The Chlamydial Cell Envelope

David E. Nelson

doi:10.1128/9781555817329.ch4

Chapter 4 : The Chlamydial Cell Envelope

Author: David E. Nelson¹

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Affiliations: 1: Department of Biology, Indiana University, Bloomington, IN 47405

Content Type: Monograph

Publication Year: 2012

Category: Bacterial Pathogenesis

Book DOI: 10.1128/9781555817329

Chapter DOI: 10.1128/9781555817329.ch4

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The Chlamydial Cell Envelope, Page 1 of 2

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Abstract:

Chlamydial development is punctuated by changes in protein-protein interactions on elementary body (EB) and reticulate body (RB) surfaces. Reduction of disulfide cross-links in the chlamydial outer membrane complex (COMC) concomitant with attachment and entry of the EB is rapidly followed by transition to the fragile RB, which is specialized for acquisition of nutrients during chlamydial growth and differentiation. This chapter reviews knowledge about the progression starting with the structure of the EB envelope in the extracellular environment and the way in which this surface interacts with, and is altered during, the process of chlamydial attachment, entry, development, and exit from host cells. The presence of gram-negative double membranes was confirmed by early transmission electron microscopy (TEM) studies of RBs and EBs, but challenges in purification and fractionation of RB membranes shifted emphasis toward EB membranes in subsequent studies. Regularly spaced hexagonal lattices were observed in negatively stained EB envelope preparations. Hexagonal lattices, located between the outer and cytoplasmic EB membranes, and similar structures were present in multiple Chlamydia species. Varying degrees of evidence suggest that additional EB OMPs may exist. The envelopes of the extracellular EB and intracellular RB differ markedly and reflect requirements for survival of chlamydiae in two unique environments. Outside the cell, the oxidized COMC provides osmotic protection, restricts loss of metabolites across the OM, and may mask immunogenic determinants that could alert host cells to the presence of these pathogens.

Citation: Nelson D. 2012. The Chlamydial Cell Envelope, p 74-96. In Tan M, Bavoil P (ed), Intracellular Pathogens I: Chlamydiales. ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch4

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The Chlamydial Cell Envelope

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Citation: Nelson D. 2012. The Chlamydial Cell Envelope, p 74-96. In Tan M, Bavoil P (ed), Intracellular Pathogens I: Chlamydiales. ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch4

/content/10.1128/9781555817329.chap4.fig4-1

FIGURE 1

Model of the EB surface. OmcB (dumbbells) and OmcA (triangles) are located primarily in the periplasm. LPS (small gray hexagons) is primarily located in the outer leaflet of the outer membrane, while phospholipids are in the inner leaflet (small open circles). OmcA is associated with the inner leaflet of the OM by its lipid moiety (not shown). An N-terminal portion of some OmcB molecules may traverse the OM and bind HS on the EB surface (chains of open hexagons). HS may also bind unknown residues on MOMP. OmcA and OmcB are cysteine cross-linked to one another in the periplasm, and, speculatively, to other OMPs such as CdsC, PorB, and some Pmps (PmpH and hypothetical PmpX). The figure shows a range of scenarios that may occur for specific Pmps. For example, the passenger domain (shown as ovals for each of the Pmps) of PmpH has been exported to the EB surface, whereas export of the passenger domain of PmpX has not been completed. Export of the hypothetical PmpZ passenger domain has been completed, but its transporter domain is not bound to other COMC proteins. Oligomers of PmpD, which have been processed from their passenger domains, are loosely associated with the surface of the EB. Polymers of the putative T3S needle protein CdsF extend from CdsC. doi:10.1128/9781555817329.ch4.f1

10.1128/9781555817329/fig4-1_thmb.gif

10.1128/9781555817329/fig4-1.gif

FIGURE 1

Citation: Nelson D. 2012. The Chlamydial Cell Envelope, p 74-96. In Tan M, Bavoil P (ed), Intracellular Pathogens I: Chlamydiales. ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch4

References

/content/book/10.1128/9781555817329.chap4

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. Allan, I.,, T. P. Hatch,, and J. H. Pearce. 1985. Influence of cysteine deprivation on chlamydial differentiation from reproductive to infective life-cycle forms. J. Gen. Microbiol. 131:3171–3177. PubMed CrossRef

3. Allen, J. E.,, M. C. Cerrone,, P. R. Beatty,, and R. S. Stephens. 1990. Cysteine-rich outer membrane proteins of Chlamydia trachomatis display compensatory sequence changes between biovariants. Mol. Microbiol. 4:1543–1550. PubMed

4. Barbour, A. G.,, K. Amano,, T. Hackstadt,, L. Perry,, and H. D. Caldwell. 1982. Chlamydia trachomatis has penicillin-binding proteins but not detectable muramic acid. J. Bacteriol. 151:420–428. PubMed

