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Chapter 9 : Protein Secretion and Pathogenesis

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Abstract:

While significant progress has been made in unraveling the contributions of protein secretion to chlamydial pathogenesis, many pivotal open questions remain. This chapter endeavors to explore current knowledge regarding chlamydial protein secretion as well as point outs substantial gaps in understanding. The type III secretion (T3S) pathway is emphasized, given that this area has received considerable attention and fruitful research has provided significant insight regarding protein secretion mechanism. However, it is important to emphasize that T3S does not represent the entire arsenal for chlamydial protein secretion and other equally important secretion mechanisms contribute to chlamydial survival. Protein secretion and translocation are accomplished by an elegantly complex secretory apparatus collectively referred to as the "injectisome". In the working model, the assembly of the core apparatus begins with membrane insertion of the outer membrane (OM) secretin CdsC followed by addition of inner membrane (IM) components CdsD and CdsJ. Secretion chaperones also play a prominent role in facilitating and potentially regulating T3S. Even without genetics, protein secretion affords opportunities to push the envelope of research. A recent genome-wide expression study of chlamydial proteins in revealed preliminary evidence for antihost function. The study included gene products annotated as hypothetical with respect to function. The results must be taken with a grain of salt since it is likely that many of the tested proteins are not actually secreted proteins.

Citation: Fields K. 2012. Protein Secretion and Pathogenesis, p 192-216. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch9
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FIGURE 1

Secretion pathways employed for proteins secretion in spp. (A) The T2S system mediates export of proteins (T2E) across the chlamydial IM via the Sec protein machinery. Once in the periplasm (PP), signal peptidases can cleave secretion signals (S), and the protein is subsequently secreted across the chlamydial OM through the GspD secretin. (B) T5S substrates (T5E) also gain access to the periplasm via the IM Sec machinery, but domains within the secreted protein mediate direct insertion into the OM. Subsequent cleavage of the passenger domain would release T5S substrates into the inclusion lumen. (C) Translocation of type II and type V secreted proteins could be achieved via formation of OMVs that subsequently fuse with host plasma membrane (PM) or inclusion membranes (InM) to release effector proteins into the host cytosol. (D) The T3S system mediates single-step secretion and translocation of effector proteins directly into the cytosol of an infected cell. doi:10.1128/9781555817329.ch9.f1

Citation: Fields K. 2012. Protein Secretion and Pathogenesis, p 192-216. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch9
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Image of FIGURE 2
FIGURE 2

A working model for the assembly and composition of the chlamydial T3SS. Stepwise addition of proteins is indicated with newly added components shown in dark grey and previously assembled components in light grey (shown with Cds or Cop letter designation only). Schematic representations of flagellar proteins are omitted for clarity but include FlhA/CT060 (CdsV paralog), FliI/CT717 (CdsN paralog), FliH/CT718 (CdsL paralog), and FliF/CT719 (CdsJ paralog). The completed injectisome spans the bacterial IM, periplasm (PP), and OM and includes TC, NC, and basal apparatus complexes. Secreted translocon (Tr) components are shown localized to the host plasma membrane (PM) or inclusion membrane (InM). Correct stoichiometry of multimeric proteins is not indicated. This figure was adapted from previously published images ( ). doi:10.1128/9781555817329.ch9.f2

Citation: Fields K. 2012. Protein Secretion and Pathogenesis, p 192-216. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch9
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References

/content/book/10.1128/9781555817329.chap9
1. Abdelrahman, Y. M.,, and R. J. Belland. 2005. The chlamydial developmental cycle. FEMS Microbiol. Rev. 29:949959. PubMed CrossRef
2. Akeda, Y.,, and J. E. Galan. 2005. Chaperone release and unfolding of substrates in type III secretion. Nature 437:911915. PubMed CrossRef
3. Alvesalo, J.,, D. Greco,, M. Leinonen,, T. Raitila,, P. Vuerela,, and P. Auvinen. 2008. Microarray analysis of a Chlamydia pneumoniae-infected human epithelial cell line by use of ontology heirarchy. J. Infect. Dis. 197:156162. PubMed CrossRef
4. Alzhanov, D.,, J. Barnes,, D. Hruby,, and D. D. Rockey. 2004. Chlamydial development is blocked in host cells transfected with Chlamydophila caviae incA. BMC Microbiol. 4:110. PubMed CrossRef
5. Azuma, Y.,, H. Hirakawa,, A. Yamashita,, Y. Cai,, M. A. Rahman,, H. Suzuki,, S. Mitaku,, H. Toh,, S. Goto,, T. Murakami,, K. Sugi,, H. Hayashi,, H. Fukushi,, H. Hattori,, S. Kuhara,, and M. Shirai. 2006. Genome sequence of the cat pathogen, Chlamydophila felis. DNA Res. 13:1523. PubMed CrossRef
