Chapter 5 : Chlamydial Adhesion and Adhesins

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Chlamydial Adhesion and Adhesins, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817329/9781555816742_Chap05-1.gif /docserver/preview/fulltext/10.1128/9781555817329/9781555816742_Chap05-2.gif


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
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of 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
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of 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
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of 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
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of 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
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of 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
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of 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
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Abromaitis, S.,, and R. S. Stephens. 2009. Attachment and entry of Chlamydia have distinct requirements for host protein disulfide isomerase. PLoS Pathog. 5: e1000357. PubMed CrossRef
2. Ajonuma, L. C.,, K. L. Fok,, L. S. Ho,, P. K. Chan,, P. H. Chow,, L. L. Tsang,, C. H. Wong,, J. Chen,, S. Li,, D. K. Rowlands,, Y. W. Chung,, and H. C. Chan. 2010. CFTR is required for cellular entry and internalization of Chlamydia trachomatis. Cell Biol. Int. 34: 593 600. PubMed CrossRef
3. Allen, J. E.,, and R. S. Stephens. 1989. Identification by sequence analysis of two-site posttranslational processing of the cysteine-rich outer membrane protein 2 of Chlamydia trachomatis serovar L2. J. Bacteriol. 171: 285 291. PubMed
4. Barczyk, M.,, S. Carracedo,, and D. Gullberg. 2010. Integrins. Cell Tissue Res. 339: 269 280.
5. Bardiau, M.,, M. Szalo,, and J. G. Mainil. 2010. Initial adherence of EPEC, EHEC and VTEC to host cells. Vet. Res. 41: 1 16. PubMed CrossRef
6. Bavoil, P.,, A. Ohlin,, and J. Schachter. 1984. Role of disulfide bonding in outer membrane structure and permeability in Chlamydia trachomatis. Infect. Immun. 44: 479 485. PubMed
7. Bavoil, P. M.,, and R. C. Hsia. 1998. Type III secretion in Chlamydia: a case of déjà vu? Mol. Microbiol. 28: 860 862. PubMed CrossRef
8. Becker, Y.,, E. Hochberg,, and Z. Zakay-Rones. 1969. Interaction of trachoma elementary bodies with host cells. Isr. J. Med. Sci. 5: 121 124. PubMed
9. Beeckman, D. S.,, C. M. Van Droogenbroeck,, B. J. De Cock,, P. Van Oostveldt,, and D. C. Vanrompay. 2007. Effect of ovotransferrin and lactoferrins on Chlamydophila psittaci adhesion and invasion in HD11 chicken macrophages. Vet. Res. 38: 729 739. PubMed CrossRef
10. Bernfield, M.,, M. Gotte,, P. W. Park,, O. Reizes,, M. L. Fitzgerald,, J. Lincecum,, and M. Zako. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68: 729 777. PubMed CrossRef
11. Beswick, E. J.,, A. Travelstead,, and M. D. Cooper. 2003. Comparative studies of glycosaminoglycan involvement in Chlamydia pneumoniae and C. trachomatis invasion of host cells. J. Infect. Dis. 187: 1291 1300.
12. Birkelund, S.,, M. Morgan-Fisher,, E. Timmerman,, K. Gevaert,, A. C. Shaw,, and G. Christiansen. 2009. Analysis of proteins in Chlamydia trachomatis L2 outer membrane complex, COMC. FEMS Immunol. Med. Microbiol. 55: 187 195. PubMed CrossRef
13. Bose, S. K.,, and R. G. Paul. 1982. Purification of Chlamydia trachomatis lymphogranuloma venereum elementary bodies and their interaction with HeLa cells. J. Gen. Microbiol. 128: 1371 1379. PubMed CrossRef
14. Brade, H., 1999. Chlamydial lipopolysaccharide, p. 229 242. In H. Brade,, S. M. Opal,, S. N. Vogel,, and D. C. Morrison (ed.), Endotoxin in Health and Disease. Marcel Dekker Inc., New York, NY.
15. Bradley, P.,, L. Cowen,, M. Menke,, J. King,, and B. Berger. 2001. BETAWRAP: successful prediction of parallel beta -helices from primary sequence reveals an association with many microbial pathogens. Proc. Natl. Acad. Sci. USA 98: 14819 14824. PubMed CrossRef
16. Bunk, S.,, I. Susnea,, J. Rupp,, J. T. Summersgill,, M. Maass,, W. Stegmann,, A. Schrattenholz,, A. Wendel,, M. Przybylski,, and C. Hermann. 2008. Immunoproteomic identification and serological responses to novel Chlamydia pneumoniae antigens that are associated with persistent C. pneumoniae infections. J. Immunol. 180: 5490 5498. PubMed
17. Burall, L. S.,, Z. Liu,, R. Rank,, and P. M. Bavoil. 2007. The chlamydial invasin-like protein gene conundrum. Microbes Infect. 9: 873 880. PubMed CrossRef
18. Byrne, G. I. 1976. Requirements for ingestion of Chlamydia psittaci by mouse fibroblasts (L cells). Infect. Immun. 14: 645 651. PubMed
19. Byrne, G. I.,, and J. W. Moulder. 1978. Parasite-specified phagocytosis of Chlamydia psittaci and Chlamydia trachomatis by L and HeLa cells. Infect. Immun. 19: 598 606. PubMed
20. Caldwell, H. D.,, J. Kromhout,, and J. Schachter. 1981. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 31: 1161 1176. PubMed
21. Campbell, L. A.,, and C. C. Kuo,. 2006. Interactions of Chlamydia with the host cells that mediate attachment and uptake, p. 505 522. In P. M. Bavoil, and P. B. Wyrick (ed.), Chlamydia Genomics and Pathogenesis. Horizon Bioscience, Norfolk, United Kingdom.
