1887

Chapter 6 : Initial Interactions of Chlamydiae with the Host Cell

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

Preview this chapter:
Zoom in
Zoomout

Initial Interactions of Chlamydiae with the Host Cell, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817329/9781555816742_Chap06-1.gif /docserver/preview/fulltext/10.1128/9781555817329/9781555816742_Chap06-2.gif

Abstract:

Chlamydiae are taken up by host cells so efficiently that the process has been termed "parasite-specified endocytosis" by Byrne and Moulder. This chapter focuses upon the active interactions of chlamydiae with the host cell and covers the stage of development up to the division of reticulate bodies (RBs). Surprisingly, different mutant cell lines displayed unique patterns of susceptibility or resistance to different serovars or to . Despite the difficulties of comparing studies between different chlamydial species or serovars, conditions, and cell types, there is sufficient evidence to suggest that individual chlamydiae are capable of utilizing different mechanisms for entry. Translocation of Tarp and its tyrosine phosphorylation appear to be one of the first means of communication with the host cell to actively subvert host processes for parasite purposes. Identification of the kinases mediating Tarp phosphorylation is an initial step in mapping the signal transduction networks initiated by to establish residence within an intracellular niche. Endocytosed elementary bodies (EBs) are rapidly transported to the peri-Golgi region of the host cell and become fusogenic with Golgi-derived vesicles. The Inc proteins do not share structural similarities to eukaryotic proteins, except for SNARE-like motifs, and homology searches do not provide substantial clues about their function. An improved understanding of the complex interactions of the important pathogens with the host cell should provide great potential for improved chemotherapeu-tic and immunoprophylactic interventions.

Citation: Hackstadt T. 2012. Initial Interactions of Chlamydiae with the Host Cell, p 126-148. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch6

Key Concept Ranking

Bacterial Proteins
0.59204525
Plasma Membrane
0.49890125
Small Interfering RNA
0.4751402
0.59204525
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Model of cooperative cell signaling during the internalization of . Upon contact with the eukaryotic host cell, Tarp is translocated from EBs by the chlamydial T3S system and exposed to the cytosol. Tarp, but not that of other species, is tyrosine phosphorylated by host kinases. A variety of host proteins display affinity for tyrosine phosphorylated Tarp. These include those potentially acting as GEFs for activation of Rac as well as those functioning in cellular signaling pathways regulating apoptosis and other regulatory cascades. Tarp is believed to independently nucleate linear actin filament formation. Rac activation, and CDC42 for , is required for activation of the cellular actin nucleating complex, Arp2/3. Tarp and Arp2/3 are proposed to function synergistically to promote the actin cytoskeletal rearrangements promoting chlamydial internalization. The mechanisms of Rac and/or CDC42 activation by those species whose Tarp is not phosphorylated, or when Tarp phosphorylation is inhibited, are undefined. Tarp is not predicted to be a membrane protein but remains associated with the nascent inclusion membrane for several hours postinfection. The means for long-term retention at the inclusion membrane is unknown. doi:10.1128/9781555817329.ch6.f1

Citation: Hackstadt T. 2012. Initial Interactions of Chlamydiae with the Host Cell, p 126-148. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch6