6. Bailey, L.,, A. Gylfe,, C. Sundin,, S. Muschiol,, M. Elofsson,, P. Nordstrom,, B. Henriques-Normark,, R. Lugert,, A. Waldenstrom,, H. Wolf-Watz,, and S. Bergstrom. 2007. Small molecule inhibitors of type III secretion in Yersinia block the Chlamydia pneumoniae infection cycle. FEBS Lett. 58:587595. PubMed CrossRef
7. Balsara, Z. R.,, S. Misaghi,, J. N. Lafave,, and M. N. Starnbach. 2006. Chlamydia trachomatis infection induces cleavage of the mitotic cyclin B1. Infect. Immun. 74:56025608. PubMed CrossRef
8. Bannantine, J. P.,, R. S. Griffiths,, W. Viratyosin,, W. J. Brown,, and D. D. Rockey. 2000. A secondary structure motif predictive of protein localization to the chlamydial inclusion membrane. Cell. Microbiol. 2:3547. PubMed CrossRef
9. Belland, R. J.,, M. A. Scidmore,, D. D. Crane,, D. M. Hogan,, W. Whitmire,, G. McClarty,, and H. D. Caldwell. 2001. Chlamydia trachomatis cytotoxicity associated with complete and partial cytotoxin genes. Proc. Natl. Acad. Sci. USA 98:1398413989. PubMed CrossRef
10. Belland, R. J.,, G. Zhong,, D. D. Crane,, D. Hogan,, D. Sturdevant,, J. Sharma,, W. L. Beatty,, and H. D. Caldwell. 2003. Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc. Natl. Acad. Sci. USA 100:84788483. PubMed CrossRef
11. Benaud, C.,, B. J. Gentil,, N. Assard,, M. Court,, J. Garin,, C. Delphin,, and J. Baudier. 2004. AHNAK interaction with the annexin 2/S100A10 complex regulates cell membrane cytoarchitecture. J. Cell Biol. 164:133144. PubMed CrossRef
12. 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. 190:16801690. PubMed CrossRef
13. Betts, H. J.,, K. Wolf,, and K. A. Fields. 2009. Effector protein modulation of host cells: examples in the Chlamydia spp. arsenal. Curr. Opin. Microbiol. 12:8187. PubMed CrossRef
14. Betts-Hampikian, H. J.,, and K. A. Fields. 2010. The chlamydial type III secretion mechanism: revealing cracks in a tough nut. Frontiers Microbiol. 1:114. PubMed CrossRef
15. Betts-Hampikian, H. J.,, and K. A. Fields. 2011. Disulfide bonding within components of the Chlamydia type III secretion appratus correlates with development. J. Bacteriol. 193:69506959. PubMed CrossRef
16. 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. 55:187195. PubMed CrossRef
17. Blaylock, B.,, B. J. Berube,, and O. Schneewind. 2010. YopR impacts type III needle polymerization in Yersinia species. Mol. Microbiol. 75:221229. PubMed CrossRef
18. Blaylock, B.,, K. E. Riordan,, D. M. Missiakas,, and O. Schneewind. 2006. Characterization of the Yersinia enterocolitica type III secretion ATPase YscN and its regulator, YscL. J. Bacteriol. 188:35253534. PubMed CrossRef
19. Blocker, A.,, J. E. Deane,, A. K. Veenendall,, P. Roversi,, J. L. Hodgkinson,, S. Johnson,, and S. M. Lea. 2008. What's the point of the type III secretion needle? Proc. Natl. Acad. Sci. USA 105:65076513. PubMed CrossRef
20. Burton, M. J.,, S. N. Rajak,, J. Bauer,, H. A. Weiss,, S. B. Tolbert,, A. Shoo,, E. Habtamu,, A. Manjurano,, P. M. Emerson,, D. Mabey,, M. J. Holland,, and R. L. Bailey. 2011. Conjunctival transcriptome in scarring trachoma. Infect. Immun. 79:499511. PubMed CrossRef
21. Cain, R. J.,, R. D. Hayward,, and V. Koronakis. 2008. Deciphering interplay between Salmonella invasion effectors. PLoS Pathog. 4:e1000037. PubMed CrossRef
22. Cambronne, E. D.,, and C. R. Roy. 2006. Recognition and delivery of effector proteins into eukaryotic cells by bacterial secretion systems. Traffic 7:929939. PubMed CrossRef
23. Case, E. D.,, E. M. Peterson,, and M. Tan. 2010. Promoters for Chlamydia type III secretion genes show a differential response to DNA supercoiling that correlates with temporal expression pattern. J. Bacteriol. 192:25692574. PubMed CrossRef
24. Chang, J. J.,, K. R. Leonard,, and Y. X. Zhang. 1997. Structural studies of the surface projections of Chlamydia trachomatis by electron microscopy. J. Med. Microbiol. 46:10131018. PubMed CrossRef
25. Chellas-Géry, B.,, C. N. Linton,, and K. A. Fields. 2007. Human GCIP interacts with CT847, a novel Chlamydia trachomatis type III secretion substrate, and is degraded in a tissue-culture infection model. Cell. Microbiol. 9:24172430. PubMed CrossRef
26. Chellas-Géry, B.,, K. Wolf,, J. Tisoncik,, T. Hackstadt,, and K. A. Fields. 2011. Biochemical and immunolocalization analyses of putative type III secretion translocator proteins CopB and CopB2 of Chlamydia trachomatis reveal significant distinctions. Infect. Immun. 79:30353046. PubMed CrossRef
27. Chen, D.,, L. Lei,, C. Lu,, R. Flores,, M. P. DeLisa,, T. C. Roberts,, F. E. Romesberg,, and G. Zhong. 2010. Secretion of the chlamydial virulence factor CPAF requires the Sec-dependent pathway. Microbiology 56:30313040. PubMed CrossRef
28. Christian, J.,, J. Vier,, S. A. Paschen,, and G. Häcker. 2010. Cleavage of the NF-κB family protein p65/RelA by the chlamydial protease-like activity factor (CPAF) impairs proinflammatory signaling in cells infected with chlamydiae. J. Biol. Chem. 285:4132041327. PubMed CrossRef
29. Clifton, D. R.,, C. A. Dooley,, S. S. Grieshaber,, R. A. Carabeo,, K. A. Fields,, and T. Hackstadt. 2005. Tyrosine phosphorylation of the chlamydial effector protein Tarp is species specific and not required for recruitment of actin. Infect. Immun. 73:38603868. PubMed CrossRef
