Peptidoglycan-associated Lipoprotein-TolB Interaction

Bouveret, Emmanuelle; Derouiche, Rahmona; Rigal, Alain; Lloubès, Roland; Lazdunski, Claude; Bénédetti, Hélène

doi:10.1074/jbc.270.19.11071

Cited by 133 publications

(96 citation statements)

References 47 publications

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“…In vivo crosslinking has established that TolB and Pal form a complex at the OM in the bacterial periplasm (29), where Pal is localized by virtue of its N-terminal lipoyl tether. Using a suppressor screen, Lazzaroni and coworkers (30) identified a number of residues in TolB that potentially comprise a Pal binding site.…”

Section: Resultsmentioning

confidence: 99%

Competitive recruitment of the periplasmic translocation portal TolB by a natively disordered domain of colicin E9

Loftus

Walker

Mate

et al. 2006

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

155

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The natively disordered N-terminal 83-aa translocation (T) domain of E group nuclease colicins recruits OmpF to a colicin-receptor complex in the outer membrane (OM) as well as TolB in the periplasm of Escherichia coli, the latter triggering translocation of the toxin across the OM. We have identified the 16-residue TolB binding epitope in the natively disordered T-domain of the nuclease colicin E9 (ColE9) and solved the crystal structure of the complex. ColE9 folds into a distorted hairpin within a canyon of the six-bladed ␤-propeller of TolB, using two tryptophans to bolt the toxin to the canyon floor and numerous intramolecular hydrogen bonds to stabilize the bound conformation. This mode of binding enables colicin side chains to hydrogen-bond TolB residues in and around the channel that runs through the ␤-propeller and that constitutes the binding site of peptidoglycan-associated lipoprotein (Pal). Pal is a globular binding partner of TolB, and their association is known to be important for OM integrity. The structure is therefore consistent with translocation models wherein the colicin disrupts the TolB-Pal complex causing local instability of the OM as a prelude to toxin import. Intriguingly, Ca 2؉ ions, which bind within the ␤-propeller channel and switch the surface electrostatics from negative to positive, are needed for the negatively charged T-domain to bind TolB with an affinity equivalent to that of Pal and competitively displace it. Our study demonstrates that natively disordered proteins can compete with globular proteins for binding to folded scaffolds but that this can require cofactors such as metal ions to offset unfavorable interactions.native disorder ͉ thermodynamics ͉ toxin

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Section: Resultsmentioning

confidence: 99%

Competitive recruitment of the periplasmic translocation portal TolB by a natively disordered domain of colicin E9

Loftus

Walker

Mate

et al. 2006

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

155

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“…TolB and peptidoglycan compete for the same binding site on Pal, which happens to be on the opposite end (structurally) of the N-terminal lipid anchor (Abergel et al, 1999;Bouveret et al, 1995;Cascales & Lloubès, 2004;Parsons et al, 2006), thus making the interactions of Pal with TolB and peptidoglycan mutually exclusive. These interactions all point to the necessity for Pal to be localized in the periplasm of the cell.…”

Section: Discussionmentioning

confidence: 99%

“…Since its discovery in 1981 (Mizuno, 1981), Pal has been well studied (Godlewska et al, 2009); mostly notably for its interactions with other bacterial proteins (Bouveret et al, 1995;Cascales et al, 2000Cascales et al, , 2002Clavel et al, 1998), its proposed role in maintaining the integrity of the outer membrane of E. coli (Cascales et al, 2002) and its other physiological interaction with the peptidoglycan layer (Lazzaroni & Portalier, 1992). TolB and peptidoglycan compete for the same binding site on Pal, which happens to be on the opposite end (structurally) of the N-terminal lipid anchor (Abergel et al, 1999;Bouveret et al, 1995;Cascales & Lloubès, 2004;Parsons et al, 2006), thus making the interactions of Pal with TolB and peptidoglycan mutually exclusive.…”