22. Capila, I.,, and R. J. Linhardt. 2002. Heparin-protein interactions. Angew. Chem. Int. Ed. Engl. 41: 391 412. PubMed
23. Carabeo, R. A.,, and T. Hackstadt. 2001. Isolation and characterization of a mutant Chinese hamster ovary cell line that is resistant to Chlamydia trachomatis infection at a novel step in the attachment process. Infect. Immun. 69: 5899 5904. PubMed
24. Cardin, A. D.,, and H. J. Weintraub. 1989. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9: 21 32. PubMed CrossRef
25. Carrasco, J. A.,, C. Tan,, R. G. Rank,, R. C. Hsia,, and P. M. Bavoil. 2011. Altered developmental expression of polymorphic membrane proteins in penicillin-stressed Chlamydia trachomatis. Cell Microbiol. 13: 1014 1025. PubMed CrossRef
26. Cevenini, R.,, M. Donati,, E. Brocchi,, F. De Simone,, and M. La Placa. 1991. Partial characterization of an 89-kDa highly immunoreactive protein from Chlamydia psittaci A/22 causing ovine abortion. FEMS Microbiol. Lett. 65: 111 115. PubMed
27. Chang, J. J.,, K. Leonard,, T. Arad,, T. Pitt,, Y. X. Zhang,, and L. H. Zhang. 1982. Structural studies of the outer envelope of Chlamydia trachomatis by electron microscopy. J. Mol. Biol. 161: 579 590. PubMed
28. Chen, J. C.,, and R. S. Stephens. 1994. Trachoma and LGV biovars of Chlamydia trachomatis share the same glycosaminoglycan-dependent mechanism for infection of eukaryotic cells. Mol. Microbiol. 11: 501 507. PubMed
29. Chen, J. C.,, J. P. Zhang,, and R. S. Stephens. 1996. Structural requirements of heparin binding to Chlamydia trachomatis. J. Biol. Chem. 271: 11134 11140. PubMed CrossRef
30. Chen, J. C. R.,, and R. S. Stephens. 1997. Chlamydia trachomatis glycosaminoglycan dependent and independent attachment to eukaryotic cells. Microb. Pathog. 22: 23 30. PubMed CrossRef
31. Chen, Y.,, M. Gotte,, J. Liu,, and P. W. Park. 2008. Microbial subversion of heparan sulfate proteoglycans. Mol. Cells 26: 415 426. PubMed
32. Collett, B. A.,, W. J. Newhall,, R. A. Jersild, Jr.,, and R. B. Jones. 1989. Detection of surface-exposed epitopes on Chlamydia trachomatis by immune electron microscopy. J. Gen. Microbiol. 135: 85 94. PubMed CrossRef
33. Conant, C. G.,, and R. S. Stephens. 2007. Chlamydia attachment to mammalian cells requires protein disulfide isomerase. Cell. Microbiol. 9: 222 232. PubMed CrossRef
34. Crane, D. D.,, J. H. Carlson,, E. R. Fischer,, P. Bavoil,, R. C. Hsia,, C. Tan,, C. C. Kuo,, and H. D. Caldwell. 2006. Chlamydia trachomatis polymorphic membrane protein D is a species-common pan-neutralizing antigen. Proc. Natl. Acad. Sci. USA 103: 1894 1899. PubMed CrossRef
35. Cunningham, A. F.,, and M. E. Ward. 2003. Characterization of human humoral responses to the major outer membrane protein and OMP2 of Chlamydophila pneumoniae. FEMS Microbiol. Lett. 227: 73 79. PubMed
36. Darville, T.,, S. Yedgar,, M. Krimsky,, C. W. Andrews, Jr.,, T. Jungas,, and D. M. Ojcius. 2004. Protection against Chlamydia trachomatis infection in vitro and modulation of inflammatory response in vivo by membrane-bound glycosaminoglycans. Microbes Infect. 6: 369 376. PubMed CrossRef
37. Dautin, N.,, and H. D. Bernstein. 2007. Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol. 61: 89 112. PubMed CrossRef
38. Dautry-Varsat, A.,, A. Subtil,, and T. Hackstadt. 2005. Recent insights into the mechanisms of Chlamydia entry. Cell. Microbiol. 7: 1714 1722. PubMed CrossRef
39. Davis, C. H.,, J. E. Raulston,, and P. B. Wyrick. 2002. Protein disulfide isomerase, a component of the estrogen receptor complex, is associated with Chlamydia trachomatis serovar E attached to human endometrial epithelial cells. Infect. Immun. 70: 3413 3418. PubMed
40. Davis, C. H.,, and P. B. Wyrick. 1997. Differences in the association of Chlamydia trachomatis serovar E and serovar L2 with epithelial cells in vitro may reflect biological differences in vivo. Infect. Immun. 65: 2914 2924. PubMed
41. Elwell, C. A.,, A. Ceesay,, J. H. Kim,, D. Kalman,, and J. N. Engel. 2008. RNA interference screen identifies Abl kinase and PDGFR signaling in Chlamydia trachomatis entry. PLoS Pathog. 4: e1000021. PubMed CrossRef