30. 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 101:1016610171. PubMed CrossRef
31. Cocchiaro, J. L.,, and R. H. Valdivia. 2009. New insights into Chlamydia intracellular survival mechanisms. Cell. Microbiol. 11:15711578. PubMed CrossRef
32. Cocucci, E.,, G. Racchetti,, P. Podini,, and J. Meldolesi. 2007. Enlargeosome traffic: exocytosis triggered by various signals is followed by endocytosis, membrane shedding or both. Traffic 8:742757. PubMed CrossRef
33. Cortes, C.,, K. A. Rzomp,, A. Tvinnereim,, M. A. Scidmore,, and B. Wizel. 2007. Chlamydia pneumoniae inclusion membrane protein Cpn0585 interacts with multiple Rab GTPases. Infect. Immun. 75:55865596. PubMed CrossRef
34. Crane, D. D.,, J. H. Carlson,, E. R. Fischer,, P. Bavoil,, R. 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 103:18941899. PubMed CrossRef
35. Cruz-Fisher, M. I.,, C. Cheng,, G. Sun,, S. Pal,, A. Teng,, D. M. Molina,, M. A. Kayala,, A. Vigil,, P. Baldi,, P. L. Felgner,, X. Liang,, and L. M. de la Maza. 2011. Identification of immunodominant antigens by probing a whole Chlamydia trachomatis open reading frame proteome microarray using sera from immunized mice. Infect. Immun. 79:246257. PubMed CrossRef
36. Curak, J.,, J. Rohde,, and I. Stagljar. 2009. Yeast as a tool to study bacterial effectors. Curr. Opin. Microbiol. 12:1823. PubMed CrossRef
37. Dautry-Varsat, A.,, A. Subtil,, and T. Hackstadt. 2005. Recent insights into the mechanisms of Chlamydia entry. Cell. Microbiol. 7:17141722. PubMed CrossRef
38. Deane, J. E.,, P. Roversi,, F. S. Cordes,, S. Johnson,, R. Kenjale,, S. Daniall,, F. Booy,, W. D. Picking,, W. L. Picking,, A. Blocker,, and S. M. Lea. 2006. Molecular model of a type three secretion system needle: implications for host cell sensing. Proc. Natl. Acad. Sci. USA 103:1252912533. PubMed CrossRef
39. Durocher, D.,, I. A. Taylor,, D. Sarbassova,, L. F. Haire,, S. L. Westcott,, S. P. Jackson,, S. J. Smerdon,, and M. B. Yaffe. 2000. The molecular basis of FHA domain: phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms. Mol. Cell 6:11691182. PubMed CrossRef
40. Ellis, T. N.,, and M. J. Kuehn. 2010. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74:8194. PubMed CrossRef
41. Elwell, C. A.,, A. Ceesay,, J. H. Kim,, D. Kalman,, and J. N. Engel. 2008. RNA interference screen identifies Able Kinase and PDGFR signaling in Chlamydia trachomatis entry. PLoS Pathog. 4:e1000021. PubMed CrossRef
42. Espina, M.,, A. J. Olive,, R. Kenjale,, D. S. Moore,, S. F. Ausar,, C. R. Middaugh,, R. W. Kaminski,, E. V. Oaks,, M. A. Baxter,, W. D. Picking,, and W. L. Picking. 2006. IpaD localizes to the tip of the type III secretion system needle of Shigella flexneri. Infect. Immun. 74:43914400. PubMed CrossRef
43. Feldman, M. F.,, and G. R. Cornelis. 2003. The multitalented type III chaperones: all you can do with 15 kDa. FEMS Microbiol. Lett. 219:151158. PubMed
44. Ferracci, F.,, F. D. Schubot,, D. S. Waugh,, and G. V. Plano. 2005. Selection and characterization of Yersinia pestis YopN mutants that constitutively block Yop secretion. Mol. Microbiol. 57:970987. PubMed CrossRef
45. Fields, K. A.,, E. R. Fischer,, D. J. Mead,, and T. Hackstadt. 2005. Analysis of putative Chlamydia trachomatis chaperones Scc2 and Scc3 and their use in the identification of type III secretion substrates. J. Bacteriol. 187:64666478. PubMed CrossRef
46. Fields, K. A.,, and T. Hackstadt. 2000. Evidence for the secretion of Chlamydia trachomatis CopN by a type III secretion mechanism. Mol. Microbiol. 38:10481060. PubMed
47. Fields, K. A.,, and T. Hackstadt,. 2006. The Chlamydia type III secretion system: structure and implications for pathogenesis, p. 220233. In P. Bavoil, and P. B. Wyrick (ed.), Chlamydia: Genomics and Pathogenesis. Horizon Press, Norfolk, United Kingdom.
48. 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. 48:671683. PubMed CrossRef
49. Fu, Y.,, and J. E. Galan. 1999. A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 401:293297. PubMed CrossRef
50. Giles, D. K.,, J. D. Whittimore,, R. W. LaRue,, J. E. Raulston,, and P. B. Wyrick. 2006. Ultrastructural analysis of chlamydial antigen-containing vesicles everting for the Chlamydia trachomatis inclusion. Microbes Infect. 8:15791591. PubMed CrossRef
51. Gonzalez-Pedrajo, B.,, T. Minamino,, M. Kihara,, and K. Namba. 2006. Interactions between C ring proteins and export apparatus components: a possible mechanism for facilitating type III protein export. Mol. Microbiol. 60:984998. PubMed CrossRef
52. 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 101:74517456. PubMed CrossRef
53. Hackstadt, T.,, M. Scidmore-Carlson,, E. Shaw,, and E. Fischer. 1999. The Chlamydia trachomatis IncA protein is required for homotypic vesicle fusion. Cell. Microbiol. 1:119130. PubMed CrossRef
54. 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. 161:2531. PubMed
55. Hakansson, S.,, K. Schesser,, C. Persson,, E. E. Galyov,, R. Rosqvist,, F. Homble,, and H. Wolf-Watz. 1996. The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J. 15:58125823. PubMed
56. Hatch, T. P., 1999. Developmental biology, p. 2967. In R. S. Stephens (ed.), Chlamydia: Intracellular Biology, Pathogenesis, and Immunity. ASM Press, Washington, DC.