Section: Discussionmentioning

confidence: 99%

“…For example, in the Tol-Pal complex, a combination of lipoproteins, integral membrane proteins and periplasmic proteins interact with each other and the peptidoglycan, forming a web of covalent and noncovalent contacts between the outer and inner membranes (Yeh et al, 2010). The outer membrane peptidoglycan associated lipoprotein (Pal; tethered to the outer membrane via its Nterminal lipid moiety) is one of the key components in the Tol-Pal complex (Godlewska et al, 2009;Gerding et al, 2007) interacting noncovalently with the peptidoglycan layer (Leduc et al, 1992;Bouveret et al, 1999), outer membrane proteins OmpA (Clavel et al, 1998) and Lpp (Cascales et al, 2002), periplasmic protein TolB (Bouveret et al, 1995 and the inner membrane protein TolA (Cascales et al, 2000;Deprez et al, 2005). Although the exact function of Pal is unknown, Pal deletion mutants in E. coli exhibit cell envelope defects and greater susceptibility to the antibiotic vancomycin (Bernadac et al, 1998;Cascales & Lloubès, 2004).…”

Section: Introductionmentioning

confidence: 99%

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Dual orientation of the outer membrane lipoprotein Pal in Escherichia coli

et al. 2015

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Peptidoglycan associated lipoprotein (Pal) of Escherichia coli (E. coli) is a characteristic bacterial lipoprotein, with an N-terminal lipid moiety anchoring it to the outer membrane. Since its discovery over three decades ago, Pal has been well studied for its participation in the TolPal complex which spans the periplasm and has been proposed to play important roles in bacterial survival, pathogenesis and virulence. Previous studies of Pal place the lipoprotein in the periplasm of E. coli, allowing it to interact with Tol proteins and the peptidoglycan layer. Here, we describe for the first time, a subpopulation of Pal which is present on the cell surface of E. coli. Flow cytometry and confocal microscopy detect anti-Pal antibodies on the surface of intact E. coli cells. Interestingly, Pal is surface exposed in an 'all or nothing' manner, such that most of the cells contain only internal Pal, with fewer cells (,20 %) exhibiting surface Pal.

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“…The Tol-Pal complex of Gram-negative bacteria includes three cytoplasmic membrane proteins TolA, TolQ and TolR, which interact with each other through their transmembrane segments Lazzaroni & Portalier, 1981). The outer-membrane-anchored Pal lipoprotein interacts with the periplasmic TolB protein and the C-terminal domain of TolA to form a complex (Bouveret et al, 1995). Deletion or mutation of any of the tol or pal genes results in numerous defects, such as periplasmic leakage, increased susceptibility to many toxic compounds and formation of outer membrane vesicles (Bernadac et al, 1998;Webster, 1991).…”

Section: Introductionmentioning

confidence: 99%

TolA mediates the differential detergent resistance pattern between the Salmonella enterica subsp. enterica serovars Typhi and Typhimurium

et al. 2011

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The tol–pal genes are essential for maintaining the outer membrane integrity and detergent resistance in various Gram-negative bacteria, including Salmonella. The role of TolA has been well established for the bile resistance of Salmonella enterica subsp. enterica serovar Typhimurium. We compared the bile resistance pattern between the S. enterica serovars Typhi and Typhimurium and observed that Typhi is more resistant to bile-mediated damage. A closer look revealed a significant difference in the TolA sequence between the two serovars which contributes to the differential detergent resistance. The tolA knockout of both the serovars behaves completely differently in terms of membrane organization and morphology. The role of the Pal proteins and difference in LPS organization between the two serovars were verified and were found to have no direct connection with the altered bile resistance. In normal Luria broth (LB), S. Typhi ΔtolA is filamentous while S. Typhimurium ΔtolA grows as single cells, similar to the wild-type. In low osmolarity LB, however, S. Typhimurium ΔtolA started chaining and S. Typhi ΔtolA showed no growth. Further investigation revealed that the chaining phenomenon observed was the result of failure of the outer membrane to separate in the dividing cells. Taken together, the results substantiate the evolution of a shorter TolA in S. Typhi to counteract high bile concentrations, at the cost of lower osmotic tolerance.

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Peptidoglycan-associated Lipoprotein-TolB Interaction

Cited by 133 publications

References 47 publications

Competitive recruitment of the periplasmic translocation portal TolB by a natively disordered domain of colicin E9

Competitive recruitment of the periplasmic translocation portal TolB by a natively disordered domain of colicin E9

Dual orientation of the outer membrane lipoprotein Pal in Escherichia coli

TolA mediates the differential detergent resistance pattern between the Salmonella enterica subsp. enterica serovars Typhi and Typhimurium

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