42. Esko, J. D.,, and S. B. Selleck. 2002. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71: 435 471. PubMed CrossRef
43. Everett, K. D.,, A. A. Andersen,, M. Plaunt,, and T. P. Hatch. 1991. Cloning and sequence analysis of the major outer membrane protein gene of Chlamydia psittaci 6BC. Infect. Immun. 59: 2853 2855. PubMed
44. Everett, K. D.,, and T. P. Hatch. 1995. Architecture of the cell envelope of Chlamydia psittaci 6BC. J. Bacteriol. 177: 877 882. PubMed
45. Fadel, S.,, and A. Eley. 2007. Chlamydia trachomatis OmcB protein is a surface-exposed glycosaminoglycan-dependent adhesin. J. Med. Microbiol. 56: 15 22. PubMed CrossRef
46. Fadel, S.,, and A. Eley. 2008a. Differential glycosaminoglycan binding of Chlamydia trachomatis OmcB protein from serovars E and LGV. J. Med. Microbiol. 57: 1058 1061. PubMed CrossRef
47. Fadel, S.,, and A. Eley. 2008b. Is lipopolysaccharide a factor in infectivity of Chlamydia trachomatis? J. Med. Microbiol. 57: 261 266. PubMed CrossRef
48. Falkow, S. 1991. Bacterial entry into eukaryotic cells. Cell 65: 1099 1102. PubMed
49. Finlay, B. B.,, and S. Falkow. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61: 136 169. PubMed
50. Gerard, H. C.,, E. Fomicheva,, J. A. Whittum-Hudson,, and A. P. Hudson. 2008. Apolipoprotein E4 enhances attachment of Chlamydophila (Chlamydia) pneumoniae elementary bodies to host cells. Microb. Pathog. 44: 279 285. PubMed CrossRef
51. Gomes, J. P.,, W. J. Bruno,, A. Nunes,, N. Santos,, C. Florindo,, M. J. Borrego,, and D. Dean. 2007. Evolution of Chlamydia trachomatis diversity occurs by widespread interstrain recombination involving hotspots. Genome Res. 17: 50 60. PubMed CrossRef
52. Gomes, J. P.,, R. C. Hsia,, S. Mead,, M. J. Borrego,, and D. Dean. 2005. Immunoreactivity and differential developmental expression of known and putative Chlamydia trachomatis membrane proteins for biologically variant serovars representing distinct disease groups. Microbes Infect. 7: 410 420. PubMed CrossRef
53. Gomes, J. P.,, A. Nunes,, W. J. Bruno,, M. J. Borrego,, C. Florindo,, and D. Dean. 2006. Polymorphisms in the nine polymorphic membrane proteins of Chlamydia trachomatis across all serovars: evidence for serovar Da recombination and correlation with tissue tropism. J. Bacteriol. 188: 275 286. PubMed CrossRef
54. Gregory, W. W.,, M. Gardner,, G. I. Byrne,, and J. W. Moulder. 1979. Arrays of hemispheric surface projections on Chlamydia psittaci and Chlamydia trachomatis observed by scanning electron microscopy. J. Bacteriol. 138: 241 244. PubMed
55. Grimwood, J.,, L. Olinger,, and R. S. Stephens. 2001. Expression of Chlamydia pneumoniae polymorphic membrane protein family genes. Infect. Immun. 69: 2383 2389. PubMed CrossRef
56. Grimwood, J.,, and R. S. Stephens. 1999. Computational analysis of the polymorphic membrane protein superfamily of Chlamydia trachomatis and Chlamydia pneumoniae. Microb. Comp. Genomics 4: 187 201. PubMed
57. Gutierrez-Martin, C. B.,, D. M. Ojcius,, R. C. Hsia,, R. Hellio,, P. M. Bavoil,, and A. Dautry-Varsat. 1997. Heparin mediated inhibition of Chlamydia psittaci adherence to HeLa cells. Microb. Pathog. 22: 47 57. PubMed
58. Hackstadt, T., 1999. Cell biology, p. 101 138. In R. S. Stephens (ed.), Chlamydia: Intracellular Biology, Pathogenesis, and Immunity. ASM Press, Washington, DC.
59. Hackstadt, T.,, W. J. Todd,, and H. D. Caldwell. 1985. Disulfide-mediated interactions of the chlamydial major outer membrane protein: role in the differentiation of chlamydiae? J. Bacteriol. 161: 25 31. PubMed
60. Hall, J. V.,, M. Schell,, S. Dessus-Babus,, C. G. Moore,, J. D. Whittimore,, M. Sal,, B. D. Dill,, and P. B. Wyrick. 2011. The multifaceted role of oestrogen in enhancing Chlamydia trachomatis infection in polarized human endometrial epithelial cells. Cell. Microbiol. 13: 1183 1199. PubMed CrossRef
61. Hatch, T. P. 1996. Disulfide cross-linked envelope proteins: the functional equivalent of peptidoglycan in chlamydiae? J. Bacteriol. 178: 1 5. PubMed
62. Hatch, T. P., 1999. Developmental biology, p. 26 67. In R. S. Stephens (ed.), Chlamydia: Intracellular Biology, Pathogenesis, and Immunity. ASM Press, Washington, DC.