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Model of the vesicular interactions of the mature chlamydial inclusion. Markers for the plasma membrane and fluid phase and early and late endosomal and lysosomal markers are absent from the inclusion membrane. Instead, chlamydiae intercept sphingolipids and cholesterol directly from the Golgi apparatus. All chlamydial species interact with cells similarly. These interactions require modification of the inclusion membrane by chlamydial protein(s) and are initiated by 2 h postinfection. doi:10.1128/9781555817329.ch6.f2

Citation: Hackstadt T. 2012. Initial Interactions of Chlamydiae with the Host Cell, p 126-148. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch6
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Sources of lipids for chlamydiae. Chlamydiae utilize multiple host sources for lipid acquisition. doi:10.1128/9781555817329.ch6.f3

Citation: Hackstadt T. 2012. Initial Interactions of Chlamydiae with the Host Cell, p 126-148. In Tan M, Bavoil P (ed), Intracellular Pathogens I: . ASM Press, Washington, DC. doi: 10.1128/9781555817329.ch6
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555817329.chap6
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. Backert, S.,, and M. Selbach. 2005. Tyrosine-phosphorylated bacterial effector proteins: the enemies within. Trends Microbiol. 13: 476 484. PubMed CrossRef
3. Bahrani, F. K.,, P. J. Sansonetti,, and C. Parsot. 1997. Secretion of Ipa proteins by Shigella flexneri: inducer molecules and kinetics of activation. Infect. Immun. 65: 4005 4010. PubMed
4. 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: 35 47. PubMed CrossRef
5. Bannantine, J. P.,, D. D. Rockey,, and T. Hackstadt. 1998. Tandem genes of Chlamydia psittaci that encode proteins localized to the inclusion membrane. Mol. Microbiol. 28: 1017 1026. PubMed CrossRef
6. 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
7. Beatty, W. L. 2008. Late endocytic multivesicular bodies intersect the chlamydial inclusion in the absence of CD63. Infect. Immun. 76: 2872 2881. PubMed CrossRef
8. 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: 13984 13989. PubMed CrossRef
9. 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: 8478 8483. PubMed CrossRef
10. Brickman, T. J.,, C. E. Barry III,, and T. Hackstadt. 1993. Molecular cloning and expression of hctB encoding a strain-variant chlamydial histone-like protein with DNA-binding activity. J. Bacteriol. 175: 4274 4281. PubMed
11. Brumell, J. H.,, and M. A. Scidmore. 2007. Manipulation of Rab GTPase function by intracellular bacterial pathogens. Microbiol. Mol. Biol. Rev. 71: 636 652. PubMed CrossRef
12. 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
13. Campbell, S.,, S. J. Richmond,, and P. Yates. 1989a. The development of Chlamydia trachomatis inclusions within the host eukaryotic cell during interphase and mitosis. J. Gen. Microbiol. 135: 1153 1165. PubMed CrossRef
14. Campbell, S.,, S. J. Richmond,, and P. S. Yates. 1989b. The effect of Chlamydia trachomatis infection on the host cell cytoskeleton and membrane compartments. J. Gen. Microbiol. 135: 2379 2386. PubMed CrossRef
15. Capmany, A.,, and M. T. Damiani. 2010. Chlamydia trachomatis intercepts Golgi-derived sphingolipids through a Rab14-mediated transport required for bacterial development and replication. PLoS One 5: e14084. PubMed CrossRef
16. Carabeo, R. A.,, C. A. Dooley,, S. S. Grieshaber,, and T. Hackstadt. 2007. Rac interacts with Abi-1 and WAVE2 to promote an Arp2/3-dependent actin recruitment during chlamydial invasion. Cell. Microbiol. 9: 2278 2288. PubMed CrossRef
