Altered protein secretion of chlamydia trachomatis in persistently infected human endocervical epithelial cells

Microbiology

Volumn 157, Issue 10, 2011, Pages 2759-2771

  Wang, Jin ^a,d   Frohlich, Kyla M ^a   Buckner, Lyndsey ^a   Quayle, Alison J ^a   Luo, Miao ^a   Feng, Xiaogeng ^a   Beatty, Wandy ^b   Hua, Ziyu ^a   Rao, Xiancai ^a   Lewis, Maria E ^a   Sorrells, Kelly ^a   Santiago, Kerri ^a   Zhong, Guangming ^c   Shen, Li ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c University of Texas Health Science Center   (United States)

^d PEKING UNIVERSITY FIRST HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BACTERIAL PROTEIN; CHLAMYDIAL PROTEASE LIKE ACTIVITY FACTOR; PROTEIN COPN; PROTEIN TARP; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM CELL; GENE CONTROL; GENE EXPRESSION; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; UTERINE CERVICITIS; UTERINE CERVIX EPITHELIUM;

BACTERIAL PROTEINS; CELL LINE; CERVIX UTERI; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; DOWN-REGULATION; ENDOPEPTIDASES; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; PROTEIN TRANSPORT; UTERINE CERVICAL DISEASES;

BACTERIA (MICROORGANISMS); CHLAMYDIA TRACHOMATIS;

EID: 80053457725     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.044917-0     Document Type: Article

References (58)

