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Polymorphic membrane proteins (pmps)

Microbiologists in general are particularly interested in the surface of pathogenic bacteria. This is because it is the surface of bacteria which comes into contact with the host and it is the surface which is particularly exposed to attack by the hosts’ immune defences. A paper in 1996 by Longbottom and colleagues, working at the Moredun veterinary research institute near Edinburgh, Scotland, which reported a new family of 4 closely related genes at the surface of Chlamydophila abortus strain S26/3 [Longbottom et al., 1996, 1998] therefore aroused great interest. C. abortus is an economically important cause of abortion in sheep and a recombinant pmp of 90 KDa shows promise as an antigen to disntinguish serologically between sheep infected with C. abortus and the frequently associated C. pecorum [Longbottom et al., 2002].

A similar family of genes were found in avian C. psittaci [Tanzer et al., 2001] and in C. felis, the cat conjunctivitis agent. Similar genes were not detected in C. trachomatis or C. pneumoniae, although they stated that they could not exclude the possibility that such genes were present [Longbotom et al., 1998]. By electron microscopy and other methods, it could be shown that these proteins, although only minor components, were nevertheless immunodominant at the C. abortus surface [Giannikopoulou et al., 1997; Longbottom et al., 1998a; Longbottom et al., 1998b]. Furthermore, the absence of these proteins from C. pecorum, suggested that the presence or absence of antibody to this new class of proteins, which they called the principal outer membrane proteins (POMPs), could be used to distinguish whether flocks of sheep were infected with C. abortus or C. pecorum.

In Chlamydophila felis 12 pmp genes with a confusingly different notation were present in 40 strains and transcripts for all these genes were detected at 24 and 48 hours post inoculation. Analysis of the relative levels of pmp gene transcription suggested that down-regulation of the expression of multiple C. felis pmp genes occurs between 24 and 48 h post inoculation. [Harley et al., 2007]. 

In C. abortus at least, the pmps are N-glycosylated. Analysis with exoglycosidases suggested that some of the oligosaccharides in the pmps face outwards, perhaps protecting the polypeptides from proteolytic enzymes, whereas the oligosaccharides in the 105 kDa pmp-related protein are oriented inwards, perhaps rendering the polypeptide chain accessible to proteases [Vretou et al., 2001]. It was suggested a possible role for the N-linked oligosaccharides in the pmps might be promotion of the proper folding and processing of these proteins.

The discovery of similar, surface exposed, outer membrane proteins, OMP4 and OMP5, in C. pneumoniae [Knudsen et al., 1999], and in C. trachomatis [Stephens et al., 1998] showed that these proteins were not just restricted to chlamydiae of veterinary interest.

The importance of these discoveries became clear from whole chlamydial genome sequencing, when a family of 9 genes encoding these proteins was found in C. trachomatis [Stephens et al., 1998] and a staggering 21 paralogous genes in C. pneumoniae [Kalman et al., 1999; a paralogous gene is a gene derived within a species from a duplication event]. There are at least 5 similar genes in C. abortus. Characteristically, all the proteins encoded by these genes are rich in the amino acid serine. They also have the amino acid phenyl-alanine at the amino terminus and most have signal peptides indicating that they are likely membrane proteins. The close relationships between these genes, which in some cases only differed by mutations affecting the reading frame of the genetic code, led to them being termed the polymorphic membrane protein, pmp genes [Stephens et al., 1998; Kalman et al., 1999]. These so-called frameshift mutations may represent an underlying mechanism for differential expression of pmp proteins and/or variation of pmp protein structure. It is also conceivable that the multiple laboratory passages of the sequenced strains may have given rise to alterations in pmp gene sequence, in which case it may be important to study fresh clinical isolates.

In both C. trachomatis and C. pneumoniae, the pmp genes are often clustered together. Taking C. trachomatis as an example, one cluster contained three adjacent genes (pmpA, pmpB & pmpC) with the predicted proteins encoded on the same strand of nucleic acid while another cluster contained four genes, with two of each gene encoded on opposing strands of DNA (pmpE, pmpF, pmpG and pmpH). The pmpI gene was also closely located near one of these clusters. The occurence of genes in clusters often indicates that they are regulated or function as one entitity. The pmpD gene is not co-located near either of the two major clusters.