57. 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. 165:379385. PubMed
58. Hefty, P. S.,, and R. S. Stephens. 2007. Chlamydial type III secretion system is encoded on ten operons preceded by sigma 70-like promoter elements. J. Bacteriol. 189:198206. PubMed CrossRef
59. Henderson, I. R.,, and A. C. Lam. 2001. Polymorphic proteins of Chlamydia spp.—autotransporters beyond the proteobacteria. Trends Microbiol. 9:573578. PubMed
60. Heuer, D.,, V. Brinkmann,, T. F. Meyer,, and A. J. Szczepek. 2003. Expression and translocation of chlamydial protease during acute and persistent infection of the epithelial HEp-2 cells with Chlamydophila (Chlamydia) pneumoniae. Cell. Microbiol. 5:315322. PubMed CrossRef
61. Heuer, D.,, L. Rejman,, 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 457:731735. PubMed CrossRef
62. Ho, T. D.,, and M. N. Starnbach. 2005. The Salmonella enterica serovar Typhimurium-encoded type III secretion systems can translocate Chlamydia trachomatis proteins into the cytosol of host cells. Infect. Immun. 73:905911. PubMed CrossRef
63. Hoare, A.,, P. Timms,, P. M. Bavoil,, and D. P. Wilson. 2008. Spatial constraints within the chlamydial host cell inclusion predict interrupted development and persistence. BMC Microbiol. 8:19. PubMed CrossRef
64. Horn, M.,, A. Collingro,, S. Schmitz-Esser,, C. L. Beier,, U. Purkhold,, B. Fartmann,, P. Brandt,, G. J. Nyakatura,, M. Droege,, D. Frishman,, T. Rattei,, H. Mewes,, and M. Wagner. 2004. Illuminating the evolutionary history of Chlamydiae. Science 304:728730. PubMed CrossRef
65. Hower, S.,, K. Wolf,, and K. A. Fields. 2009. Evidence that CT694 is a novel Chlamydia trachomatis T3S substrate capable of functioning during invasion or early cycle development. Mol. Microbiol. 72:14231437. PubMed CrossRef
66. Hsia, R. C.,, Y. Pannekoek,, E. Ingerowski,, and P. M. Bavoil. 1997. Type III secretion genes identify a putative virulence locus of Chlamydia. Mol. Microbiol. 25:351359. PubMed CrossRef
67. Huang, J.,, C. F. Lesser,, and S. Lory. 2008. The essential role of the CopN protein in Chlamydia pneumoniae intracellular growth. Nature 456:112115. PubMed CrossRef
68. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379433. PubMed
69. Hume, P. J.,, E. J. McGhie,, R. D. Hayward,, and V. Koronakis. 2003. The purified Shigella IpaB and Salmonella SipB translocators share biochemical properties and membrane topology. Mol. Microbiol. 49:425439. PubMed CrossRef
70. Jamison, W. P.,, and T. Hackstadt. 2008. Induction of type III secretion by cell-free Chlamydia trachomatis elementary bodies. Microb. Pathog. 45:435440. PubMed CrossRef
71. Jewett, T. J.,, C. A. Dooley,, D. J. Mead,, and T. Hackstadt. 2008. Chlamydia trachomatis Tarp is phosphorylated by Src family tyrosine kinases. Biochem. Biophys. Res. Commun. 371:339344. PubMed CrossRef
72. Jewett, T. J.,, E. R. Fischer,, D. J. Mead,, and T. Hackstadt. 2006. Chlamydial TARP is a bacterial nucleator of actin. Proc. Natl. Acad. Sci. USA 103:1559915604. PubMed CrossRef
73. Jewett, T. J.,, N. J. Miller,, C. A. Dooley,, and T. Hackstadt. 2010. The conserved Tarp actin binding domain is important for chlamydial invasion. PLoS Pathog. 6:e1000997. PubMed CrossRef
74. Johnson, D. L.,, and J. B. Mahony. 2007. Chlamydophila pneumoniae PknD exhibits dual amino acid specificity and phosphorylates Cpn0712, a putative type III secretion YscD homolog. J. Bacteriol. 189:75497555. PubMed CrossRef
75. Johnson, D. L.,, C. B. Stone,, and J. B. Mahony. 2008. Interactions between CdsD, CdsQ, and CdsL, three putative Chlamydophila pneumoniae type III secretion proteins. J. Bacteriol. 190:29722980. PubMed CrossRef
76. Joseph, S. S.,, and G. V. Plano. 2007. Identification of TyeA residues required to interact with YopN and to regulate Yop secretion. Adv. Exp. Med. Biol. 603:235245. PubMed CrossRef
77. 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. 21:385389. PubMed CrossRef
78. Karyagina, A. S.,, A. V. Alexeevsky,, S. A. Spirin,, N. A. Zigangirova,, and A. L. Gintsburg. 2009. Effector proteins of chlamydiae. Mol. Biol. 43:897916.