5. Barry, C. E., III,, S. F. Hayes,, and T. Hackstadt. 1992. Nucleoid condensation in Escherichia coli that express a chlamydial histone homolog. Science 256:377–379. 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. Beatty, W. L. 2006. Trafficking from CD63-positive late endocytic multivesicular bodies is essential for intracellular development of Chlamydia trachomatis. J. Cell Sci. 119:350–359. PubMed CrossRef

9. Beatty, W. L. 2008. Late endocytic multivesicular bodies intersect the chlamydial inclusion in the absence of CD63. Infect. Immun. 76:2872–2881. PubMed CrossRef

10. 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

11. Belland, R. J.,, D. E. Nelson,, D. Virok,, D. D. Crane,, D. Hogan,, D. Sturdevant,, W. L. Beatty,, and H. D. Caldwell. 2003a. Transcriptome analysis of chlamydial growth during IFN-gamma-mediated persistence and reactivation. Proc. Natl. Acad. Sci. USA 100:15971–15976. PubMed CrossRef

12. Belland, R. J.,, G. Zhong,, D. D. Crane,, D. Hogan,, D. Sturdevant,, J. Sharma,, W. L. Beatty,, and H. D. Caldwell. 2003b. Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc. Natl. Acad. Sci. USA 100:8478–8483. PubMed CrossRef

13. Belunis, C. J.,, K. E. Mdluli,, C. R. Raetz,, and F. E. Nano. 1992. A novel 3-deoxy-D-manno-octulosonic acid transferase from Chlamydia trachomatis required for expression of the genus-specific epitope. J. Biol. Chem. 267:18702–18707. PubMed

14. Betts, H. J.,, L. E. Twiggs,, M. S. Sal,, P. B. Wyrick,, and K. A. Fields. 2008. Bioinformatic and biochemical evidence for the identification of the type III secretion system needle protein of Chlamydia trachomatis. J. Bacteriol. 190:1680–1690. PubMed CrossRef

15. Birkelund, S.,, A. G. Lundemose,, and G. Christiansen. 1988. Chemical cross-linking of Chlamydia trachomatis. Infect. Immun. 56:654–659. PubMed

16. Birkelund, S.,, A. G. Lundemose,, and G. Christiansen. 1989. Immunoelectron microscopy of lipopolysaccharide in Chlamydia trachomatis. Infect. Immun. 57:3250–3253. PubMed

17. 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

18. Brade, H.,, L. Brade,, and F. E. Nano. 1987. Chemical and serological investigations on the genus-specific lipopolysaccharide epitope of Chlamydia. Proc. Natl. Acad. Sci. USA 84:2508–2512. PubMed

19. Brade, L.,, O. Holst,, P. Kosma,, Y. X. Zhang,, H. Paulsen,, R. Krausse,, and H. Brade. 1990. Characterization of murine monoclonal and murine, rabbit, and human polyclonal antibodies against chlamydial lipopolysaccharide. Infect. Immun. 58:205–213. PubMed

20. Brade, L.,, M. Nurminen,, P. H. Makela,, and H. Brade. 1985. Antigenic properties of Chlamydia trachomatis lipopolysaccharide. Infect. Immun. 48:569–572. PubMed

21. Brown, W. J.,, and D. D. Rockey. 2000. Identification of an antigen localized to an apparent septum within dividing chlamydiae. Infect. Immun. 68:708–715. PubMed CrossRef

22. Buendia, A. J.,, J. Salinas,, J. Sanchez,, M. C. Gallego,, A. Rodolakis,, and F. Cuello. 1997. Localization by immunoelectron microscopy of antigens of Chlamydia psittaci suitable for diagnosis or vaccine development. FEMS Microbiol. Lett. 150:113–119. PubMed

23. Caldwell, H. D.,, and P. J. Hitchcock. 1984. Monoclonal antibody against a genus-specific antigen of Chlamydia species: location of the epitope on chlamydial lipopolysaccharide. Infect. Immun. 44:306–314. PubMed

24. Caldwell, H. D.,, and R. C. Judd. 1982. Structural analysis of chlamydial major outer membrane proteins. Infect. Immun. 38:960–968. PubMed

25. 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

26. Caldwell, H. D.,, and C. C. Kuo. 1977a. Purification of a Chlamydia trachomatis-specific antigen by immunoadsorption with monospecific antibody. J. Immunol. 118:437–441. PubMed

27. Caldwell, H. D.,, and C. C. Kuo. 1977b. Serologic diagnosis of lymphogranuloma venereum by counterimmunoelectrophoresis with a Chlamydia trachomatis protein antigen. J. Immunol. 118:442–445. PubMed

28. Caldwell, H. D.,, C. C. Kuo,, and G. E. Kenny. 1975a. Antigenic analysis of Chlamydiae by two-dimensional immunoelectrophoresis. I. Antigenic heterogeneity between C. trachomatis and C. psittaci. J. Immunol. 115:963–968. PubMed

29. Caldwell, H. D.,, C. C. Kuo,, and G. E. Kenny. 1975b. Antigenic analysis of chlamydiae by two-dimensional immunoelectrophoresis. II. A trachoma-LGV-specific antigen. J. Immunol. 115:969–975. PubMed

