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Chapter 5 : Chlamydial Adhesion and Adhesins

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Abstract:

This chapter focuses on recent advances in understanding the attachment of chlamydial elementary body (EB) to target cells. The early hints of a role for OmcB in adhesion to mammalian cells and the subsequent identification of OmcB as an EB surface protein that binds heparin were important first steps in the understanding of chlamydial adhesion. Enzyme-linked immunosorbent assay and flow cytometric analyses showed that preincubation with recombinant OmcB dramatically decreased the incidence of EB attachment to epithelial and endothelial cells. These data strongly argue that OmcB acts as an adhesin for association to human cells and is of primary importance for infection by several chlamydial species. Regardless of the structure of the glycosaminoglycan (GAG) recognized by OmcB, it has been proposed that the attachment of chlamydiae to human cells via OmcB-GAG interactions is a first step towards successful internalization. Blocking this initial interaction between an EB and the target cell by the addition of excess soluble HS, recombinant OmcB, or anti-OmcB antibody never inhibits the infection by more than 90%. This residual infectivity points to the presence of additional adhesin-receptor interactions, and the recent identification of the polymorphic membrane protein (Pmp) family as a new group of chlamydial adhesins supports this concept. Adhesion studies suggest that perhaps all Pmp proteins act as adhesins. Given that Pmp proteins act as adhesins, the data may suggest that there is considerable pressure to diversify their expression to adapt to new niches.

Citation: Hegemann J, Moelleken K. 2012. Chlamydial Adhesion and Adhesins, p 97-125. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch5
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FIGURE 1

A conserved N-terminal binding motif in OmcB is required for HS-dependent adhesion to HEp-2 cells. (A) The N-terminal segment (aa 41 to 84) of OmcB from serovar L2 (chosen as generally representative of chlamydial OmcB proteins) is presumably exposed on the surface of EBs, while the rest of the protein remains in the periplasm in association with the outer membrane. The OmcB C-terminal region is highly conserved, while the N-terminal segment starting at aa 41 (the predicted site of cleavage by signal peptidase) is highly variable. Asterisks indicate the two alternative proteolytic cleavage sites identified in the serovar L2 OmcB, which are used with the same frequency ( ). (B) N-terminal OmcB sequences from 16 different chlamydial species and serovars were aligned using the MultAlin tool (expasy.org). Identical sequences were grouped. Basic residues are marked in bold (R = arginine, K = lysine, H = histidine). The heparin-binding motifs XBBXBX (B = basic residue; X = hydrophatic amino acid) originally proposed by Stephens are indicated by the dashed outlines ( ). The OmcB has two copies of the motif. The grey-shaded box represents the extended heparin-binding region proposed here. The synthetic OmcB peptides derived from and that confer heparin binding activity are shown below the alignments ( ). Dashes represent gaps in the alignment. OmcB accession nos. (obtained from NCBI): , AAB61619; CWL029, NP_224753; E, P23603; F/IC-Cal3, M85196; Sweden2, CBJ14964; D/H/G/K, Q548P6; A/HAR-13, YP_328263; B/Jali20/OT, YP_002888064; C, P26758; I/J, Q933I7; L1/L2/L3,P21354. (C) The OmcB protein harbors a duplication of the original heparin-binding motif XBBXBX (boxed with the basic residues in bold) (aa 41 to 100) ( ). Replacement of all three basic residues in motif I by alanine residues abolishes OmcB-mediated adhesion to epithelial HEp-2 cells ( ). Deletion of the second heparin-binding motif (motif II) also resulted in the complete loss of adhesion, indicating that the binding motif in the OmcB protein is larger than originally suggested (Fechtner et al., unpublished). Secondary-structure prediction was done with GORIV. Adhesion symbols: +++++ to −, strong adhesion to no adhesion. doi:10.1128/9781555817329.ch5.f1

Citation: Hegemann J, Moelleken K. 2012. Chlamydial Adhesion and Adhesins, p 97-125. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch5
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Image of FIGURE 2
FIGURE 2

Dependence of different OmcB proteins on the presence of heparin on target cells for successful infection. (A) The serovars E, LGV, and B vary in their requirement for HS-like GAGs on target cells for successful infection. This variability is seen in the OmcB proteins from these serovars. The extent to which binding of these OmcBs to epithelial HEp-2 cells is inhibited by heparin (“Heparin-dependent”) is indicated. A stretch of residues C terminal to the heparin-binding domain (“motif”) exhibits serovar-specific variability (“variable region”) at positions 66, 68, and 71 (relevant residues are shown in bold). The amino acid residue at position 66 determines whether or not infection is dependent on heparin. Thus, replacement of the proline at position 66 in OmcB from biovar LGV with a leucine corresponding to the residue at the same position in OmcB from serovar E makes infection by the former independent of heparin, and vice versa ( ). The sequence of the serovar E OmcB variant corresponds to that of the OmcB proteins of the trachoma and genital serovars A to D and F to K. The asterisk reflects heparin dependence of serovar B attachment ( ). (B) A model depicting binding of OmcB proteins from serovars E, L2, and B to highly sulfated GAG structures like HS or heparin, incorporating secondary structure predictions based on the amino acid sequences shown in panel A. Relevant residues are marked, and serovar-specific residues are enlarged. Strong heparin dependence of OmcB from LGV could be due to a series of interactions of the basic residues in the heparin-binding motif presented in an α-helical structure, supported by additional basic amino acids and by an asparagine at position 68 (known to form hydrogen bonds to GAGs). The leucine residue at position 66 of the OmcB from serovar E results in a structural change and thereby alters GAG recognition. The moderate heparin dependence of OmcB of serovar B could be due to loss of contact sites due to different residues at positions 68 (aspartic acid, D) and 71 (glutamic acid, E). doi:10.1128/9781555817329.ch5.f2