63. Hatch, T. P.,, I. Allan,, and J. H. Pearce. 1984. Structural and polypeptide differences between envelopes of infective and reproductive life cycle forms of Chlamydia spp. J. Bacteriol. 157: 13 20. PubMed
64. Hatch, T. P.,, M. Miceli,, and J. E. Sublett. 1986. Synthesis of disulfide-bonded outer membrane proteins during the developmental cycle of Chlamydia psittaci and Chlamydia trachomatis. J. Bacteriol. 165: 379 385. PubMed
65. Henderson, I. R.,, and A. C. Lam. 2001. Polymorphic proteins of Chlamydia spp.—autotransporters beyond the Proteobacteria. Trends Microbiol. 9: 573 578. PubMed
66. Henderson, I. R.,, and J. P. Nataro. 2001. Virulence functions of autotransporter proteins. Infect. Immun. 69: 1231 1243. PubMed CrossRef
67. Henderson, I. R.,, F. Navarro-Garcia,, M. Desvaux,, R. C. Fernandez,, and D. Ala’Aldeen. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68: 692 744. PubMed CrossRef
68. Hileman, R. E.,, J. R. Fromm,, J. M. Weiler,, and R. J. Linhardt. 1998. Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. Bioessays 20: 156 167. PubMed CrossRef
69. Junker, M.,, C. C. Schuster,, A. V. McDonnell,, K. A. Sorg,, M. C. Finn,, B. Berger,, and P. L. Clark. 2006. Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc. Natl. Acad. Sci. USA 103: 4918 4923. PubMed CrossRef
70. Kalman, S.,, W. Mitchell,, R. Marathe,, C. Lammel,, J. Fan,, R. W. Hyman,, L. Olinger,, J. Grimwood,, R. W. Davis,, and R. S. Stephens. 1999. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat. Genet. 21: 385 389. PubMed CrossRef
71. Kiselev, A. O.,, M. C. Skinner,, and M. F. Lampe. 2009. Analysis of PmpD expression and PmpD post-translational processing during the life cycle of Chlamydia trachomatis serovars A, D, and L2. PLoS One 4: e5191. PubMed CrossRef
72. Kiselev, A. O.,, W. E. Stamm,, J. R. Yates,, and M. F. Lampe. 2007. Expression, processing, and localization of PmpD of Chlamydia trachomatis serovar L2 during the chlamydial developmental cycle. PLoS ONE 2: e568. PubMed CrossRef
73. Klein, M.,, A. Kotz,, K. Bernardo,, and M. Kronke. 2003. Detection of Chlamydia pneumoniae-specific antibodies binding to the VD2 and VD3 regions of the major outer membrane protein. J. Clin. Microbiol. 41: 1957 1962. PubMed CrossRef
74. Kline, K. A.,, S. Falker,, S. Dahlberg,, S. Normark,, and B. Henriques-Normark. 2009. Bacterial adhesins in host-microbe interactions. Cell Host Microbe 5: 580 592. PubMed CrossRef
75. Knudsen, K.,, A. S. Madsen,, P. Mygind,, G. Christiansen,, and S. Birkelund. 1999. Identification of two novel genes encoding 97- to 99-kilodalton outer membrane proteins of Chlamydia pneumoniae. Infect. Immun. 67: 375 383. PubMed
76. Kraaipoel, R. J.,, and A. M. van Duin. 1979. Isoelectric focusing of Chlamydia trachomatis. Infect. Immun. 26: 775 778. PubMed
77. Kubo, A.,, and R. S. Stephens. 2000. Characterization and functional analysis of PorB, a Chlamydia porin and neutralizing target. Mol. Microbiol. 38: 772 780. PubMed CrossRef
78. Kuo, C. C.,, and T. Grayston. 1976. Interaction of Chlamydia trachomatis organisms and HeLa 229 cells. Infect. Immun. 13: 1103 1109. PubMed
79. Kuo, C. C.,, A. Lee,, and L. A. Campbell. 2004. Cleavage of the N-linked oligosaccharide from the surface of Chlamydia species affects attachment and infectivity of the organism in human epithelial and endothelial cells. Infect. Immun. 72: 6699 6701. PubMed CrossRef
80. Kuo, C. C.,, S. P. Wang,, and J. T. Grayston. 1973. Effect of polycations, polyanions and neuraminidase on the infectivity of trachoma-inclusion conjunctivitis and lymphogranuloma venereum organisms HeLa cells: sialic acid residues as possible receptors for trachoma-inclusion conjunction. Infect. Immun. 8: 74 79. PubMed
81. Liu, X.,, M. Afrane,, D. E. Clemmer,, G. Zhong,, and D. E. Nelson. 2010. Identification of Chlamydia trachomatis outer membrane complex proteins by differential proteomics. J. Bacteriol. 192: 2852 2860. PubMed CrossRef
82. Longbottom, D.,, J. Findlay,, E. Vretou,, and S. M. Dunbar. 1998a. Immunoelectron microscopic localisation of the OMP90 family on the outer membrane surface of Chlamydia psittaci. FEMS Microbiol. Lett. 164: 111 117. PubMed