17. Carabeo, R. A.,, S. Grieshaber,, A. Hasenkrug,, C. A. Dooley,, and T. Hackstadt. 2004. Requirement for the Rac GTPase in Chlamydia trachomatis invasion of non-phagocytic cells. Traffic 5: 418 425. PubMed CrossRef
18. Carabeo, R. A.,, S. S. Grieshaber,, E. Fischer,, and T. Hackstadt. 2002. Chlamydia trachomatis induces remodeling of the actin cytoskeleton during attachment and entry into HeLa cells. Infect. Immun. 70: 3793 3803. PubMed
19. 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 CrossRef
20. 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
21. Carlson, J. H.,, S. Hughes,, D. Hogan,, G. Cieplak,, D. Sturdevant,, G. McClarty,, H. D. Caldwell,, and R. J. Belland. 2004. Polymorphisms in the Chlamydia trachomatis cytotoxin locus associated with ocular and genital isolates. Infect. Immun. 72: 7063 7072. PubMed CrossRef
22. 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: 41320 41327. PubMed CrossRef
23. Clausen, J. D.,, G. Christiansen,, H. U. Holst,, and S. Birkelund. 1997. Chlamydia trachomatis utilizes the host cell microtubule network during early events of infection. Mol. Microbiol. 25: 441 449. PubMed CrossRef
24. Clifton, D. R.,, C. A. Dooley,, S. S. Grieshaber,, R. A. Carabeo,, K. A. Fields,, and T. Hackstadt. 2005. Tyrosine phosphorylation of chlamydial Tarp is species specific and not required for the recruitment of actin. Infect. Immun. 73: 3860 3868. PubMed CrossRef
25. Clifton, D. R.,, K. A. Fields,, S. Grieshaber,, C. A. Dooley,, E. Fischer,, D. 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
26. Cocchiaro, J.,, 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
27. Coers, J.,, I. Bernstein-Hanley,, D. Grotsky,, I. Parvanova,, J. C. Howard,, G. A. Taylor,, W. F. Dietrich,, and M. N. Starnbach. 2008. Chlamydia muridarum evades growth restriction by the IFN-gamma-inducible host resistance factor Irgb10. J. Immunol. 180: 6237 6245. PubMed
28. Conant, C. G.,, and R. S. Stephens. 2007. Chlamydia attachment to mammalian cells requires protein disulfide isomerase. Cell. Microbiol. 9: 222 232. PubMed CrossRef
29. Coombes, B. K.,, and J. B. Mahony. 2002. Identification of MEK- and phosphoinositide 3-kinase-dependent signalling as essential events during Chlamydia pneumoniae invasion of HEp2 cells. Cell. Microbiol. 4: 447 460. PubMed CrossRef
30. 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: 5586 5596. PubMed CrossRef
31. 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
32. 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
33. Dehoux, P.,, R. Flores,, C. Dauga,, G. Zhong,, and A. Subtil. 2011. Multi-genome identification and characterization of chlamydiae-specific type III secretion substrates: the Inc proteins. BMC Genomics 12: 109. PubMed CrossRef
34. Delevoye, C.,, M. Nilges,, P. Dehoux,, F. Paumet,, S. Perrinet,, A. Dautry-Varsat,, and A. Subtil. 2008. SNARE protein mimicry by an intracellular bacterium. PLoS Pathog. 4: e1000022. PubMed CrossRef
35. Derre, I.,, M. Pypaert,, A. Dautry-Varsat,, and H. Agaisse. 2007. RNAi screen in Drosophila cells reveals the involvement of the Tom complex in Chlamydia infection. PLoS Pathog. 3: 1446 1458. PubMed CrossRef
36. Dessus-Babus, S.,, S. T. Knight,, and P. B. Wyrick. 2000. Chlamydial infection of polarized HeLa cells induces PMN chemotaxis but the cytokine profile varies between disseminating and non-disseminating strains. Cell. Microbiol. 2: 317 327. PubMed CrossRef
37. DeVinney, R.,, J. L. Puente,, A. Gauthier,, D. Goosney,, and B. Finlay. 2001. Enterohaemorrhagic and enteropathogenic Escherichia coli use different Tir-based mechanism for pedestal formation. Mol. Microbiol. 41: 1445 1458. PubMed CrossRef
38. 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