79. Keyser, P.,, M. Elofsson,, S. Rosell,, and H. Wolf-Watz. 2008. Virulence blockers as alternatives to antibiotics: type III secretion inhibitors against Gram-negative bacteria. J. Intern. Med. 264:1729. PubMed CrossRef
80. Kiselev, A. O.,, W. 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:e568e569. PubMed CrossRef
81. Kubori, T.,, A. Sukhan,, S. Aizawa,, and J. Galan. 2000. Molecular characterization and assembly of the needle complex of the Salmonella typhimurium type III secretion system. Proc. Natl. Acad. Sci. USA 97:1022510230. PubMed CrossRef
82. Lad, S. P.,, J. Li,, J. da Silva Correia,, Q. Pan,, S. Gadwal,, R. J. Ulevitch,, and E. Li. 2007a. Cleavage of p65/RelA of the NF-κB pathway by Chlamydia. Proc. Natl. Acad. Sci. USA 104:29332938. PubMed CrossRef
83. Lad, S. P.,, G. Yang,, D. A. Scott,, G. Wang,, P. Nair,, J. Mathison,, V. S. Reddy,, and E. Li. 2007b. Chlamydial CT441 is a PDZ domain-containing tail-specific protease that interferes with the NF-kB pathway of immune responses. J. Bacteriol. 189:66196625. PubMed CrossRef
84. Lawton, W. D.,, R. L. Erdman,, and M. J. Surgalla. 1963. Biosynthesis and purification of V and W antigens in Pasteurella pestis J. Immunol. 91:179184. PubMed
85. Le Negrate, G.,, A. Krieg,, M. L. Faustin,, A. Godzik,, S. Krajewski,, and J. C. Reed. 2008. ChlaDub1 of Chlamydia trachomatis suppresses NF-κB activation and inhibits I-κBα ubiquitination and degradation. Cell. Microbiol. 10:18791892. PubMed CrossRef
86. 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. 192:28522860. PubMed CrossRef
87. Lorenzini, E.,, A. Singer,, B. Singh,, R. Lam,, T. Skarina,, N. Y. Chirgadze,, A. Savchenko,, and R. S. Gupta. 2010. Structure and protein-protein interaction studies on Chlamydia trachomatis protein CT670 (YscO Homolog). J. Bacteriol. 192:27462756. PubMed CrossRef
88. Markham, A. P.,, Z. A. Jaafar,, K. E. Kemege,, C. R. Middaugh,, and P. S. Hefty. 2009. Biophysical characterization of Chlamydia trachomatis CT584 supports its potential role as a type III secretion needle tip protein. Biochemistry 48:1035310361. PubMed CrossRef
89. Marlovits, T. C.,, and C. E. Stebbins. 2009. Type III secretion systems shape up as they ship out. Curr. Opin. Microbiol. 13:16. PubMed CrossRef
90. Marvis, M.,, A. L. Page,, R. Tournebize,, B. Demers,, P. Sansonetti,, and C. Parsot. 2002. Regulation of transcription by the activity of the Shigella flexneri type III secretion apparatus. Mol. Microbiol. 43:15431553. PubMed CrossRef
91. Matson, J. S.,, K. A. Durick,, D. S. Bradley,, and M. L. Nilles. 2005. Immunization of mice with YscF provides protection from Yersinia pestis infections. BMC Microbiol. 24:3848. PubMed CrossRef
92. Matsumoto, A. 1982. Electron microscopic observations of surface projections on Chlamydia psittaci reticulate bodies. J. Bacteriol. 150:358364. PubMed
93. Matsumoto, A., 1988. Structural characteristics of chlamydial bodies, p. 2145. In A. L. Barron (ed.), Microbiology of Chlamydia. CRC Press, Boca Raton, FL.
94. Maurer, A. P.,, A. Mehlitz,, H. J. Mollenkopf,, and T. F. Meyer. 2007. Gene expression profiles of Chlamydophila pneumoniae during the developmental cycle and iron depletion-mediated persistence. PLoS Pathog. 3:752769. PubMed CrossRef
95. Mehlitz, A.,, S. Banhart,, S. Hess,, M. Selback,, and T. F. Meyer. 2008. Complex kinase requirements for Chlamydia trachomatis Tarp phosphorylation. FEMS Microbiol. Lett. 289:233240. PubMed CrossRef
96. Mehlitz, A.,, S. Banhart,, A. P. Maurer,, A. Kaushansky,, A. G. Gordus,, J. Zielecki,, G. MacBeath,, and T. F. Meyer. 2010. Tarp regulates early Chlamydia-induced host cell survival through interactions with the human adaptor protein SHC1. J. Cell Biol. 190:143157. PubMed CrossRef
97. Misaghi, S.,, Z. R. Balsara,, A. Catic,, E. Spooner,, H. L. Ploegh,, and M. N. Starnbach. 2006. Chlamydia trachomatis-derived deubiquitinating enzymes in mammalian cells during infection. Mol. Microbiol. 61:142150. PubMed CrossRef
98. Mital, J.,, N. J. Miller,, E. R. Fischer,, and T. Hackstadt. 2010. Specific chlamydial inclusion membrane proteins associate with active Src family kinases in microdomains that interact with the host microtubule network Cell. Microbiol. 12:12351249. PubMed CrossRef
99. Moraes, T. F.,, T. Spreter,, and N. C. Strynadka. 2008. Piecing together the type III injectisome of bacterial pathogens. Curr. Opin. Struct. Biol. 18:258266. PubMed CrossRef
