a sensor for misfolded OMPs and consequently cleaves the cytoplasmic RseA in the periplasm. In a second cleavage step, the cleaved RseA is degraded further by RseP (YaeL), leading to the release of σ (RpoE), which results in an elevated expression of periplasmic chaperones, isomerases, and proteases, and of OM-associated folding factors. See the text for further details.

Citation: Kleinschmidt J. 2007. Assembly of Integral Membrane Proteins from the Periplasm into the Outer Membrane, p 30-66. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch3
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Image of FIGURE 2
FIGURE 2

Folding of OmpA into lipid bilayers requires both Skp and LPS (adapted from ). Data shown correspond to folding experiments of urea-denatured OmpA into lipid bilayers, which were added 30 min after dilution of the denaturant urea in the absence of Skp and LPS (○), in the presence of Skp (♦), in the presence of LPS (▲), and in the presence of both Skp and LPS (●). The folding kinetics was fastest and folding yields were highest when both Skp and LPS were present. Folding was inhibited when either Skp or LPS was absent. The folding kinetics in the presence of Skp and LPS also compares favorably with the folding kinetics from the urea-denatured state in the absence of Skp and LPS, indicating that OmpA is insertion competent in vivo, in the absence of urea, when in complex with Skp and LPS. The data shown in also indicated that OmpA did not develop native structure in complex with Skp and LPS, but only in the presence of lipid bilayers.

Citation: Kleinschmidt J. 2007. Assembly of Integral Membrane Proteins from the Periplasm into the Outer Membrane, p 30-66. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch3
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Image of FIGURE 3
FIGURE 3

A model of the Skp/LPS-assisted folding pathway of the β-barrel protein OmpA of the OM of is depicted. After translocation across the cytoplasmic membrane by the SecY/E/G system in unfolded form (U), OmpA binds three molecules of the trimeric Skp, which is a periplasmic chaperone and keeps OmpA soluble in an unfolded state (USkp). The complex of unfolded OmpA and Skp interacts with LPS molecules to form a folding-competent intermediate of OmpA (FCSkpLPS). In the final step, folding-competent OmpA inserts and folds into the lipid bilayer. ( .)

Citation: Kleinschmidt J. 2007. Assembly of Integral Membrane Proteins from the Periplasm into the Outer Membrane, p 30-66. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch3
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Image of FIGURE 4
FIGURE 4

(A) Time courses of the movement of Trp-7 toward the bilayer center at 2, 28, and 40°C. Distances were obtained from curve fits to fluorescence-quenching profiles as described in the text. Data points represented by filled circles were the fitted quenching-profile minima, open circles denote extrapolated distances from the observed quenching profiles. The solid lines are fits of single- or double-exponential functions to the data. (B) Time courses of the movement of Trp-143 toward the bi-layer center at 2 and 28°C and from the bi-layer center at 30 and 40°C. At 2°C, the distances of Trp-143 could only be obtained by extrapolation (open circles). The solid lines are fits of the data to single- or double-exponential functions. ( .)

Citation: Kleinschmidt J. 2007. Assembly of Integral Membrane Proteins from the Periplasm into the Outer Membrane, p 30-66. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch3
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Tables

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TABLE 1

Examples of outer membrane proteins of known high-resolution structure

Citation: Kleinschmidt J. 2007. Assembly of Integral Membrane Proteins from the Periplasm into the Outer Membrane, p 30-66. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch3
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TABLE 2

Proteins suggested to be involved in assembly of outer membrane proteins

Citation: Kleinschmidt J. 2007. Assembly of Integral Membrane Proteins from the Periplasm into the Outer Membrane, p 30-66. In Ehrmann M (ed), The Periplasm. ASM Press, Washington, DC. doi: 10.1128/9781555815806.ch3

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