39. Fields, K. A.,, and T. Hackstadt. 2000. Evidence for the secretion of Chlamydia trachomatis CopN by a type III secretion mechanism. Mol. Microbiol. 38: 1048 1060. PubMed CrossRef
40. Fields, K. A.,, and T. Hackstadt. 2002. The chlamydial inclusion: escape from the endocytic pathway. Annu. Rev. Cell Dev. Biol. 18: 221 245. PubMed CrossRef
41. Fields, K. A.,, D. 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
42. Fudyk, T.,, L. Olinger,, and R. S. Stephens. 2002. Selection of mutant cell lines resistant to infection by Chlamydia trachomatis and Chlamydia pneumoniae. Infect. Immun. 70: 6444 6447. PubMed CrossRef
43. Gabel, B. R.,, S. C. Ijzendoorn,, and J. N. Engel. 2004. Lipid raft-mediated entry is not required for Chlamydia trachomatis infection of cultured epithelial cells. Infect. Immun. 72: 7367 7373. PubMed CrossRef
44. Grieshaber, N.,, E. Fischer,, D. 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
45. Grieshaber, N. A.,, S. S. Grieshaber,, E. R. Fischer,, and T. Hackstadt. 2006. A small RNA inhibits translation of the histone-like protein Hc1 in Chlamydia trachomatis. Mol. Microbiol. 59: 541 550. PubMed CrossRef
46. Grieshaber, S.,, N. Grieshaber,, and T. Hackstadt. 2003. Chlamydia trachomatis uses host cell dynein to traffic to the microtube organizing center in a p50 dynamitin independent process. J. Cell Biol. 116: 3793 3802. PubMed CrossRef
47. Gruenheid, S.,, R. DeVinney,, F. Bladt,, D. Goosney,, S. Gelkp,, G. D. Gish,, T. Pawson,, and B. Finlay. 2001. Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat. Cell Biol. 3: 856 859. PubMed CrossRef
48. Guseva, N. V.,, S. T. Knight,, J. D. Whittimore,, and P. B. Wyrick. 2003. Primary cultures of female swine genital epithelial cells in vitro: a new approach for the study of hormonal modulation of chlamydia infection. Infect. Immun. 71: 4700 4710. PubMed CrossRef
49. Hackstadt, T., 1999. Cell biology, p. 101 138. In R. S. Stephens (ed.), Chlamydia: Intracellular Biology, Pathogenesis, and Immunity. ASM Press, Washington, DC.
50. Hackstadt, T. 2000. Redirection of host vesicle trafficking pathways by intracellular parasites. Traffic 1: 93 99. PubMed CrossRef
51. Hackstadt, T.,, W. Baehr,, and Y. Ying. 1991. Chlamydia trachomatis developmentally regulated protein is homologous to eukaryotic histone a. Proc. Natl. Acad. Sci. USA 88: 3937 3941. PubMed
52. Hackstadt, T.,, E. R. Fischer,, M. A. Scidmore,, D. D. Rockey,, and R. A. Heinzen. 1997. Origins and functions of the chlamydial inclusion. Trends Microbiol. 5: 288 293. PubMed CrossRef
53. Hackstadt, T.,, D. D. Rockey,, R. A. Heinzen,, and M. A. Scidmore. 1996. Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J. 15: 964 977. PubMed
54. Hackstadt, T.,, M. A. Scidmore-Carlson,, E. I. Shaw,, and E. R. Fischer. 1999. The Chlamydia trachomatis IncA protein is required for homotypic vesicle fusion. Cell. Microbiol. 1: 119 130. PubMed CrossRef
55. 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
56. Hatch, T. P.,, M. Miceli,, and J. A. Silverman. 1985. Synthesis of protein in host-free reticulate bodies of Chlamydia psittaci and Chlamydia trachomatis. J. Bacteriol. 162: 938 942. PubMed
57. Hayward, R. D.,, R. J. Cain,, E. J. McGhie,, N. Phillips,, M. J. Garner,, and V. Koronakis. 2005. Cholesterol binding by the bacterial type III translocon is essential for virulence effector delivery into mammalian cells. Mol. Microbiol. 56: 590 603. PubMed CrossRef
58. Heinzen, R. A.,, and T. Hackstadt. 1997. The Chlamydia trachomatis parasitophorous vacuolar membrane is not passively permeable to low-molecular-weight compounds. Infect. Immun. 65: 1088 1094. PubMed
59. 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