100. Morita-Ishihara, T.,, M. Ogawa,, H. Sagara,, M. Yoshida,, E. Katayama,, and C. Sasakawa. 2006. Shigella Spa33 is an essential C-ring component of type III secretion machinery. J. Biol. Chem. 281:599607. PubMed CrossRef
101. Mueller, C. A.,, P. Broz,, and G. Cornelis. 2008. The type III secretion system tip complex and translocon. Mol. Microbiol. 68:10851095. PubMed CrossRef
102. Mueller, C. A.,, P. Broz,, S. Muller,, P. Ringler,, F. Erne-Brand,, I. Sorg,, M. Kuhn,, A. Engel,, and G. Cornelis. 2005. The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 310:674676. PubMed CrossRef
103. 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 103:1456614571. PubMed CrossRef
104. Newhall, W. J.,, and R. B. Jones. 1983. Disulfide-linked oligomers of the major outer membrane protein of chlamydiae. J. Bacteriol. 154:344349. PubMed
105. Neyt, C.,, and G. R. Cornelis. 1999. Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD. Mol. Microbiol. 33:971981. PubMed CrossRef
106. Nichols, B. A.,, P. Y. Setzer,, F. Pang,, and C. R. Dawson. 1985. New view of the surface projections of Chlamydia trachomatis. J. Bacteriol. 164:344349. PubMed
107. Niehus, E.,, E. Cheng,, and M. Tan. 2008. DNA supercoiling-dependent gene regulation in Chlamydia. J. Bacteriol. 190:64196427. PubMed CrossRef
108. Page, A. L.,, and C. Parsot. 2002. Chaperones of the type III secretion pathway: jacks of all trades. Mol. Microbiol. 46:111. PubMed CrossRef
109. Pallen, M. J.,, S. A. Beatson,, and C. M. Bailey. 2005. Bioinformatics, genomics and evolution of non-flagellar type III secretion systems: a Darwinian perspective. FEMS Microbiol. Rev. 29:201229. PubMed CrossRef
110. Pallen, M. J.,, M. S. Francis,, and K. Futterer. 2003. Tetratricopeptide-like repeats in type III-secretion chaperones and regulators. FEMS Microbiol. Lett. 223:5360. PubMed
111. Parsot, C.,, C. Hamiaux,, and A. Page. 2003. The various and varying roles of specific chaperones in type III secretion systems. Curr. Opin. Microbiol. 6:714. PubMed
112. Pennini, M. E.,, S. Perrinet,, A. Dautry-Varsat,, and A. Subtil. 2010. Histone methylation by NUE, a novel nuclear effector of the intracellular pathogen Chlamydia trachomatis. PLoS Pathog. 6:e10000995. PubMed CrossRef
113. Quinaud, M.,, J. Chabert,, E. Faudry,, E. Neumann,, D. Lemaire,, A. Pastor,, S. Elsen,, A. Dessen,, and I. Attree. 2005. The PscE-PscF-PscG complex controls type III secretion needle biogenesis in Pseudomonas aeruginosa. J. Biol. Chem. 280:3629336300. PubMed CrossRef
114. Quinaud, M.,, S. Ple,, V. Job,, C. Contreras-Martel,, J. P. Simorre,, I. Attree,, and A. Dessen. 2007. Structure of the heterotrimeric complex that regulates type III secretion needle formation. Proc. Natl. Acad. Sci. USA 104:78037808. PubMed CrossRef
115. Radermacher, A. N.,, and G. R. Crabtree. 2008. Monster protein controls calcium entry and fights infection. Immunity 28:1314. PubMed CrossRef
116. Rao, X.,, P. Deighan,, Z. Hua,, J. Wang,, M. Luo,, J. Wang,, Y. Liang,, G. Zhong,, A. Hochschild,, and L. Shen. 2009. A regulator from Chlamydia trachomatis modulates the activity of RNA polymerase through direct interaction with the beta subunit and the primary sigma subunit. Genes Dev. 23:18181829. PubMed CrossRef
117. Read, T.,, G. Myers,, R. Brunham,, W. Nelson,, I. Paulsen,, J. Heidelberg,, E. Holtzapple,, H. Khouri,, N. Federova,, H. Carty,, L. Umayam,, D. Haft,, J. Peterson,, M. Beanan,, O. White,, S. Salzberg,, R. Hsia,, G. McClarty,, R. Rank,, P. Bavoil,, and C. 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. 31:21342147. PubMed CrossRef
118. 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. 2000. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28:13971406. PubMed CrossRef
119. Ren, Q.,, S. J. Robertson,, D. Howe,, L. F. Barrows,, and R. A. Heizen. 2003. Comparative DNA microarray analysis of host cell transcriptional responses to infection by Coxiella burnetii or Chlamydia trachomatis. Ann. N. Y. Acad. Sci. 990:701713. PubMed
120. Riordan, K. E.,, and O. Schneewind. 2008. YscU cleavage and the assembly of Yersinia type III secretion machine complexes. Mol. Microbiol. 68:14851501. PubMed CrossRef
121. Rockey, D. D.,, and D. T. Alzhanov,. 2006. Proteins in the chlamydial inclusion membrane, p. 234254. In P. Bavoil, and P. B. Wyrick (ed.), Chlamydia: Genomics and Pathogenesis. Horizon Press, Norfolk, United Kingdom.