30. Caldwell, H. D.,, and L. J. Perry. 1982. Neutralization of Chlamydia trachomatis infectivity with antibodies to the major outer membrane protein. Infect. Immun. 38:745–754. PubMed

31. Campbell, L. A.,, C. C. Kuo,, and J. T. Grayston. 1990. Structural and antigenic analysis of Chlamydia pneumoniae. Infect. Immun. 58:93–97. PubMed

32. Campbell, L. A.,, C. C. Kuo,, R. W. Thissen,, and J. T. Grayston. 1989. Isolation of a gene encoding a Chlamydia sp. strain TWAR protein that is recognized during infection of humans. Infect. Immun. 57:71–75. PubMed

33. 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

34. Carabeo, R. A.,, D. J. Mead,, and T. Hackstadt. 2003. Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc. Natl. Acad. Sci. USA 100:6771–6776. PubMed CrossRef

35. Carlson, J. H.,, S. F. Porcella,, G. McClarty,, and H. D. Caldwell. 2005. Comparative genomic analysis of Chlamydia trachomatis oculotropic and genitotropic strains. Infect. Immun. 73:6407–6418. PubMed CrossRef

36. 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

37. 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

38. Cevenini, R.,, A. Moroni,, V. Sambri,, S. Perini,, and M. La Placa. 1989. Serological response to chlamydial infection in sheep, studied by enzyme-linked immunosorbent assay and immunoblotting. FEMS Microbiol. Immunol. 1:459–464. PubMed

39. 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 CrossRef

40. 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

41. Clarke, I. N.,, M. E. Ward,, and P. R. Lambden. 1988. Molecular cloning and sequence analysis of a developmentally regulated cysteine-rich outer membrane protein from Chlamydia trachomatis. Gene 71:307–314. PubMed

42. Clifton, D. R.,, K. A. Fields,, S. S. Grieshaber,, C. A. Dooley,, E. R. Fischer,, D. J. Mead,, R. A. Carabeo,, and T. Hackstadt. 2004. A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin. Proc. Natl. Acad. Sci. USA 101:10166–10171. PubMed CrossRef

43. Cocchiaro, J. L.,, Y. Kumar,, E. R. Fischer,, T. Hackstadt,, and R. H. Valdivia. 2008. Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc. Natl. Acad. Sci. USA 105:9379–9384. PubMed CrossRef

44. 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

45. Conant, C. G.,, and R. S. Stephens. 2007. Chlamydia attachment to mammalian cells requires protein disulfide isomerase. Cell. Microbiol. 9:222–232. PubMed CrossRef

46. 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

47. 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 CrossRef

48. 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

49. DeMars, R.,, and J. Weinfurter. 2008. Interstrain gene transfer in Chlamydia trachomatis in vitro: mechanism and significance. J. Bacteriol. 190:1605–1614. PubMed CrossRef

50. Demars, R.,, J. Weinfurter,, E. Guex,, J. Lin,, and Y. Potucek. 2007. Lateral gene transfer in vitro in the intracellular pathogen Chlamydia trachomatis. J. Bacteriol. 189:991–1003. PubMed CrossRef

51. Doughri, A. M.,, J. Storz,, and K. P. Altera. 1972. Mode of entry and release of chlamydiae in infections of intestinal epithelial cells. J. Infect. Dis. 126:652–657. PubMed CrossRef

52. Eissenberg, L. G.,, P. B. Wyrick,, C. H. Davis,, and J. W. Rumpp. 1983. Chlamydia psittaci elementary body envelopes: ingestion and inhibition of phagolysosome fusion. Infect. Immun. 40:741–751. PubMed

53. Everett, K. D.,, and T. P. Hatch. 1991. Sequence analysis and lipid modification of the cysteine-rich envelope proteins of Chlamydia psittaci 6BC. J. Bacteriol. 173:3821–3830. PubMed

54. Everett, K. D.,, and T. P. Hatch. 1995. Architecture of the cell envelope of Chlamydia psittaci 6BC. J. Bacteriol. 177:877–882. PubMed

55. 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

56. Fields, K. A.,, D. J. Mead,, C. A. Dooley,, and T. Hackstadt. 2003. Chlamydia trachomatis type III secretion: evidence for a functional apparatus during early-cycle development. Mol. Microbiol. 48:671–683. PubMed CrossRef

57. Fudyk, T.,, L. Olinger,, and R. S. Stephens. 2002. Selection of mutant cell lines resistant to infection by Chlamydia spp. Infect. Immun. 70:6444–6447. PubMed CrossRef

58. Garrett, A. J.,, M. J. Harrison,, and G. P. Manire. 1974. A search for the bacterial mucopeptide component, muramic acid, in Chlamydia. J. Gen. Microbiol. 80:315–318. PubMed CrossRef

59. Giannikopoulou, P.,, L. Bini,, P. D. Simitsek,, V. Pallini,, and E. Vretou. 1997. Two-dimensional electrophoretic analysis of the protein family at 90 kDa of abortifacient Chlamydia psittaci. Electrophoresis 18:2104–2108. PubMed CrossRef

