Mechanism of anchoring of OmpA protein to the cell wall peptidoglycan of the gram‐negative bacterial outer membrane

Park, Jeong Soon; Lee, Woo Cheol; Yeo, Kwon Joo; Ryu, Kyoung‐Seok; Kumarasiri, Malika; Hesek, Dušan; Lee, Mijoon; Mobashery, Shahriar; Song, Junho; Kim, Kyung Sik; Lee, Je Chul; Cheong, Chaejoon; Jeon, Young Ho; Kim, Hye-Yeon

doi:10.1096/fj.11-188425

Cited by 173 publications

(201 citation statements)

References 51 publications

Supporting

Mentioning

197

Contrasting

Order By: Relevance

“…We do note, however, that TprC N lacks a recognizable OmpA-like peptidoglycan-binding motif (18,44), an observation that we do not find surprising given the reverse bipartite topologies of TprC and OmpA (61) and the phylogenetic distance separating spirochetes from diderms which do possess OmpA orthologs (46). Furthermore, it has not escaped our attention that the topologic model proposed for TprC can be extended readily to TprI, which differs from TprC mainly within the periplasmic domain, and TprF, which is predicted to be entirely periplasmic (Fig.…”

Section: Discussionmentioning

confidence: 86%

TprC/D (Tp0117/131), a Trimeric, Pore-Forming Rare Outer Membrane Protein of Treponema pallidum, Has a Bipartite Domain Structure

et al. 2012

View full text Add to dashboard Cite

e Identification of Treponema pallidum rare outer membrane proteins (OMPs) has been a longstanding objective of syphilis researchers. We recently developed a consensus computational framework that employs a battery of cellular localization and topological prediction tools to generate ranked clusters of candidate rare OMPs (D. L. Cox et al., Infect. Immun. 78:5178 -5194, 2010). TP0117/TP0131 (TprC/D), a member of the T. pallidum repeat (Tpr) family, was a highly ranked candidate. Circular dichroism, heat modifiability by SDS-PAGE, Triton X-114 phase partitioning, and liposome incorporation confirmed that full-length, recombinant TprC (TprC Fl ) forms a ␤-barrel capable of integrating into lipid bilayers. Moreover, TprC Fl increased efflux of terbium-dipicolinic acid complex from large unilamellar vesicles and migrated as a trimer by blue-native PAGE. We found that in T. pallidum, TprC is heat modifiable, trimeric, expressed in low abundance, and, based on proteinase K accessibility and opsonophagocytosis assays, surface exposed. From these collective data, we conclude that TprC is a bona fide rare OMP as well as a functional ortholog of Escherichia coli OmpF. We also discovered that TprC has a bipartite architecture consisting of a soluble N-terminal portion (TprC N ), presumably periplasmic and bound directly or indirectly to peptidoglycan, and a C-terminal ␤-barrel (TprC C ). Syphilitic rabbits generate antibodies exclusively against TprC C , while secondary syphilis patients fail to mount a detectable antibody response against either domain. The syphilis spirochete appears to have resolved a fundamental dilemma arising from its extracellular lifestyle, namely, how to enhance OM permeability without increasing its vulnerability to the antibody-mediated defenses of its natural human host.

show abstract

Section: Discussionmentioning

confidence: 86%

TprC/D (Tp0117/131), a Trimeric, Pore-Forming Rare Outer Membrane Protein of Treponema pallidum, Has a Bipartite Domain Structure

et al. 2012

View full text Add to dashboard Cite

show abstract

“…With the glycan chains perpendicular to the cell surface, the resulting hexagonal cells form an underlying network capable of organizing and supporting OM proteins (55). Additional findings, including crystallographic data (56)(57)(58), support the VS model. One striking aspect is that the diameter of individual cells within its predicted matrix (ϳ60 Å) is about the same as that of many OMP ␤-barrels, including those of OmpF, LamB, TolC, LGP, and the dimeric form of the TonB C terminus (Fig.…”

mentioning

confidence: 57%

ROSET Model of TonB Action in Gram-Negative Bacterial Iron Acquisition

Klebba

2016

J Bacteriol

View full text Add to dashboard Cite

.g., OmpA), localizing it near the periplasmic interface of the OM bilayer. Porins and other OM proteins associate with PG, and this general affinity allows the TonB CTD dimer to survey the periplasmic surface of the OM bilayer. Energized rotational motion of the TonB N terminus in the fluid IM bilayer promotes the lateral movement of the TonB-ExbBD complex in the IM and of the TonB CTD dimer across the inner surface of the OM. When it encounters an accessible TonB box of a (ligand-bound) LGP, the monomeric form of the CTD binds and recruits it into a 4-stranded ␤-sheet. Because the CTD is rotating, this binding reaction transfers kinetic energy, created by the electrochemical proton gradient across the IM, through the periplasm to the OM protein. The equilibration of the TonB C terminus between the dimeric and monomeric forms that engage in different binding reactions allows the identification of ironloaded LGP and then the internalization of iron through their trans-outer membrane ␤-barrels. Hence, the ROSET model postulates a mechanism for the transfer of energy from the IM to the OM, triggering iron uptake.T he 239-amino-acid TonB protein underlies several aspects of Gram-negative bacterial cell envelope physiology, including obligatory involvement in metal (iron) transport through the outer membrane (OM), susceptibility to numerous bacteriocins/ microcins, and infection by certain bacteriophages. Regarding the role in iron transport, bacteria generally acquire iron by the elaboration of siderophores (1) that complex it in the environment. The subsequent active transport of ferric siderophores through OM receptor proteins (2, 3) requires TonB (4, 5).FepA is one such OM protein that selectively recognizes and internalizes the native siderophore of Escherichia coli, ferric enterobactin (FeEnt) (6). The N-terminal 150-residue globular portion of FepA (N-domain) resides within a C-terminal 22-stranded ␤-barrel (Fig. 1). The C-terminal ␤-barrel places FepA and its relatives in the porin superfamily (7,8). Their selectivity for ligands (9-11) and the fact that high-affinity ligand binding (12) triggers uptake through their transmembrane channels led to the designation ligand-gated porins (LGP) (13). They require energy and TonB for functionality, so they are also energy-and TonBdependent receptors or TonB-dependent transporters (TBDT) (14). None of these designations is fully appropriate, in that OM proteins in this class are not diffusive porins (15) and neither are they true transporters, a term usually reserved for ATP-or proton motive force (PMF)-driven inner membrane (IM) permeases (16). With the additional stipulation that their activities are TonB and energy dependent, in this paper, I will refer to FepA and its orthologs/paralogs as LGP.The need for TonB in the energy-dependent uptake of metals (ferric siderophores [3], heme [17], and cobalt as vitamin B 12 [2]) is a key aspect of cellular nutrition and an enigmatic feature of cell envelope physiology. FeEnt transport through the OM requires the electroche...

show abstract

“…In the vast majority, regardless of function, the entire polypeptide comprises the ␤-barrel (82,83). Three classes of bipartite OMPs, in which a single polypeptide comprises the entire OMspanning protein, have emerged as exceptions to this generalization: autotransporters (84), BamAs (Omp85 superfamily) (85)(86)(87)(88), and OmpAs (65,66,89). Whereas BamA and OmpA consist of ␤-barrels with sizeable periplasmic domains, the autotransporters are distinctive in that the hydrophilic passenger domain extrudes through the barrel to the exterior of the cell.…”

mentioning

confidence: 99%