Comparison of the C. trachomatis and C. pneumoniae pmp sequences showed a large amount of heterogeneity among members of the family; the maximum identity between any 2 pmp proteins being only 37.5% [Grimwood et al., 1998]. C. pneumoniae and C. trachomatis pmp genes group into 6 families, each of which contains at least one C. trachomatis sequence plus at least one C. pneumoniae sequence, suggesting each family has a specific functional role in chlamydial biology. One of these families, based on the single C. trachomatis pmpG gene, had 11 homologues in C. pneumoniae, indicating that multiple gene duplications have occurred [Grimwood et al., 1998; 2001]. The large number of genes, significant nucleotide sequence polymorphisms, the clustering of genes, the various locations in the genome, the gene duplication and different coding directions suggest that recombination is an important mechanism for sequence variability [Stephens et al., 1998].

The pmp genes encode large proteins of from 288 to 582 amino acids . In particular, all encode repeats (2-13 copies) of the amino acid sequence GGAI and FXXN in the N terminal half of the protein [Stephens et al., 1998; Kalman et al., 1999; Grimwood et al., 1998; Grimwood & Stephens, 1999]. In C. trachomatis only, genes for 2 predicted protein-degrading enzymes are found adjacent to one of the pmp gene clusters. As the target for these enzymes is the amino acid sequence -glycine-glycine- it is likely pmp-encoded proteins are the targets of these degradative enzymes. Moreover, as these enzymes are not present in the C. pneumoniae genome sequence, they may provide a crucial biological function differentiating C. trachomatis from C. pneumoniae [Kalman et al., 1999]. Computational analysis indicates that there are six related families of pmps, each with at least one C. trachomatis and one C. pneumoniae orthologue. In C. pneumoniae one of these families has undergone prolific expansion in resulting in 13 protein paralogues . The maintenance of orthologues from each species suggests specific functions for the proteins in chlamydial biology [Grimwood & Stephens, 1999].

Palmer (2002) points out that pathogens such as Rickettsia, Chlamydiaceae, Ehrlichia, Mycoplasma and spirochaetes often devote a high percentage of their genomes to paralogous families of polymorphic surface molecules which may be significant for evasion of the host immune response [see: chlamydial evolution - genome degradation]. 

Transcription and Translation

All of the pmp genes for C. trachomatis and C. pneumoniae are transcribed, but only a few are stably translated and present in the chlamydial outer membrane. The expression of several pmps differs among different C. pneumoniae strains. Some pmps, for example pmp8 and 11, appear to be stably expressed in C. pneumoniae elementary bodies [Pedersen et al., 2001]. Expression of pmp10 even varies within a strain. This appears to be due to inter and intra strain variation in the number of guanine residues [Stephens & Lamell, 2000; Pedersen et al., 2001].  Expression can even vary within a single inclusion derived from infection with just one elementary body. This results with only a few bacteria expressing pmp10 within the inclusion [Pedersen et al., 2001], again  reflecting switching events based on the number of guanine residues, with some of the progeny in frame for translation, and others not.

It is clear that some, at least, of the pmp proteins are produced early in infection [Lindquist and Stephens, 1998], while others in C. psittaci are produced late in development co-temporaneously with the cysteine rich periplasmic proteins [Tanzer et al., 2001]. The pmps are produced in the intact host [Birkelund et al., 1998], and some at least are located at the surface of the infectious chlamydial elementary body [Longbottom et al., 1998a, 1998b, Knudsen et al., 1999] where some are trypsin sensitive [Tanzer et al., 2001]. The pmps in C. psittaci were dependent on disulphide bonds for their maintenance in sodium lauryl sacosine or sodium dodecyl sulphate- [detergent] insoluble complexes, but there was no evidence for interpeptide -S-S- bond crosslinking [Tanzer et al., 2001]. Using a photoactivatable, lipophilic, radiolabelled probe for surface proteins which were then identified from gels by mass spectrometry, Tanzer & Hatch (2001) elegantly demonstrated that Pmps E, G, and H,  the major outer membrane protein, and a mixture of 46-kDa proteins thought to consist of the open reading frame 623 protein and possibly a modified form of the major outer membrane protein were surface located in C. trachomatis serovar L2. Using proteomics techniques Van Dahl et al., 2002 identified ten pmp proteins expressed by elementary bodies of C. pneumoniae strain CWL029.  Eight of these Pmps were further investigated. All eight were found to be expressed from 36 to 48 hours post infection. Pmp6, Pmp20 and Pmp21 were found in cleaved forms, and the cleavage sites of Pmp6 and Pmp21 were identified.  Both sites are located between the C-terminal predicted beta barrel and the N-terminal predicted parallel beta helix fold. This position is consistent with the theory that these Pmps are autotransporters which cleave off their N-terminal portion. They may also have a role in attachment and entry since an N-terminal triangular beta-layer motif might provide the bacteria with a shielding lattice and ensure proper spacing to a host cell or to an epitope exposed to the complement system. If the lipid modifications of Pmp10 and Pmp11 are used as anchors inserted into the host cell membrane, subsequent action of other entry molecules would depend on proper spacing. However, this is speculative [Van Dahl et al., 2002]. Proteomic studies confirm that MOMP and pmp10 are closely associated in the outer envelope of Chlamydophila pneumoniae CWL029, where it is thought to protect the C-terminus of the major outer membrane protein from proteolytic cleavage [Juul et al., 2007].