60. 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

61. Grieshaber, N. A.,, E. R. Fischer,, D. J. Mead,, C. A. Dooley, and T. Hackstadt. 2004. Chlamydial histone-DNA interactions are disrupted by a metabolite in the methylerythritol phosphate pathway of isoprenoid biosynthesis. Proc. Natl. Acad. Sci. USA 101:7451–7456. PubMed CrossRef

62. Griffiths, P. C.,, H. L. Philips,, M. Dawson,, and M. J. Clarkson. 1992. Antigenic and morphological differentiation of placental and intestinal isolates of Chlamydia psittaci of ovine origin. Vet. Microbiol. 30:165–177. PubMed

63. 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

64. Hackstadt, T. 1986. Identification and properties of chlamydial polypeptides that bind eucaryotic cell surface components. J. Bacteriol. 165:13–20. PubMed

65. Hackstadt, T. 1991. Purification and N-terminal amino acid sequences of Chlamydia trachomatis histone analogs. J. Bacteriol. 173:7046–7049. PubMed

66. Hackstadt, T.,, W. Baehr,, and Y. Ying. 1991. Chlamydia trachomatis developmentally regulated protein is homologous to eukaryotic histone H1. Proc. Natl. Acad. Sci. USA 88:3937–3941. PubMed

67. Hackstadt, T.,, and H. D. Caldwell. 1985. Effect of proteolytic cleavage of surface-exposed proteins on infectivity of Chlamydia trachomatis. Infect. Immun. 48:546–551. PubMed

68. Hackstadt, T.,, M. A. Scidmore,, and D. D. Rockey. 1995. Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc. Natl. Acad. Sci. USA 92:4877–4881. PubMed

69. 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

70. Hatch, G. M.,, and G. McClarty. 1998. Phospholipid composition of purified Chlamydia trachomatis mimics that of the eucaryotic host cell. Infect. Immun. 66:3727–3735. PubMed

71. Hatch, T. P. 1996. Disulfide cross-linked envelope proteins: the functional equivalent of peptidoglycan in chlamydiae? J. Bacteriol. 178:1–5. PubMed

72. 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

73. 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

74. Hatch, T. P.,, D. W. Vance, Jr.,, and E. Al-Hossainy. 1981. Identification of a major envelope protein in Chlamydia spp. J. Bacteriol. 146:426–429. PubMed

75. Henderson, I. R.,, and A. C. Lam. 2001. Polymorphic proteins of Chlamydia spp.—autotransporters beyond the Proteobacteria. Trends Microbiol. 9:573–578. PubMed

76. Heuer, D.,, A. Rejman Lipinski,, N. Machuy,, A. Karlas,, A. Wehrens,, F. Siedler,, V. Brinkmann,, and T. F. Meyer. 2009. Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457:731–735. PubMed CrossRef

77. Higashi, N. 1965. Electron microscopic studies on the mode of reproduction of trachoma virus and psittacosis virus in cell cultures. Exp. Mol. Pathol. 76:24–39. PubMed

78. Hybiske, K.,, and R. S. Stephens. 2007. Mechanisms of host cell exit by the intracellular bacterium Chlamydia. Proc. Natl. Acad. Sci. USA 104:11430–11435. PubMed CrossRef

79. Iliffe-Lee, E. R.,, and G. McClarty. 2000. Regulation of carbon metabolism in Chlamydia trachomatis. Mol. Microbiol. 38:20–30. PubMed

80. Kari, L.,, M. M. Goheen,, L. B. Randall,, L. D. Taylor,, J. H. Carlson,, W. M. Whitmire,, D. Virok,, K. Rajaram,, V. Endresz,, G. McClarty,, D. E. Nelson,, and H. D. Caldwell. 2011. Generation of targeted Chlamydia trachomatis null mutants. Proc. Natl. Acad. Sci. USA 108:7189–7193. PubMed CrossRef

81. 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

82. 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

83. 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

84. Kubo, A.,, and R. S. Stephens. 2001. Substrate-specific diffusion of select dicarboxylates through Chlamydia trachomatis PorB. Microbiology 147:3135–3140. PubMed

85. Kuo, C.,, N. Takahashi,, A. F. Swanson,, Y. Ozeki,, and S. Hakomori. 1996. An N-linked high-mannose type oligosaccharide, expressed at the major outer membrane protein of Chlamydia trachomatis, mediates attachment and infectivity of the microorganism to HeLa cells. J. Clin. Investig. 98:2813–2818. PubMed CrossRef

86. Kuo, C. C.,, and T. Grayston. 1976. Interaction of Chlamydia trachomatis organisms and HeLa 229 cells. Infect. Immun. 13:1103–1109. PubMed

87. Kuo, C. C.,, A. Lee,, and L. A. Campbell. 2004. Cleavage of the N-linked oligosaccharide from the surfaces of Chlamydia species affects attachment and infectivity of the organisms in human epithelial and endothelial cells. Infect. Immun. 72:6699–6701. PubMed CrossRef