Citation: Hegemann J, Moelleken K. 2012. Chlamydial Adhesion and Adhesins, p 97-125. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch5
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Image of FIGURE 3
FIGURE 3

General properties of selected Pmp proteins from and . Pmp proteins including PmpD from (A) and Pmp6, Pmp20, and Pmp21 from (B) are presumably autotransporters, as they exhibit the typical three-domain structure with N-terminal signal sequence (ss), passenger domain, and β-barrel ( ). Pmp proteins are characterized by the presence of the repeat motifs GGA(I,V,L) and FxxN (motif positions are indicated by white and grey vertical bars) ( ). PmpD, Pmp6, Pmp20, and Pmp21 are processed posttranslationally (at positions indicated by scissors and the numbered N-terminal residue) to yield processed forms indicated by the black lines beneath each protein. (A) PmpD exhibits a complex (presumably biphasic) processing pattern, yielding insoluble as well as soluble forms (drawn according to their apparent molecular weight) ( ). (B) Processing of the Pmp6, Pmp20, and Pmp21 proteins results in processed forms labeled for their relative positions (N, M, or C terminal) in the full-length protein ( ). Functionally characterized protein derivatives of Pmp6, Pmp20, and Pmp21 are marked by thin brackets. NLS, nuclear localization signal; RGD, integrin binding site. Domain structure was predicted with Pfam HMM search at expasy.org. doi:10.1128/9781555817329.ch5.f3

Citation: Hegemann J, Moelleken K. 2012. Chlamydial Adhesion and Adhesins, p 97-125. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch5
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Image of FIGURE 4
FIGURE 4

Pmp proteins are adhesins, and binding is mediated by repeat motifs. The PDs of the three largest Pmp proteins from mediate adhesion to epithelial HEp-2 cells and attenuate subsequent infection ( ). Recombinant subdomains of N-Pmp21 and M-Pmp21, each harboring two motifs only, adhered efficiently to human cells, but point mutations in the motifs, or a 4-residue-deletion (labeled by Δ), abrogated binding. Likewise, a synthetic peptide derived from M-Pmp21 carrying a doublet of FxxN and GGAI was able to significantly reduce infection, while a scrambled peptide showed no activity. Repeat motifs GGA(I,V,L) and FxxN are labeled as in Fig. 3 . doi:10.1128/9781555817329.ch5.f4

Citation: Hegemann J, Moelleken K. 2012. Chlamydial Adhesion and Adhesins, p 97-125. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch5
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Image of FIGURE 5
FIGURE 5

Oligomerization model for the Pmp proteins. (A) Experimental evidence for native PmpD oligomers on infectious EBs was provided by Swanson and colleagues ( ). Structure predictions reveal three-stranded β-helix domains in most of the Pmp proteins. In other proteins these β-helices (triangular prisms) have been shown to interact with each other to form oligomeric structures. The model shows the passenger domain (light grey prism) of a Pmp protein that has a β-barrel (cylinder) interacting with a processed form of Pmp (dark grey prism) via β-helix or other interaction domains. (B) On the EB cell surface Pmp oligomers could be formed by full-length and/or processed forms of a single species of Pmp protein, forming homo-oligomers (single-shaded oligomers). Alternatively or in addition, hetero-oligomers could be formed from processed and nonprocessed forms of the same Pmp subtype or a combination of Pmp subtypes. Variable expression of individual Pmp proteins indicated by “on” and “off” might increase the diversity of Pmp complexes. doi:10.1128/9781555817329.ch5.f5

Citation: Hegemann J, Moelleken K. 2012. Chlamydial Adhesion and Adhesins, p 97-125. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch5
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Image of FIGURE 6
FIGURE 6

Generalized model for chlamydial adhesion to host cells. Attachment of chlamydiae to host cells is proposed to be a two-step mechanism. The initial, reversible association of the EB with the host cell is via binding of the OmcB protein to HS and/or HSPG in soluble form or associated with the host cell surface. Additional interactions may involve chlamydial high-mannose oligosaccharide structures and host cell mannose receptors (not shown). In the next step, Pmp proteins (and possibly other adhesins including invasin-like chlamydial proteins) bind to as yet unidentified receptors on the host cell surface. Surface-localized PDI and/or membrane-associated estrogen receptor (mER) may serve as a structural component of one or more of the host cell receptors. These tight interactions may then allow interaction of the type III secretion system (T3SS) of the EB with the host membrane and release of the first wave of effector proteins (including Tarp) into the host cytosol (see chapter 6). More details are provided in the text. doi:10.1128/9781555817329.ch5.f6

Citation: Hegemann J, Moelleken K. 2012. Chlamydial Adhesion and Adhesins, p 97-125. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch5
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Tables

Generic image for table
TABLE 1a

EB cell surface components associated with adhesion and/or infection

Citation: Hegemann J, Moelleken K. 2012. Chlamydial Adhesion and Adhesins, p 97-125. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch5
Generic image for table
TABLE 1b

EB cell surface components associated with adhesion and/or infection

Citation: Hegemann J, Moelleken K. 2012. Chlamydial Adhesion and Adhesins, p 97-125. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch5
Generic image for table
TABLE 2

Host cell surface localized/soluble molecules with relevance to adhesion and/or infection

Citation: Hegemann J, Moelleken K. 2012. Chlamydial Adhesion and Adhesins, p 97-125. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch5

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