It is possible that many of the pmp genes are silent, i.e. not normally expressed. It is not clear whether the variability of pmp gene sequence represents antigenic variability due to pressure from the host immune system, or is simply intrinsic variability. So far, the function of the pmp gene products is unknown. However a red blood cell-disrupting cytolysin has been expressed in a gene bank cloned from C. trachomatis serovar L2 and its corresponding gene found homologous with the  pmpD gene from the whole C. trachomatis genome sequence. Thus pmpD is probably a cytolysin, which may contribute to host cell disruption and the release of chlamydial elementary bodies [Lampe et al., 1998]. However it appears to be distinct from the chlamydial cytotoxin described by Belland et al., 2001.  Henderson & Lam (2001) in a review point out that the pmps resemble members of the type V autotransporters family of proteins and suggest that they may follow the same secretion pathway. The autotransporter concept is supported by the work of Kiselev et al., 2007, who analyzed the transcription and translation of the pmpD gene in C. trachomatis serovar L2. By real-time reverse transcription polymerase chain reaction, the pmpD gene was found to be upregulated at 16 - 24 hours post infection. The PmpD protein was initially localized on the surface of reticulate bodies, followed at 24 hours by its secretion outside the organism. Both events, the upregulation of pmpD gene transcription and PmpD protein processing and secretion, were coincidental with the period of replication and differentiation of RBs into EBs. Penicillin inhibited the cleavage and secretion of the autotransporter domain.

In C. trachomatis serovars E and L2, all pmps were found to be expressed at two hours, confirming their involvement in reticulate body development. Serological studies indicated that PmpD was highly antigenic. antibody to PmpF was not present in sera from infected subjects, even though pmpF had the highest levels of expression but with with differential expression of the pmpFE operon for the same strains. Differential expression of the mppFE operon was not explained by absence of promoter, as a putative pmpFE promoter was identified, which was, surprisingly, 100% conserved for all strains. Analyses of ribosomal binding sites, RNase E, and hairpin structures suggest that there are complex regulatory mechanisms for this operon. It was suggested that the dissimilar expression of the same pmp for different C. trachomatis strains might explain different strain-specific phenotype and requirements. Differences in pmp gene transcription between clinical and reference isolates of C. trachomatis serovar E suggest the particular need for studies of clinical strains [Nunes et al., 2007].

Phyllogeny of C. trachomatis pmps in relationship to disease groups and tissue specificity

Stothard et al., 2003 explored the possibility that pmp gene sequences might provide useful variability for epidemiological studies. They initially sought to determine the amount of diversity within an individual pmp gene among serovars using RFLP (restriction fragment length polymorphism) analysis as a preliminary screen for sequence divergence among serovars A to L3 of C. trachomatis. Little variation was observed for some of the genes, such as pmpA, but substantial variation was observed in others, such as pmpI. Usefully, pmpH and pmpE yielded RFLP patterns that grouped the 15 serovars of C. trachomatis into ocular, urogenital, and LGV groups. Both these proteins have been localized to the outer membrane. The pmpE, pmpH, and pmpI genes from each of the 15 serovars of C. trachomatis were therefore sequenced. Evolutionary analysis revealed three distinct divergence patterns. PmpI was highly conserved, resulting in an ambiguous phylogenetic pattern [not shown]. This might indicate either that PmpI plays a general role in pathogenesis; or that it is not exposed to immune pressure, either because it is not surface located [Tanzer & Hatch, 2001] or because it is not expressed. PmpE showed up to 6.5% nucleotide and amino acid diversity among serovars in different disease groups, particularly among ocular serovars, but only 0.5% dissimilarity within serovars. In serovar L2 there is controversy as to whether pmpE is [Tanzer & Hatch, 2001], or is not [Mygind et al., 2000] surface located. Finally, the evolution of pmpH showed three groups reflecting the three disease groups. This is intriguing as this protein belongs to the type V secretion pathway  proteins that include, in other bacteria,  various toxins, adhesins and mediators of intracellular motility. Thus it is possible that pmpH may play a significant role in pathogenesis [Stothard et al., 2003].