83. Longbottom, D.,, M. Russell,, S. M. Dunbar,, G. E. Jones,, and A. J. Herring. 1998b. Molecular cloning and characterization of the genes coding for the highly immunogenic cluster of 90-kilodalton envelope proteins from the Chlamydia psittaci subtype that causes abortion in sheep. Infect. Immun. 66: 1317 1324. PubMed
84. Longbottom, D.,, M. Russell,, G. E. Jones,, F. A. Lainson,, and A. J. Herring. 1996. Identification of a multigene family coding for the 90 kDa proteins of the ovine abortion subtype of Chlamydia psittaci. FEMS Microbiol. Lett. 142: 277 281. PubMed
85. Maslow, A. S.,, C. H. Davis,, J. Choong,, and P. B. Wyrick. 1988. Estrogen enhances attachment of Chlamydia trachomatis to human endometrial epithelial cells in vitro. Am. J. Obstet. Gynecol. 159: 1006 1014. PubMed
86. Matsumoto, A. 1982. Surface projections of Chlamydia psittaci elementary bodies as revealed by freeze-deep-etching. J. Bacteriol. 151: 1040 1042. PubMed
87. Mazar, J.,, and P. A. Cotter. 2006. Topology and maturation of filamentous haemagglutinin suggest a new model for two-partner secretion. Mol. Microbiol. 62: 641 654. PubMed CrossRef
88. Menozzi, F. D.,, K. Pethe,, P. Bifani,, F. Soncin,, M. J. Brennan,, and C. Locht. 2002. Enhanced bacterial virulence through exploitation of host glycosaminoglycans. Mol. Microbiol. 43: 1379 1386. PubMed CrossRef
89. Mitchell, C. M.,, K. M. Hovis,, P. M. Bavoil,, G. S. Myers,, J. A. Carrasco,, and P. Timms. 2010. Comparison of koala LPCoLN and human strains of Chlamydia pneumoniae highlights extended genetic diversity in the species. BMC Genomics 11: 442. PubMed CrossRef
90. Moelleken, K.,, and J. H. Hegemann. 2008. The Chlamydia outer membrane protein OmcB is required for adhesion and exhibits biovar-specific differences in glycosaminoglycan binding. Mol. Microbiol. 67: 403 419. PubMed CrossRef
91. Moelleken, K.,, E. Schmidt,, and J. H. Hegemann. 2010. Members of the Pmp protein family of Chlamydia pneumoniae mediate adhesion to human cells via short repetitive peptide motifs. Mol. Microbiol. 78: 1004 1017. PubMed CrossRef
92. Montigiani, S.,, F. Falugi,, M. Scarselli,, O. Finco,, R. Petracca,, G. Galli,, M. Mariani,, R. Manetti,, M. Agnusdei,, R. Cevenini,, M. Donati,, R. Nogarotto,, N. Norais,, I. Garaguso,, S. Nuti,, G. Saletti,, D. Rosa,, G. Ratti,, and G. Grandi. 2002. Genomic approach for analysis of surface proteins in Chlamydia pneumoniae. Infect. Immun. 70: 368 379. PubMed
93. Myers, G. S.,, S. A. Mathews,, M. Eppinger,, C. Mitchell,, K. K. O’Brien,, O. R. White,, F. Benahmed,, R. C. Brunham,, T. D. Read,, J. Ravel,, P. M. Bavoil,, and P. Timms. 2009. Evidence that human Chlamydia pneumoniae was zoonotically acquired. J. Bacteriol. 191: 7225 7233. PubMed CrossRef
94. Mygind, P.,, G. Christiansen,, and S. Birkelund. 1998a. Topological analysis of Chlamydia trachomatis L2 outer membrane protein 2. J. Bacteriol. 180: 5784 5787. PubMed
95. Mygind, P.,, G. Christiansen,, K. Persson,, and S. Birkelund. 1998b. Analysis of the humoral immune response to Chlamydia outer membrane protein 2. Clin. Diagn. Lab. Immunol. 5: 313 318. PubMed
96. Mygind, P. H.,, G. Christiansen,, P. Roepstorff,, and S. Birkelund. 2000. Membrane proteins PmpG and PmpH are major constituents of Chlamydia trachomatis L2 outer membrane complex. FEMS Microbiol. Lett. 186: 163 169. PubMed
97. Niessner, A.,, C. Kaun,, G. Zorn,, W. Speidl,, Z. Turel,, G. Christiansen,, A. S. Pedersen,, S. Birkelund,, S. Simon,, A. Georgopoulos,, W. Graninger,, R. de Martin,, J. Lipp,, B. R. Binder,, G. Maurer,, K. Huber,, and J. Wojta. 2003. Polymorphic membrane protein (PMP) 20 and PMP 21 of Chlamydia pneumoniae induce proinflammatory mediators in human endothelial cells in vitro by activation of the nuclear factor-kappaB pathway. J. Infect. Dis. 188: 108 113. PubMed CrossRef
98. Nobbs, A. H.,, R. J. Lamont,, and H. F. Jenkinson. 2009. Streptococcus adherence and colonization. Microbiol. Mol. Biol. Rev. 73: 407 450. PubMed CrossRef
99. Nunes, A.,, J. P. Gomes,, S. Mead,, C. Florindo,, H. Correia,, M. J. Borrego,, and D. Dean. 2007. Comparative expression profiling of the Chlamydia trachomatis pmp gene family for clinical and reference strains. PLoS ONE 2: e878. PubMed CrossRef