60. 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
61. 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: 1423 1437. PubMed CrossRef
62. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62: 379 433. PubMed
63. Igietseme, J. U.,, P. B. Wyrick,, D. Goyeau,, and R. G. Rank. 1994. An in vitro model for immune control of chlamydial growth in polarized epithelial cells. Infect. Immun. 62: 3528 3535. PubMed
64. Jamison, W. P.,, and T. Hackstadt. 2008. Induction of type III secretion by cell-free Chlamydia trachomatis elementary bodies. Microb. Pathog. 45: 435 440. PubMed CrossRef
65. 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: 339 344. PubMed CrossRef
66. 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: 15599 15604. PubMed CrossRef
67. 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
68. Kane, C. D.,, and G. I. Byrne. 1998. Differential effects of γ interferon on Chlamydia trachomatis growth in polarized and nonpolarized human epithelial cells in culture. Infect. Immun. 66: 2349 2351. PubMed
69. Kumar, Y.,, J. Cocchiaro,, and R. H. Valdivia. 2006. The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. Curr. Biol. 16: 1646 1651. PubMed CrossRef
70. Kumar, Y.,, and R. H. Valdivia. 2008. Actin and intermediate filaments stabilize the Chlamydia trachomatis vacuole by forming dynamic structural scaffolds. Cell Host Microbe 4: 159 169. PubMed CrossRef
71. Lad, S. P.,, J. Li,, J. da Silva Correia,, Q. Pan,, S. Gadwal,, R. J. Ulevitch,, and E. Li. 2007. Cleavage of p65/RelA of the NF-kappaB pathway by Chlamydia. Proc. Natl. Acad. Sci. USA 104: 2933 2938. PubMed CrossRef
72. Lane, B. J.,, C. Mutchier,, S. Al Khodor,, S. S. Grieshaber,, and R. A. Carabeo. 2008. Chlamydial entry involves TARP binding of guanine nucleotide exchange factors. PLoS Pathog. 4: e1000014. PubMed
73. Lee, V. T.,, S. K. Mazmanian,, and O. Schneewind. 2001. A program of Yersinia enterocolitica type III secretion reactions is activated by specific signals. J. Bacteriol. 183: 4970 4978. PubMed CrossRef
74. Li, Z.,, C. Chen,, D. Chen,, Y. Wu,, Y. Zhong,, and G. Zhong. 2008. Characterization of fifty putative inclusion membrane proteins encoded in the Chlamydia trachomatis genome. Infect. Immun. 76: 2746 2757. PubMed CrossRef
75. Lipsky, N. G.,, and R. E. Pagano. 1985a. Intracellular translocation of fluorescent sphingolipids in cultured fibroblasts: endogenously synthesized sphingomyelin and glucocerebroside analogues pass through the Golgi apparatus en route to the plasma membrane. J. Cell Biol. 100: 27 34. PubMed
76. Lipsky, N. G.,, and R. E. Pagano. 1985b. A vital stain for the Golgi apparatus. Science 228: 745 747. PubMed CrossRef
77. Lutter, E. I.,, C. Bonner,, M. Holland,, R. J. Suchland,, W. E. Stamm,, T. J. Jewett,, G. McClarty,, and T. Hackstadt. 2010. Phylogenetic analysis of Chlamydia trachomatis Tarp and correlation with clinical phenotype. Infect. Immun. 78: 3678 3688. PubMed CrossRef
78. Majeed, M.,, and E. Kihlstrom. 1991. Mobilization of F-actin and clathrin during redistribution of Chlamydia trachomatis to an intracellular site in eucaryotic cells. Infect. Immun. 59: 4465 4472. PubMed
79. 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
80. Matsumoto, A.,, H. Bessho,, K. Uehira,, and T. Suda. 1991. Morphological studies of the association of mitochondria with chlamydial inclusions and the fusion of chlamydial inclusions. J. Electron Microsc. 40: 356 363. PubMed
81. McBride, T.,, and E. Wilde III,. 1990. Intracellular translocation of Chlamydia trachomatis, p. 36 39. In W. R. Bowie,, H. D. Caldwell,, R. P. Jones, et al. (ed.), Chlamydial Infections. Cambridge University Press, Cambridge, United Kingdom.