Gomes et al., 2004 performed phylogenetic analyses and statistical modeling on pmpC gene sequences of 18 reference serovars and 1 genovariant of C. trachomatis. They observed a clear distinction for disease groups, corresponding to levels of tissue specificity and virulence of the organism. Moreover, the most prevalent serovars, E, F, and Da, formed a distinct clade containing two putative insertion sequence (IS)-like elements, while all other genital serovars contained only one such element. Ocular trachoma serovars also contained both insertions and the finding is of interest as no IS-like elements, which might be expected to facilitate recombination had previously been identified for the Chlamydiaceae. This latter concept is supported by the finding that 7 (58%) of 12 clinical isolates had pmpC sequences that were identical to the sequences of other serovars, providing clear evidence for a high rate of whole-gene recombination. Thus, recombination and the differential presence of IS-like elements among distinct disease and prevalence groups may contribute to genome plasticity, leading to adaptive changes in tissue tropism and pathogenesis during the course of the organism's evolution.  Expression of pmpC expression occurred at 2 h, and peaked at 18 - 24 hours [Gomes et al., 2005].  It was suggested that heterogeneous biovariant-specific pmpC expression throughout development tegether with differential PmpC immunoreactivity indicates a role for pmpC in antigenic variation.

Subsequently Gomes et al., (2006) performed genomic and molecular analyses for the entire pmp gene family of C. trachomatis for the 18 reference serological variants (serovars) and genovariant Ja in order to identify specific regions that differentiated chlamydial disease groups. They found that the mean genetic distance among all serovars varied from 0.1% for pmpA to 7.0% for pmpF.  Phylogeny showed that for six of nine pmp genes ( ie not pmpA, pmpD, or pmpE), the serovars clustered based on tissue tropism. The most most common serovars, E and F, clustered distantly from the remaining urogenital group for five pmp genes. These pmp genes may facilitate infection and transmission for E and F. Surprisingly, serovar Da clustered with the ocular group from pmpE to pmpI, (which are located together in the chromosome), again providing evidence for intergenomic recombination. In pmpE, pmpF and pmpH, distinct domains were identified where substitutions concentrated and which were associated with specific disease groups. These data are consistent with the earlier observations of Stothard et al., 2003 (above) and suggest mechanisms which vary among pmp genes which might promote antigenic polymorphisms and/or diverse adhesin - receptor interactions, and which might also be involved in immune evasion and differential tissue tropism.

Carlson et al., (2005) sequenced and compared the genome of oculotropic C. trachomatis A/Har13 with the pre-existing genome sequence for genitotropic D/UW3. A disproportionate number of single nucleotide changes (SNPs) were observed within some members of the polymorphic membrane protein gene family that corresponded to predicted T-cell epitopes that bind HLA class I and II alleles. These results indicate that some of the pmps are likely targets for cell mediated immunity.

Potential of pmpD as a vaccine candidate

PmpD is immunogenic in natural human infection [Nunes et al., 2007]. PmpD, the longest of the 21 pmps expressed by Chlamydophila pneumoniae, is split into an N-terminal, middle and C-terminal portion. The N-terminal pmpD translocates to the surface of the chlamydiae where it is non-covalently bound to other components of the outer membrane. Antibodies against N-terminal pmpD were neutralising. Recombinant N-terminal pmpD also stimulated monocyte activation [Wehrl et al., 2004].

Crane et al., (2006) confirmed that pmpD is a highly conserved surface membrane protein in C. trachomatis capable of generating species-specific neutralising antibody against all C. trachomatis serovars. However, pre-existing antibody against serovariable-neutralizing targets, such as the major outer membrane protein, blocked pmpD - mediated neutralization. It was suggested that a decoy-like immune evasion strategy may be active in vivo whereby immunodominant type-specific surface antigens block the neutralizing ability of species-specific pmpD antibody. Furthermore, a vaccine protocol using recombinant pmpD to elicit neutralizing antibody in the absence of immunodominant type-specific antibody might surpass the level of protection achieved through natural immunity. 

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References

Birkelund, S., Knudsen, K., Madsen, A.S. et al., (1998) Differential expression of Chlamydia pneumoniae OMP4 and OMP5 after infection of C57-Black mice. In: Chlamydial infections. Proceedings of the ninth international symposium on human chlamydial infection, pages 275-278. Pub: International Chlamydia Symposium, San Francisco USA, ISBN 0-9664383-0-2.