100. Pedersen, A. S.,, G. Christiansen,, and S. Birkelund. 2001. Differential expression of Pmp10 in cell culture infected with Chlamydia pneumoniae CWL029. FEMS Microbiol. Lett. 203: 153 159. PubMed
101. Peterson, E. M.,, L. M. de la Maza,, L. Brade,, and H. Brade. 1998. Characterization of a neutralizing monoclonal antibody directed at the lipopolysaccharide of Chlamydia pneumoniae. Infect. Immun. 66: 3848 3855. PubMed
102. Pizarro-Cerda, J.,, and P. Cossart. 2006. Bacterial adhesion and entry into host cells. Cell 124: 715 727. PubMed CrossRef
103. Portig, I.,, J. C. Goodall,, R. L. Bailey,, and J. S. Gaston. 2003. Characterization of the humoral immune response to Chlamydia outer membrane protein 2 in chlamydial infection. Clin. Diagn. Lab. Immunol. 10: 103 107. PubMed CrossRef
104. Puolakkainen, M.,, C. C. Kuo,, and L. A. Campbell. 2005. Chlamydia pneumoniae uses the mannose 6-phosphate/insulin-like growth factor 2 receptor for infection of endothelial cells. Infect. Immun. 73: 4620 4625. PubMed CrossRef
105. Puolakkainen, M.,, A. Lee,, T. Nosaka,, H. Fukushi,, C. C. Kuo,, and L. A. Campbell. 2008. Retinoic acid inhibits the infectivity and growth of Chlamydia pneumoniae in epithelial and endothelial cells through different receptors. Microb. Pathog. 44: 410 416. PubMed CrossRef
106. Raulston, J. E. 1995. Chlamydial envelope components and pathogen-host cell interactions. Mol. Microbiol. 15: 607 616. PubMed CrossRef
107. Read, T. D.,, G. S. Myers,, R. C. Brunham,, W. C. Nelson,, I. T. Paulsen,, J. Heidelberg,, E. Holtzapple,, H. Khouri,, N. B. Federova,, H. A. Carty,, L. A. Umayam,, D. H. Haft,, J. Peterson,, M. J. Beanan,, O. White,, S. L. Salzberg,, R. C. Hsia,, G. McClarty,, R. G. Rank,, P. M. Bavoil,, and C. M. Fraser. 2003. Genome sequence of Chlamydophila caviae ( Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. Nucleic Acids Res. 31: 2134 2147. PubMed CrossRef
108. Rockey, D. D.,, J. Lenart,, and R. S. Stephens. 2000. Genome sequencing and our understanding of chlamydiae. Infect. Immun. 68: 5473 5479. PubMed CrossRef
109. Rostand, K. S.,, and J. D. Esko. 1997. Microbial adherence to and invasion through proteoglycans. Infect. Immun. 65: 1 8. PubMed
110. Schroeder, T. H.,, M. M. Lee,, P. W. Yacono,, C. L. Cannon,, A. A. Gerceker,, D. E. Golan,, and G. B. Pier. 2002. CFTR is a pattern recognition molecule that extracts Pseudomonas aeruginosa LPS from the outer membrane into epithelial cells and activates NF-kappa B translocation. Proc. Natl. Acad. Sci. USA 99: 6907 6912. PubMed CrossRef
111. Shaw, A. C.,, K. Gevaert,, H. Demol,, B. Hoorelbeke,, J. Vandekerckhove,, M. R. Larsen,, P. Roepstorff,, A. Holm,, G. Christiansen,, and S. Birkelund. 2002. Comparative proteome analysis of Chlamydia trachomatis serovar A, D and L2. Proteomics 2: 164 186. PubMed
112. Shirai, M.,, H. Hirakawa,, K. Ouchi,, M. Tabuchi,, F. Kishi,, M. Kimoto,, H. Takeuchi,, J. Nishida,, K. Shibata,, R. Fujinaga,, H. Yoneda,, H. Matsushima,, C. Tanaka,, S. Furukawa,, K. Miura,, A. Nakazawa,, K. Ishii,, T. Shiba,, M. Hattori,, S. Kuhara,, and T. Nakazawa. 2000. Comparison of outer membrane protein genes omp and pmp in the whole genome sequences of Chlamydia pneumoniae isolates from Japan and the United States. J. Infect. Dis. 181( Suppl. 3): S524 S527. PubMed CrossRef
113. Skipp, P.,, J. Robinson,, C. D. O’Connor,, and I. N. Clarke. 2005. Shotgun proteomic analysis of Chlamydia trachomatis. Proteomics 5: 1558 1573. PubMed CrossRef
114. Soderlund, G.,, and E. Kihlstrom. 1982. Physicochemical surface properties of elementary bodies from different serotypes of Chlamydia trachomatis and their interaction with mouse fibroblasts. Infect. Immun. 36: 893 899. PubMed
115. Soriani, M.,, P. Petit,, R. Grifantini,, R. Petracca,, G. Gancitano,, E. Frigimelica,, F. Nardelli,, C. Garcia,, S. Spinelli,, G. Scarabelli,, S. Fiorucci,, R. Affentranger,, M. Ferrer-Navarro,, M. Zacharias,, G. Colombo,, L. Vuillard,, X. Daura,, and G. Grandi. 2010. Exploiting antigenic diversity for vaccine design: the Chlamydia ArtJ paradigm. J. Biol. Chem. 285: 30126 30138. PubMed CrossRef