82. Mehlitz, A.,, S. Banhart,, S. Hess,, M. Selbach,, and T. F. Meyer. 2008. Complex kinase requirements for Chlamydia trachomatis Tarp phosphorylation. FEMS Microbiol. Lett. 289: 233 240. PubMed CrossRef
83. 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: 143 157. PubMed CrossRef
84. 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: 142 150. PubMed CrossRef
85. 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: 1235 1249. PubMed CrossRef
86. Moore, E. R.,, E. R. Fischer,, D. J. Mead,, and T. Hackstadt. 2008. The chlamydial inclusion preferentially intercepts basolaterally directed sphingomyelin-containing exocytic vacuoles. Traffic 9: 2130 2140. PubMed CrossRef
87. Moore, E. R.,, D. J. Mead,, C. A. Dooley,, J. Sager,, and T. Hackstadt. 2011. The trans-Golgi SNARE syntaxin 6 is recruited to the chlamydial inclusion membrane. Microbiology 157: 830 838. PubMed CrossRef
88. Moorhead, A. M.,, J. Y. Jung,, A. Smirnov,, S. Kaufer,, and M. A. Scidmore. 2010. Multiple host proteins that function in phosphatidylinositol-4-phosphate metabolism are recruited to the chlamydial inclusion. Infect. Immun. 78: 1990 2007. PubMed CrossRef
89. Moorhead, A. R.,, K. A. Rzomp,, and M. A. Scidmore. 2007. The Rab6 effector Bicaudal D1 associates with Chlamydia trachomatis inclusions in a biovar-specific manner. Infect. Immun. 75: 781 791. PubMed CrossRef
90. Moulder, J. W. 1991. Interaction of chlamydiae and host cells in vitro. Microbiol. Rev. 55: 143 190. PubMed
91. Nelson, D. E., et al. 2005. Chlamydial interferon gamma immune evasion is linked to host infection tropism. Proc. Natl. Acad. Sci. USA 102: 10658 10663. PubMed CrossRef
92. 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.
93. Novick, P.,, and M. Zerial. 1997. The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol. 9: 496 504. PubMed
94. Parlati, F.,, O. Varlamov,, K. Paz,, J. A. McNew,, D. Hurtado,, T. H. Sollner,, and J. E. Rothman. 2002. Distinct SNARE complexes mediating membrane fusion in Golgi transport based on combinatorial specificity. Proc. Natl. Acad. Sci. USA 99: 5424 5429. PubMed CrossRef
95. Paumet, F.,, J. Wesolowski,, A. Garcia-Diaz,, C. Delevoye,, N. Aulner,, H. A. Shuman,, A. Subtil,, and J. E. Rothman. 2009. Intracellular bacteria encode inhibitory SNARE-like proteins. PLoS ONE 4: e7375. PubMed CrossRef
96. Perara, E.,, D. Ganem,, and J. N. Engel. 1992. A developmentally regulated chlamydial gene with apparent homology to eukaryotic histone a. Proc. Natl. Acad. Sci. USA 89: 2125 2129. PubMed
97. Pirbhai, M.,, F. Dong,, Y. Zhong,, K. Z. Pan,, and G. Zhong. 2006. The secreted protease factor CPAF is responsible for degrading pro-apoptotic BC-only proteins in Chlamydia trachomatis-infected cells. J. Biol. Chem. 281: 31495 31501. PubMed CrossRef
98. Prain, C. J.,, and J. H. Pearce. 1989. Ultrastructural studies on the intracellular fate of Chlamydia psittaci (strain guinea pig inclusion conjunctivitis) and Chlamydia trachomatis (strain lymphogranuloma venereum 434): modulation of intracellular events and relationship with endocytic mechanism. J. Gen. Microbiol. 135: 2107 2123. PubMed
99. Qualmann, B.,, and M. M. Kessels. 2009. New players in actin polymerization—Wb-domain-containing actin nucleators. Trends Cell Biol. 19: 276 285. PubMed CrossRef
100. Read, T. D., et al. 2000. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28: 1397 1406. PubMed
101. Read, T. D., et al. 2003. Genome sequence of Chlamydiophila caviae ( Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. Nucleic Acids Res. 31: 2134 2147. PubMed
102. Rejman Lipinski, A.,, J. Heymann,, C. Meissner,, A. Karlas,, V. Brinkmann,, T. F. Meyer,, and D. Heuer. 2009. Rab6 and Rab11 regulate Chlamydia trachomatis development and golgin-84-dependent Golgi fragmentation. PLoS Pathog. 5: e1000615. PubMed CrossRef
103. Ridderhof, J. C.,, and R. C. Barnes. 1989. Fusion of inclusions following superinfection of HeLa cells by two serovars of Chlamydia trachomatis. Infect. Immun. 57: 3189 3193. PubMed