88. Lambden, P. R.,, J. S. Everson,, M. E. Ward,, and I. N. Clarke. 1990. Sulfur-rich proteins of Chlamydia trachomatis: developmentally regulated transcription of polycistronic mRNA from tandem promoters. Gene 87:105–112. PubMed

89. Lazarev, V. N.,, G. G. Borisenko,, M. M. Shkarupeta,, I. A. Demina,, M. V. Serebryakova,, M. A. Galyamina,, S. A. Levitskiy,, and V. M. Govorun. 2010. The role of intracellular glutathione in the progression of Chlamydia trachomatis infection. Free Radic. Biol. Med. 49:1947–1955. PubMed CrossRef

90. Levy, N. J.,, and J. W. Moulder. 1982. Attachment of cell walls of Chlamydia psittaci to mouse fibroblasts (L cells). Infect. Immun. 37:1059–1065. PubMed

91. Lim, J. B.,, and J. B. Klauda. 2011. Lipid chain branching at the iso- and anteiso-positions in complex Chlamydia membranes: a molecular dynamics study. Biochim. Biophys. Acta 1808:323–331. PubMed CrossRef

92. 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

93. 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

94. 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

95. 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

96. Lukacova, M.,, M. Baumann,, L. Brade,, U. Mamat,, and H. Brade. 1994. Lipopolysaccharide smooth-rough phase variation in bacteria of the genus Chlamydia. Infect. Immun. 62:2270–2276. PubMed

97. Manire, G. P. 1966. Structure of purified cell walls of dense forms of meningopneumonitis organisms. J. Bacteriol. 91:409–413. PubMed

98. Manire, G. P.,, and A. Tamura. 1967. Preparation and chemical composition of the cell walls of mature infectious dense forms of meningopneumonitis organisms. J. Bacteriol. 94:1178–1183. PubMed

99. Matsumoto, A. 1973. Fine structures of cell envelopes of Chlamydia organisms as revealed by freeze-etching and negative staining techniques. J. Bacteriol. 116:1355–1363. PubMed

100. Matsumoto, A. 1981. Electron microscopic observations of surface projections and related intracellular structures of Chlamydia organisms. J. Electron Microsc. (Tokyo) 30:315–320.

101. Matsumoto, A. 1982. Electron microscopic observations of surface projections on Chlamydia psittaci reticulate bodies. J. Bacteriol. 150:358–364. PubMed

102. Matsumoto, A.,, N. Higashi,, and A. Tamura. 1973. Electron microscope observations on the effects of polymixin B sulfate on cell walls of Chlamydia psittaci. J. Bacteriol. 113:357–364. PubMed

103. Matsumoto, A.,, and G. P. Manire. 1970a. Electron microscopic observations on the effects of penicillin on the morphology of Chlamydia psittaci. J. Bacteriol. 101:278–285. PubMed

104. Matsumoto, A.,, and G. P. Manire. 1970b. Electron microscopic observations on the fine structure of cell walls of Chlamydia psittaci. J. Bacteriol. 104:1332–1337. PubMed

105. McCoy, A. J.,, and A. T. Maurelli. 2006. Building the invisible wall: updating the chlamydial peptidoglycan anomaly. Trends Microbiol. 14:70–77. PubMed CrossRef

106. Melgosa, M. P.,, C. C. Kuo,, and L. A. Campbell. 1993. Outer membrane complex proteins of Chlamydia pneumoniae. FEMS Microbiol. Lett. 112:199–204. PubMed

107. 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

108. Molleken, 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

109. Morrison, S. G.,, and R. P. Morrison. 2005. A predominant role for antibody in acquired immunity to chlamydial genital tract reinfection. J. Immunol. 175:7536–7542. PubMed

110. Moulder, J. W. 1962. Some basic properties of the psittacosis-lymphogranuloma venereum group of agents. Structure and chemical composition of isolated particles. Ann. N. Y. Acad. Sci. 98:92–99. PubMed

111. Moulder, J. W. 1991. Interaction of chlamydiae and host cells in vitro. Microbiol. Rev. 55:143–190. PubMed

112. Moulder, J. W.,, D. L. Novosel,, and J. E. Officer. 1963. Inhibition of the growth of agents of the psittacosis group by D-cycloserine and its specific reversal by D-alanine. J. Bacteriol. 85:707–711. PubMed

113. Muller-Loennies, S.,, S. Gronow,, L. Brade,, R. MacKenzie,, P. Kosma,, and H. Brade. 2006. A monoclonal antibody against a carbohydrate epitope in lipopolysaccharide differentiates Chlamydophila psittaci from Chlamydophila pecorum, Chlamydophila pneumoniae, and Chlamydia trachomatis. Glycobiology 16:184–196. PubMed CrossRef