116. Stephens, R. S.,, S. Kalman,, C. Lammel,, J. Fan,, R. Marathe,, L. Aravind,, W. Mitchell,, L. Olinger,, R. L. Tatusov,, Q. Zhao,, E. V. Koonin,, and R. W. Davis. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282: 754 759. PubMed CrossRef
117. Stephens, R. S.,, K. Koshiyama,, E. Lewis,, and A. Kubo. 2001. Heparin-binding outer membrane protein of chlamydiae. Mol. Microbiol. 40: 691 699. PubMed CrossRef
118. Su, H.,, L. Raymond,, D. D. Rockey,, E. Fischer,, T. Hackstadt,, and H. D. Caldwell. 1996. A recombinant Chlamydia trachomatis major outer membrane protein binds to heparan sulfate receptors on epithelial cells. Proc. Natl. Acad. Sci. USA 93: 11143 11148. PubMed
119. Su, H.,, N. G. Watkins,, Y. X. Zhang,, and H. D. Caldwell. 1990. Chlamydia trachomatis-host cell interactions: role of the chlamydial major outer membrane protein as an adhesin. Infect. Immun. 58: 1017 1025. PubMed
120. Swanson, A. F.,, R. A. Ezekowitz,, A. Lee,, and C. C. Kuo. 1998. Human mannose-binding protein inhibits infection of HeLa cells by Chlamydia trachomatis. Infect. Immun. 66: 1607 1612. PubMed
121. Swanson, A. F.,, and C. C. Kuo. 1994. Binding of the glycan of the major outer membrane protein of Chlamydia trachomatis to HeLa cells. Infect. Immun. 62: 24 28. PubMed
122. Swanson, K. A.,, L. D. Taylor,, S. D. Frank,, G. L. Sturdevant,, E. R. Fischer,, J. H. Carlson,, W. M. Whitmire,, and H. D. Caldwell. 2009. Chlamydia trachomatis polymorphic membrane protein D is an oligomeric autotransporter with a higher-order structure. Infect. Immun. 77: 508 516. PubMed CrossRef
123. Tan, C.,, R. C. Hsia,, H. Shou,, J. A. Carrasco,, R. G. Rank,, and P. M. Bavoil. 2010. Variable expression of surface-exposed polymorphic membrane proteins in in vitro-grown Chlamydia trachomatis. Cell. Microbiol. 12: 174 187. PubMed CrossRef
124. Tan, C.,, R. C. Hsia,, H. Shou,, C. L. Haggerty,, R. B. Ness,, C. A. Gaydos,, D. Dean,, A. M. Scurlock,, D. P. Wilson,, and P. M. Bavoil. 2009. Chlamydia trachomatis-infected patients display variable antibody profiles against the nine-member polymorphic membrane protein family. Infect. Immun. 77: 3218 3226. PubMed CrossRef
125. Tan, C.,, J. K. Spitznagel,, H.-Z. Shou,, R.-C. Hsia,, and P. M. Bavoil,. 2006. The polymorphic membrane protein gene family of the Chlamydiaceae, p. 195 218. In P. M. Bavoil, and P. B. Wyrick (ed.), Chlamydia Genomics and Pathogenesis. Horizon Bioscience, Norfolk, United Kingdom.
126. Tanzer, R. J.,, and T. P. Hatch. 2001. Characterization of outer membrane proteins in Chlamydia trachomatis LGV serovar L2. J. Bacteriol. 183: 2686 2690. PubMed CrossRef
127. Tanzer, R. J.,, D. Longbottom,, and T. P. Hatch. 2001. Identification of polymorphic outer membrane proteins of Chlamydia psittaci 6BC. Infect. Immun. 69: 2428 2434. PubMed CrossRef
128. Taraktchoglou, M.,, A. A. Pacey,, J. E. Turnbull,, and A. Eley. 2001. Infectivity of Chlamydia trachomatis serovar LGV but not E is dependent on host cell heparan sulfate. Infect. Immun. 69: 968 976. PubMed CrossRef
129. Ting, L. M.,, R. C. Hsia,, C. G. Haidaris,, and P. M. Bavoil. 1995. Interaction of outer envelope proteins of Chlamydia psittaci GPIC with the HeLa cell surface. Infect. Immun. 63: 3600 3608. PubMed
130. Turnbull, J. E. 2010. Heparan sulfate glycomics: towards systems biology strategies. Biochem. Soc. Trans. 38: 1356 1360. PubMed CrossRef
131. Turnbull, J. E.,, R. L. Miller,, Y. Ahmed,, T. M. Puvirajesinghe,, and S. E. Guimond. 2010. Glycomics profiling of heparan sulfate structure and activity. Methods Enzymol. 480: 65 85. PubMed CrossRef
132. Ulanova, M.,, S. Gravelle,, and R. Barnes. 2008. The role of epithelial integrin receptors in recognition of pulmonary pathogens. J. Innate Immun. 1: 4 17. PubMed CrossRef
133. Vance, D. W., Jr.,, and T. P. Hatch. 1980. Surface properties of Chlamydia psittaci. Infect. Immun. 29: 175 180. PubMed
134. Vandahl, B. B.,, S. Birkelund,, H. Demol,, B. Hoorelbeke,, G. Christiansen,, J. Vandekerckhove,, and K. Gevaert. 2001. Proteome analysis of the Chlamydia pneumoniae elementary body. Electrophoresis 22: 1204 1223. PubMed CrossRef