104. Rivera-Amill, V.,, B. J. Kim,, J. Seshu,, and M. E. Konkel. 2001. Secretion of the virulence-associated Campylobacter invasion antigens from Campylobacter jejuni requires a stimulatory signal. J. Infect. Dis. 183: 1607 1616. PubMed CrossRef
105. Robertson, D. K.,, L. Gu,, R. K. Rowe,, and W. L. Beatty. 2009. Inclusion biogenesis and reactivation of persistent Chlamydia trachomatis requires host cell sphingolipid biosynthesis. PLoS Pathog. 5: e1000664. PubMed CrossRef
106. Robinson, R. C.,, K. Turbedsky,, D. A. Kaiser,, J. B. Marchand,, H. N. Higgs,, S. Choe,, and T. D. Pollard. 2001. Crystal structure of Arp2/3 complex. Science 294: 1679 1684. PubMed CrossRef
107. 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: 217 228. PubMed
108. Rockey, D. D.,, R. A. Heinzen,, and T. Hackstadt. 1995. Cloning and characterization of a Chlamydia psittaci gene coding for a protein localized in the inclusion membrane of infected cells. Mol. Microbiol. 15: 617 626. PubMed
109. Rockey, D. D.,, and J. L. Rosquist. 1994. Protein antigens of Chlamydia psittaci present in infected cells but not detected in the infectious elementary body. Infect. Immun. 62: 106 112. PubMed
110. Rockey, D. D.,, M. A. Scidmore,, J. P. Bannantine,, and W. J. Brown. 2002. Proteins in the chlamydial inclusion membrane. Microbes Infect. 4: 333 340. PubMed
111. Rothman, J. E.,, and F. T. Wieland. 1996. Protein sorting by transport vesicles. Science 272: 227 234. PubMed
112. 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: 5362 5373. PubMed CrossRef
113. 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: 5855 5870. PubMed
114. Schimmoller, F.,, I. Simon,, and S. R. Pfeffer. 1998. Rab GTPases, directors of vesicle docking. J. Biol. Chem. 273: 22161 22164. PubMed
115. Schramm, N.,, and P. B. Wyrick. 1995. Cytoskeletal requirements in Chlamydia trachomatis infection of host cells. Infect. Immun. 63: 324 332. PubMed
116. Scidmore, M. A.,, E. Fischer,, and T. Hackstadt. 2003. Restricted fusion of Chlamydia trachomatis vesicles with endocytic compartments during the initial stages of infection. Infect. Immun. 71: 973 984. PubMed
117. 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
118. Scidmore, M. A.,, and T. Hackstadt. 2001. Mammalian 14-3-3beta associates with the Chlamydia trachomatis inclusion membrane via its interaction with IncG. Mol. Microbiol. 39: 1638 1650. PubMed
119. 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
120. 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
121. Sinai, A. P.,, and K. A. Joiner. 1997. Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu. Rev. Microbiol. 51: 415 462. PubMed CrossRef
122. Stephens, R. S., et al. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282: 754 759. PubMed
123. Stuart, E. S.,, W. C. Webley,, and L. C. Norkin. 2003. Lipid rafts, caveolae, caveolin-1, and entry by chlamydiae into host cells. Exp. Cell. Res. 287: 67 78. PubMed
124. Su, H.,, G. McClarty,, F. Dong,, G. M. Hatch,, Z. Pan, K,, 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
125. 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: 792 800. PubMed
126. Subtil, A.,, B. Wyplosz,, M. E. Balana,, and A. Dautry-Varsat. 2004. Analysis of Chlamydia caviae entry sites and involvement of Cdc42 and Rac activity. J. Cell Sci. 117: 3923 3933. PubMed CrossRef
127. Suchland, R. J.,, D. D. Rockey,, J. P. Bannantine,, and W. E. Stamm. 2000. Isolates of Chlamydia trachomatis that occupy nonfusogenic inclusions lack IncA, a protein localized to the inclusion membrane. Infect. Immun. 68: 360 367. PubMed
128. Tao, S.,, R. Kaul,, and W. M. Wenman. 1991. Identification and nucleotide sequence of a developmentally regulated gene encoding a eukaryotic histone a-like protein from Chlamydia trachomatis. J. Bacteriol. 173: 2818 2822. PubMed
129. Taraska, T.,, D. M. Ward,, R. S. Ajioka,, P. B. Wyrick,, S. R. Davis-Kaplan,, C. H. Davis,, and J. Kaplan. 1996. The late chlamydial inclusion membrane is not derived from the endocytic pathway and is relatively deficient in host proteins. Infect. Immun. 64: 3713 3727.