114. Muschiol, S.,, L. Bailey,, A. Gylfe,, C. Sundin,, K. Hultenby,, S. Bergstrom,, M. Elofsson,, H. Wolf-Watz,, S. Normark,, and B. Henriques-Normark. 2006. A small-molecule inhibitor of type III secretion inhibits different stages of the infectious cycle of Chlamydia trachomatis. Proc. Natl. Acad. Sci. USA 103:14566–14571. PubMed CrossRef

115. Mygind, P.,, G. Christiansen,, and S. Birkelund. 1998. Topological analysis of Chlamydia trachomatis L2 outer membrane protein 2. J. Bacteriol. 180:5784–5787. PubMed

116. 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

117. Nano, F. E.,, P. A. Barstad,, L. W. Mayer,, J. E. Coligan, and H. D. Caldwell. 1985. Partial amino acid sequence and molecular cloning of the encoding gene for the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 48:372–377. PubMed

118. Narita, T.,, P. B. Wyrick,, and G. P. Manire. 1976. Effect of alkali on the structure of cell envelopes of Chlamydia psittaci elementary bodies. J. Bacteriol. 125:300–307. PubMed

119. Nelson, D. E.,, D. D. Crane,, L. D. Taylor,, D. W. Dorward,, M. M. Goheen,, and H. D. Caldwell. 2006. Inhibition of chlamydiae by primary alcohols correlates with the strain-specific complement of plasticity zone phospholipase D genes. Infect. Immun. 74:73–80. PubMed CrossRef

120. Newhall, W. J. 1987. Biosynthesis and disulfide cross-linking of outer membrane components during the growth cycle of Chlamydia trachomatis. Infect. Immun. 55:162–168. PubMed

121. Newhall, W. J., 1988. Macromolecular and antigenic composition of chlamydiae, p. 47-70. In A. L. Barron (ed.), Microbiology of Chlamydia. CRC Press, Boca Raton, FL.

122. Newhall, W. J.,, B. Batteiger,, and R. B. Jones. 1982. Analysis of the human serological response to proteins of Chlamydia trachomatis. Infect. Immun. 38:1181–1189. PubMed

123. Newhall, W. J.,, and R. B. Jones. 1983. Disulfide-linked oligomers of the major outer membrane protein of chlamydiae. J. Bacteriol. 154:998–1001. PubMed

124. Nguyen, B. D.,, D. Cunningham,, X. Liang,, X. Chen,, E. J. Toone,, C. R. Raetz,, P. Zhou,, and R. H. Valdivia. 2011. Lipooligosaccharide is required for the generation of infectious elementary bodies in Chlamydia trachomatis. Proc. Natl. Acad. Sci. USA 108:10284–10289. PubMed CrossRef

125. Nurminen, M.,, M. Leinonen,, P. Saikku,, and P. H. Makela. 1983. The genus-specific antigen of Chlamydia: resemblance to the lipopolysaccharide of enteric bacteria. Science 220:1279–1281. PubMed

126. Nurminen, M.,, E. T. Rietschel,, and H. Brade. 1985. Chemical characterization of Chlamydia trachomatis lipopolysaccharide. Infect. Immun. 48:573–575. PubMed

127. Oomen, C. J.,, P. van Ulsen,, P. van Gelder,, M. Feijen,, J. Tommassen,, and P. Gros. 2004. Structure of the translocator domain of a bacterial autotransporter. EMBO J. 23:1257–1266. PubMed CrossRef

128. 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

129. Rank, R. G.,, J. Whittimore,, A. K. Bowlin,, and P. B. Wyrick. 2011. In vivo ultrastructural analysis of the intimate relationship between polymorphonuclear leukocytes and the chlamydial developmental cycle. Infect. Immun. 79:3291–3301. PubMed CrossRef

130. Rasmussen-Lathrop, S. J.,, K. Koshiyama,, N. Phillips,, and R. S. Stephens. 2000. Chlamydia-dependent biosynthesis of a heparan sulphate-like compound in eukaryotic cells. Cell. Microbiol. 2:137–144. PubMed

131. Raulston, J. E. 1995. Chlamydial envelope components and pathogen-host cell interactions. Mol. Microbiol. 15:607–616. PubMed

132. Raulston, J. E.,, C. H. Davis,, T. R. Paul,, J. D. Hobbs,, and P. B. Wyrick. 2002. Surface accessibility of the 70-kilodalton Chlamydia trachomatis heat shock protein following reduction of outer membrane protein disulfide bonds. Infect. Immun. 70:535–543. PubMed

133. Read, T. D.,, R. C. Brunham,, C. Shen,, S. R. Gill,, J. F. Heidelberg,, O. White,, E. K. Hickey,, J. Peterson,, T. Utterback,, K. Berry,, S. Bass,, K. Linher,, J. Weidman,, H. Khouri,, B. Craven,, C. Bowman,, R. Dodson,, M. Gwinn,, W. Nelson,, R. DeBoy,, J. Kolonay,, G. McClarty,, S. L. Salzberg,, J. Eisen,, and C. M. Fraser. 2000a. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28:1397–1406. PubMed