135. Vandahl, B. B.,, A. S. Pedersen,, K. Gevaert,, A. Holm,, J. Vandekerckhove,, G. Christiansen,, and S. Birkelund. 2002. T he expression, processing and localization of polymorphic membrane proteins in Chlamydia pneumoniae strain CWL029. BMC Microbiol. 2: 36. PubMed CrossRef
136. Vretou, E.,, P. C. Goswami,, and S. K. Bose. 1989. Adherence of multiple serovars of Chlamydia trachomatis to a common receptor on HeLa and McCoy cells is mediated by thermolabile protein(s). J. Gen. Microbiol. 135: 3229 3237. PubMed CrossRef
137. Wadstrom, T.,, and A. Ljungh. 1999. Glycosaminoglycan-binding microbial proteins in tissue adhesion and invasion: key events in microbial pathogenicity. J. Med. Microbiol. 48: 223 233. PubMed CrossRef
138. Wagels, G.,, S. Rasmussen,, and P. Timms. 1994. Comparison of Chlamydia pneumoniae isolates by Western blot (immunoblot) analysis and DNA sequencing of the omp2 gene. J. Clin. Microbiol. 32: 2820 2823. PubMed
139. Wang, A.,, S. C. Johnston,, J. Chou,, and D. Dean. 2010. A systemic network for Chlamydia pneumoniae entry into human cells. J. Bacteriol. 192: 2809 2815. PubMed CrossRef
140. Watson, M. W.,, P. R. Lambden,, J. S. Everson,, and I. N. Clarke. 1994. Immunoreactivity of the 60 kDa cysteine-rich proteins of Chlamydia trachomatis, Chlamydia psittaci and Chlamydia pneumoniae expressed in Escherichia coli. Microbiology 140: 2003 2011. PubMed CrossRef
141. Wehrl, W.,, V. Brinkmann,, P. R. Jungblut,, T. F. Meyer,, and A. J. Szczepek. 2004. From the inside out—processing of the chlamydial autotransporter PmpD and its role in bacterial adhesion and activation of human host cells. Mol. Microbiol. 51: 319 334. PubMed CrossRef
142. Wells, T. J.,, M. Totsika,, and M. A. Schembri. 2010. Autotransporters of Escherichia coli: a sequence-based characterization. Microbiology 156: 2459 2469. PubMed CrossRef
143. Wells, T. J.,, J. J. Tree,, G. C. Ulett,, and M. A. Schembri. 2007. Autotransporter proteins: novel targets at the bacterial cell surface. FEMS Microbiol. Lett. 274: 163 172. PubMed CrossRef
144. Wuppermann, F. N.,, J. H. Hegemann,, and C. A. Jantos. 2001. Heparan sulfate-like glycosaminoglycan is a cellular receptor for Chlamydia pneumoniae. J. Infect. Dis. 184: 181 187. PubMed CrossRef
145. Wuppermann, F. N.,, K. Moelleken,, M. Julien,, C. A. Jantos,, and J. H. Hegemann. 2008. Chlamydia pneumoniae GroEL1 protein is cell surface associated and required for infection of HEp-2 cells. J. Bacteriol. 190: 3757 3767. PubMed CrossRef
146. Wyllie, S.,, R. H. Ashley,, D. Longbottom,, and A. J. Herring. 1998. The major outer membrane protein of Chlamydia psittaci functions as a porin-like ion channel. Infect. Immun. 66: 5202 5207. PubMed
147. Wyrick, P. B.,, J. Choong,, C. H. Davis,, S. T. Knight,, M. O. Royal,, A. S. Maslow,, and C. R. Bagnell. 1989. Entry of genital Chlamydia trachomatis into polarized human epithelial cells. Infect. Immun. 57: 2378 2389. PubMed
148. Yabushita, H.,, Y. Noguchi,, H. Habuchi,, S. Ashikari,, K. Nakabe,, M. Fujita,, M. Noguchi,, J. D. Esko,, and K. Kimata. 2002. Effects of chemically modified heparin on Chlamydia trachomatis serovar L2 infection of eukaryotic cells in culture. Glycobiology 12: 345 351. PubMed CrossRef
149. Yan, Y.,, S. Silvennoinen-Kassinen,, M. Leinonen,, and P. Saikku. 2006. Inhibitory effect of heparan sulfate-like glycosaminoglycans on the infectivity of Chlamydia pneumoniae in HL cells varies between strains. Microbes Infect. 8: 866 872. PubMed CrossRef
150. Zaretzky, F. R.,, R. Pearce-Pratt,, and D. M. Phillips. 1995. Sulfated polyanions block Chlamydia trachomatis infection of cervix-derived human epithelia. Infect. Immun. 63: 3520 3526. PubMed
151. Zhang, J. P.,, and R. S. Stephens. 1992. Mechanism of C. trachomatis attachment to eukaryotic host cells. Cell 69: 861 869. PubMed CrossRef


Generic image for table

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

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

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

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error