130. Tipples, G.,, and G. McClarty. 1993. The obligate intracellular bacterium Chlamydia trachomatis is auxotrophic for three of the four ribonucleoside triphosphates. Mol. Microbiol. 8: 1105 1114. PubMed
131. van der Goot, F. G.,, G. Tran van Nhieu,, A. Allaoui,, P. Sansonetti,, and F. Lafont. 2004. Rafts can trigger contact-mediated secretion of bacterial effectors via a lipid-based mechanism. J. Biol. Chem. 279: 47792 47798. PubMed CrossRef
132. van Meer, G.,, E. H. K. Stelzer,, R. W. Winjnaendts-van-Resandt,, and K. Simons. 1987. Sorting of sphingolipids in epithelial (Madin-Darby Canine Kidney) cells. J. Cell Biol. 105: 1623 1635. PubMed
133. van Ooij, C.,, G. Apodaca,, and J. Engel. 1997. Characterization of the Chlamydia trachomatis vacuole and its interaction with the host endocytic pathway in HeLa cells. Infect. Immun. 65: 758 766. PubMed
134. van Ooij, C.,, L. Kalman,, S. van Ijzendoorn,, M. Nishijima,, K. Hanada,, K. Mostov,, and J. N. Engel. 2000. Host cell-derived sphingolipids are required for the intracellular growth of Chlamydia trachomatis. Cell. Microbiol. 2: 627 637. PubMed
135. van'tHof, W.,, and G. vanMeer. 1990. Generation of lipid polarity in intestinal epithelial (Caco-2) cells: sphingolipid synthesis in the Golgi complex and sorting before vesicular traffic to the plasma membrane. J. Cell Biol. 111: 977 986. PubMed
136. Verbeke, P.,, L. Welter-Stahl,, S. Ying,, J. Hansen,, G. Hacker,, T. Darville,, and D. M. Ojcius. 2006. Recruitment of BAD by the Chlamydia trachomatis vacuole correlates with host-cell survival. PLoS Pathog. 2: e45. PubMed CrossRef
137. Wagar, E. A.,, and R. S. Stephens. 1988. Developmental-form-specific DNA-binding proteins in Chlamydia spp. Infect. Immun. 56: 1678 1684. PubMed
138. Wolf, K.,, G. V. Plano,, and K. A. Fields. 2009. A protein secreted by the respiratory pathogen Chlamydia pneumoniae impairs IL-17 signaling via interaction with human Act1. Cell. Microbiol. 11: 767 779. PubMed CrossRef
139. 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
140. Wyrick, P. B. 2000. Intracellular survival by Chlamydia. Cell. Microbiol. 2: 275 282. PubMed
141. 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
142. Wyrick, P. B.,, C. H. Davis,, S. T. Knight,, J. Choong,, J. E. Raulston,, and N. Schramm. 1993. An in vitro human epithelial cell culture system for studying the pathogenesis of Chlamydia trachomatis. Sex. Transm. Dis. 20: 248 256. PubMed
143. Zhong, G. 2009. Killing me softly: chlamydial use of proteolysis for evading host defenses. Trends Microbiol. 17: 467 474. PubMed CrossRef
144. 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: 935 942. PubMed

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