134. Read, T. D.,, C. M. Fraser,, R. C. Hsia,, and P. M. Bavoil. 2000b. Comparative analysis of Chlamydia bacteriophages reveals variation localized to a putative receptor binding domain. Microb. Comp. Genomics 5:223–231. PubMed

135. Rund, S.,, B. Lindner,, H. Brade,, and O. Holst. 1999. Structural analysis of the lipopolysaccharide from Chlamydia trachomatis serotype L2. J. Biol. Chem. 274:16819–16824. PubMed

136. Salari, S. H.,, and M. E. Ward. 1981. Polypeptide composition of Chlamydia trachomatis. J. Gen. Microbiol. 123:197–207. PubMed

137. Schachter, J.,, and M. Grossman. 1981. Chlamydial infections. Annu. Rev. Med. 32:45–61.

138. Scidmore, M. A.,, E. R. Fischer,, and T. Hackstadt. 1996a. Sphingolipids and glycoproteins are differentially trafficked to the Chlamydia trachomatis inclusion. J. Cell Biol. 134:363–374. PubMed

139. Scidmore, M. A.,, D. D. Rockey,, E. R. Fischer,, R. A. Heinzen,, and T. Hackstadt. 1996b. Vesicular interactions of the Chlamydia trachomatis inclusion are determined by chlamydial early protein synthesis rather than route of entry. Infect. Immun. 64:5366–5372. PubMed

140. 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

141. Shaw, E. I.,, C. A. Dooley,, E. R. Fischer,, M. A. Scidmore,, K. A. Fields,, and T. Hackstadt. 2000. Three temporal classes of gene expression during the Chlamydia trachomatis developmental cycle. Mol. Microbiol. 37:913–925. PubMed CrossRef

142. 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

143. 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

144. 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

145. Stephens, R. S.,, and C. J. Lammel. 2001. Chlamydia outer membrane protein discovery using genomics. Curr. Opin. Microbiol. 4:16–20. PubMed

146. Stephens, R. S.,, J. M. Poteralski,, and L. Olinger. 2006. Interaction of Chlamydia trachomatis with mammalian cells is independent of host cell surface heparan sulfate glycosaminoglycans. Infect. Immun. 74:1795–1799. PubMed CrossRef

147. Stephens, R. S.,, M. R. Tam,, C. C. Kuo,, and R. C. Nowinski. 1982. Monoclonal antibodies to Chlamydia trachomatis: antibody specificities and antigen characterization. J. Immunol. 128:1083–1089. PubMed

148. Stuart, E. S.,, and A. B. Macdonald. 1989. Some characteristics of a secreted chlamydial antigen recognized by IgG from C. trachomatis patient sera. Immunology 68:469–473. PubMed

149. Stuart, E. S.,, P. B. Wyrick,, J. Choong,, S. B. Stoler,, and A. B. MacDonald. 1991. Examination of chlamydial glycolipid with monoclonal antibodies: cellular distribution and epitope binding. Immunology 74:740–747. PubMed

150. Su, H.,, G. McClarty,, F. Dong,, G. M. Hatch,, Z. K. Pan,, and G. Zhong. 2004. Activation of Raf/MEK/ERK/cPLA2 signaling pathway is essential for chlamydial acquisition of host glycerophospholipids. J. Biol. Chem. 279:9409–9416. PubMed CrossRef

151. 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

152. Suchland, R. J.,, K. M. Sandoz,, B. M. Jeffrey,, W. E. Stamm,, and D. D. Rockey. 2009. Horizontal transfer of tetracycline resistance among Chlamydia spp. in vitro. Antimicrob. Agents Chemother. 53:4604–4611. PubMed CrossRef

153. Sun, G.,, S. Pal,, A. K. Sarcon,, S. Kim,, E. Sugawara,, H. Nikaido,, M. J. Cocco,, E. M. Peterson,, and L. M. de la Maza. 2007. Structural and functional analyses of the major outer membrane protein of Chlamydia trachomatis. J. Bacteriol. 189:6222–6235. PubMed CrossRef

154. Swanson, A. F.,, and C. C. Kuo. 1991. Evidence that the major outer membrane protein of Chlamydia trachomatis is glycosylated. Infect. Immun. 59:2120–2125. PubMed

155. 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

156. 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

157. Tamura, A.,, and G. P. Manire. 1967. Preparation and chemical composition of the cell membranes of developmental reticulate forms of meningopneumonitis organisms. J. Bacteriol. 94:1184–1188. PubMed

158. Tamura, A.,, and G. P. Manire. 1968. Effect of penicillin on the multiplication of meningopneumonitis organisms (Chlamydia psittaci). J. Bacteriol. 96:875–880. PubMed

159. Tamura, A.,, A. Matsumoto,, G. P. Manire,, and N. Higashi. 1971. Electron microscopic observations on the structure of the envelopes of mature elementary bodies and developmental reticulate forms of Chlamydia psittaci. J. Bacteriol. 105:355–360. PubMed