122. Rockey, D. D.,, D. Grosenbach,, D. E. Hruby,, M. G. Peacock,, R. A. Heinzen,, and T. Hackstadt. 1997. Chlamydia psittaci IncA is phosphorylated by the host cell and is exposed on the cytoplasmic face of the developing inclusion. Mol. Microbiol. 24:217228. PubMed CrossRef
123. Rzomp, K. A.,, A. R. Moorhead,, and M. A. Scidmore. 2006. The GTPase Rab4 interacts with Chlamydia trachomatis inclusion membrane protein CT229. Infect. Immun. 74:53625373. PubMed CrossRef
124. Rzomp, K. A.,, L. D. Scholtes,, B. J. Briggs,, G. R. Whittaker,, and M. A. Scidmore. 2003. Rab GTPases are recruited to chlamydial inclusions in both a species-dependent and species-independent manner. Infect. Immun. 71:58555870. PubMed CrossRef
125. Saier, M. H. 2006. Protein secretion and membrane insertion systems in gram-negative bacteria. J. Membr. Biol. 214:7590. PubMed CrossRef
126. Sambri, V.,, M. Donati,, K. Storni,, M. Di Leo,, M. Agnisdei,, R. Petracca,, O. Finco,, G. Grandi,, G. Ratti,, and C. Cevenini. 2004. Experimental infection by Chlamydia pneumoniae in the hamster. Vaccine 22:11311137. PubMed CrossRef
127. Sawa, T.,, T. Yahr,, M. Ohara,, K. Kurahashi,, M. A. Gropper,, J. P. Wiener-Kronish,, and D. W. Frank. 1999. Active and passive immunization with the Pseudomonas V antigen protects against type III intoxication and lung injury. Nat. Med. 5:392398. PubMed CrossRef
128. Scidmore, M. A. 2011. Recent advances in Chlamydia subversion of host cytoskeletal and membrane trafficking pathways. Microbes Infect. 13:527535. PubMed CrossRef
129. Scidmore, M. A.,, and T. Hackstadt. 2001. Mammalian 14-3-3 beta associates with the Chlamydia trachomatis inclusion membrane via its interaction with IncG. Mol. Microbiol. 39:16381650. PubMed CrossRef
130. Sharma, J.,, Y. Zhong,, F. Dong,, J. M. Piper,, G. Wang,, and G. Zhong. 2006. Profiling of human antibody responses to Chlamydia trachomatis urogenital tract infection using microplates with 156 chlamydial fusion proteins. Infect. Immun. 74:14901499. PubMed CrossRef
131. Silvia-Herzog, E.,, F. Ferracci,, M. W. Jackson,, S. S. Joseph,, and G. V. Plano. 2008. Membrane localization and topology of the Yersinia pestis YscJ lipoprotein. Microbiology 154:593607. PubMed CrossRef
132. Silvia-Herzog, E.,, S. S. Joseph,, A. Avery,, J. Coba,, K. Wolf,, K. A. Fields,, and G. V. Plano. 2011. Scc1 (CP0432) and Scc4 (CP0033) function as a type III secretion chaperone for CopN of Chlamydia pneumoniae. J. Bacteriol. 193:34903496. PubMed CrossRef
133. Sisko, J. L.,, K. Spaeth,, Y. Kumar,, and R. H. Valdivia. 2006. Multifunctional analysis of Chlamydia-specific genes in a yeast expression system. Mol. Microbiol. 60:5166. PubMed CrossRef
134. Slepenkin, A.,, L. M. de la Maza,, and E. M. Peterson. 2005. Interaction between components of the type III secretion system of Chlamydiaceae. J. Bacteriol. 187:473479. PubMed CrossRef
135. Slepenkin, A.,, P. A. Enquist,, U. Hagglund,, L. M. de la Maza,, M. Elofsson,, and E. M. Peterson. 2007. Reversal of the antichlamydial activity of putative type III secretion inhibitors by iron. Infect. Immun. 75:34783489. PubMed CrossRef
136. Slepenkin, A.,, V. Motin,, L. M. de la Maza,, and E. M. Peterson. 2003 Temporal expression of type III secretion genes in Chlamydia pneumoniae. Infect. Immun. 71:25552562. PubMed CrossRef
137. Spaeth, K. E.,, Y. S. Chen,, and R. H. Valdivia. 2009. The Chlamydia type III secretion system C-ring engages a chaperone-effector protein complex. PLoS Pathog. 5:e1000579. PubMed CrossRef
138. 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 282:754759. PubMed CrossRef
139. Stone, C. B.,, D. C. Bulir,, J. D. Gilchrist,, R. K. Toor,, and J. B. Mahony. 2010. Interactions between flagellar and type III secretion proteins in Chlamydia pneumoniae. BMC Microbiol. 10:18. PubMed CrossRef
140. Stone, C. B.,, D. C. Bulir,, C. A. Emdin,, R. M. Pirie,, E. A. Porfilio,, J. W. Slootstra,, and J. B. Mahony. 2011. Chlamydia pneumoniae CdsL regulates CdsN ATPase activity and disruption with a peptide mimetic prevents bacterial invasion. Frontiers Microbiol. doi:10.3389/fmicb.2011.00021. PubMed CrossRef
141. Stone, C. B.,, D. L. Johnson,, D. C. Bulir,, J. D. Gilchrist,, and J. B. Mahony. 2008. Characterization of the putative type III secretion ATPase CdsN (Cpn0707) of Chlamydophila pneumoniae. J. Bacteriol. 190:65806588. PubMed CrossRef
142. Subtil, A.,, C. Delevoye,, M. E. Balana,, L. Tastevin,, S. Perrinet,, and A. Dautry-Varsat. 2005. A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates. Mol. Microbiol. 56:16361647. PubMed CrossRef
143. Subtil, A.,, C. Parsot,, and A. Dautry-Varsat. 2001. Secretion of predicted Inc proteins of Chlamydia pneumoniae by a heterologous type III machinery. Mol. Microbiol. 39:792800. PubMed CrossRef
144. Tammiruusu, A.,, T. Penttila,, R. Lahesmaa,, M. Sarvas,, M. Puolakkainen,, and J. M. Vuola. 2007. Intranasal administration of chlamydial outer protein N (CopN) induces protection against pulmonary Chlamydia pneumoniae infection in a mouse model. Vaccine 25:283290. PubMed CrossRef