Carlson, J. H., Porcella, S. F., Mcclarty, G. & Caldwell, H. D. (2005). Comparative genomic analysis of Chlamydia trachomatis oculotropic and genitotropic strains. Infection and Immunity 73, 6407 - 6418.

Crane, D. D., Carlson, J. H., fischer E. R., Bavoil, P., Hsia, R-C., Tan, C., Kuo, C.C & Caldwell, H. D. (2006). Chlamydia trachomatis polymorphic membrane protein D is a species-common pan-neutralizing antigen. Proc Natl Acad Sci U S A. 103, 1894 -1899. Full article

Giannikopoulou, P., Bini, L., Simitsek, P. D., Pallini, V. & Vretou, E. (1997). Two-dimensional electrophoretic analysis of the protein family at 90 kDa of abortifacient Chlamydia psittaci. Electrophoresis 18, 2104 - 2108. [An early proteomics study from Siena which identified expression of the pmp family in C. abortus before the whole genomic sequence. Good stuff].

Gomes, J. P., Bruno, W. J., Borrego, M. J. & Dean, D. (2004). Recombination in the genome of Chlamydia trachomatis involving the polymorphic membrane protein C gene relative to ompA and evidence for horizontal gene transfer. Journal of Bacteriology 186, 4295 - 4306.

Gomes, J. P., Hsia, R. C., Mead, S., Borrego, M. J. & Dean, D. (2005). Immunoreactivity and differential developmental expression of known and putative Chlamydia trachomatis membrane proteins for biologically variant serovars representing distinct disease groups. Microbes and Infection 7, 410 - 420.

Gomes, J. P., Nunes, A., Bruno, W. J., Borrego, M. J., Florindo, C. & Dean, D. (2006). Polymorphisms in the nine polymorphic membrane proteins of Chlamydia trachomatis across all serovars: evidence for serovar Da recombination and correlation with tissue tropism. Journal of Bacteriology 188, 275 - 286. Full article

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Grimwood, J., Olinger, L. & Stephens, R. S. (2001). Expression of Chlamydia pneumoniae polymorphic membrane protein family genes. Infection and Immunity 69, 2383 - 2389. Full article

Henderson, I. R. & Lam, A. C. (2001) Polymorphic proteins of Chlamydia spp.--autotransporters beyond the Proteobacteria. Trends in Microbiology 9, 573 - 578. [Review].

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Kalman, S., Mitchell, W., Marathe, R. et al., (1999). Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nature Genetics 21, 385 - 389.

Kiselev, A. O., Stamm, W. E., Yates, J. R. & Lampe, M. F. (2007). Expression, processing, and localization of PmpD of Chlamydia trachomatis serovar L2 during the chlamydial developmental cycle. Public Library of Science One Jun 27; 2(6): e568 Full article (html) Full article

Knudsen, K., Madsen, A. S., Mygind, P., Christiansen, G. & Birkelund, S. (1999). Identification of two novel genes encoding 97- to 99-kilodalton outer membrane proteins of Chlamydia pneumoniae. Infection and Immunity 67, 375 - 383.

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Longbottom, D., Russell, M., Jones, G. E., Lainson, F. A. & Herring, A. J. (1996). Identification of a multigene family coding for the 90 kDa proteins of the ovine abortion subtype of Chlamydia psittaci. FEMS Microbiology Letters 142, 277 - 281.[First discovery of the polymorphic membrane proteins and initial recognition of their potential as protective antigens].

 

Longbottom, D., Findlay, J., Vretou, E. & Dunbar, S. M. (1998b). Immunoelectron microscopic localisation of the OMP90 family on the outer membrane surface of Chlamydia psittaci. FEMS Microbiology Letters 164, 111 - 117.

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Vandahl, B. B., Pedersen, A. S., Gevaert, K., Holm, A., Vandekerckhove, J., Christiansen, G. & Birkelund, S. (2002). The expression, processing and localization of polymorphic membrane proteins in Chlamydia pneumoniae strain CWL029. Biomed Central Microbiology Nov 26 [E-print]. Full article

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Wehrl, W., Brinkmann, V., Jungblut, P. R., Meyer, T. F. & Szczepek, A. J. (2004).   From the inside out - processing of the Chlamydial autotransporter PmpD and its role in bacterial adhesion and activation of human host cells. Molecular Microbiology 51, 319 - 334.

[MEW] January 2008.
 

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