160. 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

161. 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

162. 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

163. 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

164. Tao, S.,, R. Kaul,, and W. M. Wenman. 1991. Identification and nucleotide sequence of a developmentally regulated gene encoding a eukaryotic histone H1-like protein from Chlamydia trachomatis. J. Bacteriol. 173:2818–2822. PubMed

165. Taylor, L. D.,, D. E. Nelson,, D. W. Dorward,, W. M. Whitmire,, and H. D. Caldwell. 2010. Biological characterization of Chlamydia trachomatis plasticity zone MACPF domain family protein CT153. Infect. Immun. 78:2691–2699. PubMed CrossRef

166. 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

167. Tjaden, J.,, H. H. Winkler,, C. Schwoppe,, M. Van Der Laan,, T. Mohlmann,, and H. E. Neuhaus. 1999. Two nucleotide transport proteins in Chlamydia trachomatis, one for net nucleoside triphosphate uptake and the other for transport of energy. J. Bacteriol. 181:1196–1202. PubMed

168. Vandahl, B. B.,, S. Birkelund,, and G. Christiansen. 2004. Genome and proteome analysis of Chlamydia. Proteomics 4:2831–2842. PubMed CrossRef

169. Vandahl, B. B.,, K. Gevaert,, H. Demol,, B. Hoorelbeke,, A. Holm,, J. Vandekerckhove,, G. Christiansen,, and S. Birkelund. 2001. Time-dependent expression and processing of a hypothetical protein of possible importance for regulation of the Chlamydia pneumoniae developmental cycle. Electrophoresis 22:1697–1704. PubMed CrossRef

170. Vandahl, B. B.,, A. S. Pedersen,, K. Gevaert,, A. Holm,, J. Vandekerckhove,, G. Christiansen,, and S. Birkelund. 2002. The expression, processing and localization of polymorphic membrane proteins in Chlamydia pneumoniae strain CWL029. BMC Microbiol. 2:36. PubMed CrossRef

171. Vora, G. J.,, and E. S. Stuart. 2003. A role for the glycolipid exoantigen (GLXA) in chlamydial infectivity. Curr. Microbiol. 46:217–223. PubMed CrossRef

172. Vretou, E.,, P. Giannikopoulou,, D. Longbottom,, and E. Psarrou. 2003. Antigenic organization of the N-terminal part of the polymorphic outer membrane proteins 90, 91A, and 91B of Chlamydophila abortus. Infect. Immun. 71:3240–3250. PubMed CrossRef

173. Watson, M. W.,, P. R. Lambden,, M. E. Ward,, and I. N. Clarke. 1989. Chlamydia trachomatis 60 kDa cysteine rich outer membrane protein: sequence homology between trachoma and LGV biovars. FEMS Microbiol. Lett. 53:293–297. PubMed

174. Webley, W. C.,, G. J. Vora,, and E. S. Stuart. 2004. Cell surface display of the chlamydial glycolipid exoantigen (GLXA) demonstrated by antibody-dependent complement-mediated cytotoxicity. Curr. Microbiol. 49:13–21. PubMed CrossRef

175. 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

176. Welter-Stahl, L.,, D. M. Ojcius,, J. Viala,, S. Girardin,, W. Liu,, C. Delarbre,, D. Philpott,, K. A. Kelly,, and T. Darville. 2006. Stimulation of the cytosolic receptor for peptidoglycan, Nod1, by infection with Chlamydia trachomatis or Chlamydia muridarum. Cell. Microbiol. 8:1047–1057. PubMed CrossRef

177. Wichlan, D. G.,, and T. P. Hatch. 1993. Identification of an early-stage gene of Chlamydia psittaci 6BC. J. Bacteriol. 175:2936–2942. PubMed

178. Wilson, D. P.,, P. Timms,, D. L. McElwain,, and P. M. Bavoil. 2006. Type III secretion, contact-dependent model for the intracellular development of Chlamydia. Bull. Math. Biol. 68:161–178. PubMed CrossRef

179. Wilson, D. P.,, J. A. Whittum-Hudson,, P. Timms,, and P. M. Bavoil. 2009. Kinematics of intracellular chlamydiae provide evidence for contact-dependent development. J. Bacteriol. 191:5734–5742. PubMed CrossRef

180. Wolf, K.,, H. J. Betts,, B. Chellas-Gery,, S. Hower,, C. N. Linton,, and K. A. Fields. 2006. Treatment of Chlamydia trachomatis with a small molecule inhibitor of the Yersinia type III secretion system disrupts progression of the chlamydial developmental cycle. Mol. Microbiol. 61:1543–1555. PubMed CrossRef

181. Wylie, J. L.,, G. M. Hatch,, and G. McClarty. 1997. Host cell phospholipids are trafficked to and then modified by Chlamydia trachomatis. J. Bacteriol. 179:7233–7242. PubMed

182. 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

183. Zhang, J. P.,, and R. S. Stephens. 1992. Mechanism of C. trachomatis attachment to eukaryotic host cells. Cell 69:861–869. PubMed CrossRef