145. Tan, C.,, R. Hsia,, H. Shou,, J. Carrasco,, R. Rank,, and P. Bavoil. 2010. Variable expression of surface-exposed polymorphic proteins in in vitro-grown Chlamydia trachomatis. Cell. Microbiol. 12:174187. PubMed CrossRef
146. Tanzer, R. J.,, D. Longbottom,, and T. P. Hatch. 2001. Identification of polymorphic outer membrane proteins of Chlamydia psittaci 6BC. Infect. Immun. 69:24282434. PubMed CrossRef
147. Thalmann, J.,, K. Janik,, M. May,, K. Sommer,, J. Ebeling,, K. Hofmann,, H. Genth,, and A. Klos. 2010. Actin re-organization induced by Chlamydia trachomatis serovar D—evidence for a critical role of the effector protein CT166 targeting Rac. PLoS One doi:10.1371/journal.pone.0009887. PubMed CrossRef
148. Thomas, N. A.,, W. Deng,, J. L. Puente,, E. A. Frey,, C. K. Yip,, N. C. Strynadka,, and B. B. Finlay. 2005. CesT is a multi-effector chaperone and recruitment factor required for the efficient type III secretion of both LEE- and non-LEE-encoded effectors of enteropathogenic Escherichia coli. Mol. Microbiol. 57:17621779. PubMed CrossRef
149. Thomson, N. R.,, C. Yeats,, K. Bell,, M. T. Holden,, S. D. Bentley,, M. Linvingstone,, A. M. Cerdeno-Tarraga,, B. Harris,, J. Doggett,, D. Ormond,, K. Mungall,, K. Clarke,, T. Feltwell,, Z. Hance,, M. Sanders,, M. A. Quail,, C. Price,, B. G. Barrell,, J. Parkhill,, and D. Longbottom. 2005. The Chlamydophila abortus genome sequence reveals an array of variable proteins that contribute to interspecies variation. Genome Res. 15:629640. PubMed CrossRef
150. Tietzel, I.,, C. El-Haibi,, and R. A. Carabeo. 2009. Chlamydial entry involves Tarp binding of guanine nucleotide exchange factors. PLoS Pathog. 4:e1000014.
151. Torruellas, J.,, M. W. Jackson,, J. W. Pennock,, and G. V. Plano. 2005. The Yersinia pestis type III secretion needle plays a role in regulation of Yop secretion. Mol. Microbiol. 57:17191733. PubMed CrossRef
152. Valdivia, R. H. 2008. Chlamydia effector proteins and new insights into chlamydial cellular microbiology. Curr. Opin. Microbiol. 11:5359. PubMed CrossRef
153. Vandahl, B. B.,, A. S. Pedersen,, K. Gevaert,, A. Holm,, J. Vandekerckhove,, J. Christensen,, and S. Birkelund. 2002. The expression, processing and localization of polymorphic membrane proteins in Chlamydia pneumoniae strain CWL029. BMC Microbiol. 2:36. PubMed CrossRef
154. Veenendall, A. K.,, J. L. Hodgkinson,, L. Schwarzer,, D. Stabat,, S. F. Zenk,, and A. Blocker. 2007. The type III secretion system needle tip complex mediates host cell sensing and translocon insertion. Mol. Microbiol. 63:17191730. PubMed CrossRef
155. Verma, A.,, and A. T. Maurelli. 2003. Identification of two eukaryote-like serine/threonine kinases encoded by Chlamydia trachomatis serovar L2 and characterization of interacting partners of Pkn1. Infect. Immun. 71:57725784. PubMed CrossRef
156. Wang, J.,, L. Chen,, F. Chen,, Y. X. Zhang,, J. Baseman,, S. Perdue,, I. T. Hyeh,, R. Shain,, M. J. Holland,, R. L. Bailey,, D. Mabey,, P. Yu,, and G. Zhong. 2009. A chlamydial type III-secreted effector protein (Tarp) is predominantly recognized by antibodies from humans infected with Chlamydia trachomatis and induces protective immunity against upper genital tract pathologies in mice. Vaccine 27:29672980. PubMed CrossRef
157. Wang, J.,, Y. X. Zhang,, C. Lu,, L. Lei,, P. Yu,, and G. Zhong. 2010. A genome-wide profiling of the humoral immune response to Chlamydia trachomatis infection reveals vaccine candidate antigens expressed in humans. J. Immunol. 185:16701680. PubMed CrossRef
158. 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. 51:319334. PubMed CrossRef
159. Wilson, D. P.,, P. Timms,, D. L. McElwain,, and P. Bavoil. 2006. Type III secretion, contact-dependent model for the intracellular development of Chlamydia. Bull. Math. Biol. 68:161178. PubMed CrossRef
160. Wolf, K.,, H. J. Betts,, B. Chellas-Géry,, S. Hower,, C. L. 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. 61:15431555. PubMed CrossRef
161. Wolf, K.,, E. R. Fischer,, and T. Hackstadt. 2000. Ultrastructural analysis of developmental events in Chlamydia pneumoniae-infected cells. Infect. Immun. 68:23792385. PubMed CrossRef
162. Wolf, K.,, G. V. Plano,, and K. A. Fields. 2009. A protein secreted by the respiratory pathogen Chlamydia pneumoniae impairs signaling via interaction with human Act1. Cell. Microbiol. 11:769779. PubMed CrossRef
163. Yip, C. K.,, T. G. Kimbrough,, H. B. Felise,, M. Vuckovic,, N. A. Thomas,, R. A. Pfuetzner,, E. A. Frey,, B. B. Finlay,, S. I. Miller,, and N. C. Strynadka,. 2005. Structural characterization of the molecular platform for type III secretion system assembly. Nature 435:702707. PubMed CrossRef
164. Zhong, G. 2009. Killing me softly: chlamydial use of proteolysis for evading host defenses. Trends Microbiol. 17:467473. PubMed CrossRef
165. Zhong, G.,, P. Fan,, H. Ji,, F. Dong,, and Y. Huang. 2001. Identification of a chlamydial protease-like activity factor responsible for the degradation of host transcription factors. J. Exp. Med. 193:935942. PubMed CrossRef

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