1. Amano, A., Takeuchi, H. & Furuta, N. (2010). Outer membrane vesicles function as offensive weapons in host-parasite interactions. Microbes Infect 12, 791-798.
2. Bannantine, J. P., Stamm, W. E., Suchland, R. J. & Rockey, D. D. (1998). Chlamydia trachomatis IncA is localized to the inclusion membrane and is recognized by antisera from infected humans and primates. Infect Immun 66, 6017-6021.
3. 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.
4. Beatty, W. L., Morrison, R. P. & Byrne, G. I. (1994). Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol Rev 58, 686-699.
5. Belland, R. J., Nelson, D. E., Virok, D., Crane, D. D., Hogan, D., Sturdevant, D., Beatty, W. L. & Caldwell, H. D. (2003). Transcriptome analysis of chlamydial growth during IFN-gamma-mediated persistence and reactivation. Proc Natl Acad Sci U S A 100, 15971-15976.
6. Betts, H. J., Wolf, K. & Fields, K. A. (2009). Effector protein modulation of host cells: examples in the Chlamydia spp. arsenal. Curr Opin Microbiol 12, 81-87.
7. Brunham, R. C. & Rey-Ladino, J. (2005). Immunology of Chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat Rev Immunol 5, 149-161.
8. Chen, D., Lei, L., Lu, C., Flores, R., DeLisa, M. P., Roberts, T. C., Romesberg, F. E. & Zhong, G. (2010). Secretion of the chlamydial virulence factor CPAF requires the Sec-dependent pathway. Microbiology 156, 3031-3040.
9. Clifton, D. R., Fields, K. A., Grieshaber, S. S., Dooley, C. A., Fischer, E. R., Mead, D. J., Carabeo, R. A. & Hackstadt, T. (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 U S A 101, 10166-10171.
10. Cocchiaro, J. L., Kumar, Y., Fischer, E. R., Hackstadt, T. & Valdivia, R. H. (2008). Cytoplasmic lipid droplets are translocated into he lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc Natl Acad Sci U S A 105, 9379-9384.
11. Deka, S., Vanover, J., Dessus-Babus, S., Whittimore, J., Howett, M. K., Wyrick, P. B. & Schoborg, R. V. (2006). Chlamydia trachomatis enters a viable but non-cultivable (persistent) state within herpes simplex virus type 2 (HSV-2) co-infected host cells. Cell Microbiol 8, 149-162.
12. Ellis, T. N. & Kuehn, M. J. (2010). Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev 74, 81-94.
13. Fichorova, R. N., Rheinwald, J. G. & Anderson, D. J. (1997). Generation of papillomavirus-immortalized cell lines from normal human ectocervical, endocervical, and vaginal epithelium that maintain expression of tissue-specific differentiation proteins. Biol Reprod 57, 847-855.
14. Fields, K. A. & Hackstadt, T. (2000). Evidence for the secretion of Chlamydia trachomatis CopN by a type III secretion mechanism. Mol Microbiol 38, 1048-1060.
15. Giles, D. K. & Wyrick, P. B. (2008). Trafficking of chlamydial antigens to the endoplasmic reticulum of infected epithelial cells. Microbes Infect 10, 1494-1503.
16. Giles, D. K., Whittimore, J. D., LaRue, R. W., Raulston, J. E. & Wyrick, P. B. (2006). Ultrastructural analysis of chlamydial antigen-containing vesicles everting from the Chlamydia trachomatis inclusion. Microbes Infect 8, 1579-1591.
17. Gottlieb, R. A. & Adachi, S. (2000). Nitrogen cavitation for cell disruption to obtain mitochondria from cultured cells. Methods Enzymol 322, 213-221.
18. Gottlieb, S. L., Brunham, R. C., Byrne, G. I., Martin, D. H., Xu, F. & Berman, S. M. (2010). Introduction: The natural history and immunobiology of Chlamydia trachomatis genital infection and implications for Chlamydia control. J Infect Dis 201 (Suppl. 2), S85-S87.
19. Guseva, N. V., Dessus-Babus, S. C., Whittimore, J. D., Moore, C. G. & Wyrick, P. B. (2005). Characterization of estrogen-responsive epithelial cell lines and their infectivity by genital Chlamydia trachomatis. Microbes Infect 7, 1469-1481.
20. Harper, A., Pogson, C. I., Jones, M. L. & Pearce, J. H. (2000). Chlamydial development is adversely affected by minor changes in amino acid supply, blood plasma amino acid levels, and glucose deprivation. Infect Immun 68, 1457-1464.
21. Hatch, T. P. (1999). Developmental biology. In Chlamydia. Intracellular Biology, Pathogenesis, and Immunity. Edited by R. S. Stephens, pp. 29-67. Washington, DC: American Society for Microbiology.
22. Herbst-Kralovetz, M. M., Quayle, A. J., Ficarra, M., Greene, S., Rose, W. A., II, Chesson, R., Spagnuolo, R. A. & Pyles, R. B. (2008). Quantification and comparison of Toll-like receptor expression and responsiveness in primary and immortalized human female lower genital tract epithelia. Am J Reprod Immunol 59, 212-224.
23. Heuer, D., Brinkmann, V., Meyer, T. F. & Szczepek, A. J. (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, 315-322.
24. Hogan, R. J., Mathews, S. A., Mukhopadhyay, S., Summersgill, J. T. & Timms, P. (2004). Chlamydial persistence: beyond the biphasic paradigm. Infect Immun 72, 1843-1855.
25. Hower, S., Wolf, K. & Fields, K. A. (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.
26. Hua, Z., Rao, X., Feng, X., Luo, X., Liang, Y. & Shen, L. (2009). Mutagenesis of region 4 of sigma 28 from Chlamydia trachomatis defines determinants for protein-protein and protein-DNA interactions. J Bacteriol 191, 651-660.
27. Huang, J., Lesser, C. F. & Lory, S. (2008). The essential role of the CopN protein in Chlamydia pneumoniae intracellular growth. Nature 456, 112-115.
28. Hybiske, K. & Stephens, R. S. (2007). Mechanisms of host cell exit by the intracellular bacterium Chlamydia. Proc Natl Acad Sci U S A 104, 11430-11435.
29. Kadurugamuwa, J. L. & Beveridge, T. J. (1995). Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol 177, 3998-4008.
30. Kawana, K., Quayle, A. J., Ficarra, M., Ibana, J. A., Shen, L., Kawana, Y., Yang, H., Marrero, L., Yavagal, S. & other authors (2007). CD1d degradation in Chlamydia trachomatis-infected epithelial cells is the result of both cellular and chlamydial proteasomal activity. J Biol Chem 282, 7368-7375.
31. Klos, A., Thalmann, J., Peters, J., Gérard, H. C. & Hudson, A. P. (2009). The transcript profile of persistent Chlamydophila (Chlamydia) pneumoniae in vitro depends on the means by which persistence is induced. FEMS Microbiol Lett 291, 120-126.
32. Lambden, P. R., Pickett, M. A. & Clarke, I. N. (2006). The effect of penicillin on Chlamydia trachomatis DNA replication. Microbiology 152, 2573-2578.
33. Loeb, M. R. (1974). Bacteriophage T4-mediated release of envelope components from Escherichia coli. J Virol 13, 631-641.
34. Matsumoto, A. & Manire, G. P. (1970). Electron microscopic observations on the effects of penicillin on the morphology of Chlamydia psittaci. J Bacteriol 101, 278-285.
35. McBroom, A. J., Johnson, A. P., Vemulapalli, S. & Kuehn, M. J. (2006). Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol 188, 5385-5392.
36. Molano, M., Meijer, C. J., Weiderpass, E., Arslan, A., Posso, H., Franceschi, S., Ronderos, M., Mun ̃ oz, N. & van den Brule, A. J. (2005). The natural course of Chlamydia trachomatis infection in asymptomatic Colombian women: a 5-year follow-up study. J Infect Dis 191, 907-916.
37. Moorman, D. R., Sixbey, J. W. & Wyrick, P. B. (1986). Interaction of Chlamydia trachomatis with human genital epithelium in culture. J Gen Microbiol 132, 1055-1067.
38. Moulder, J. W. (1991). Interaction of chlamydiae and host cells in vitro. Microbiol Rev 55, 143-190.
39. Ouellette, S. P., Hatch, T. P., AbdelRahman, Y. M., Rose, L. A., Belland, R. J. & Byrne, G. I. (2006). Global transcriptional upregulation in the absence of increased translation in Chlamydia during IFNc-mediated host cell tryptophan starvation. Mol Microbiol 62, 1387-1401.
40. Rao, X., Deighan, P., Hua, Z., Hu, X., Wang, J., Luo, M., Wang, J., Liang, Y., Zhong, G. & other authors (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, 1818-1829.
41. Rasmussen, S. J., Eckmann, L., Quayle, A. J., Shen, L., Zhang, Y. X., Anderson, D. J., Fierer, J., Stephens, R. S. & Kagnoff, M. F. (1997). Secretion of proinflammatory cytokines by epithelial cells in response to Chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis. J Clin Invest 99, 77-87.
42. Raulston, J. E. (1997). Response of Chlamydia trachomatis serovar E to iron restriction in vitro and evidence for iron-regulated chlamydial proteins. Infect Immun 65, 4539-4547.
43. Reveneau, N., Crane, D. D., Fischer, E. & Caldwell, H. D. (2005). Bactericidal activity of first-choice antibiotics against gamma interferon-induced persistent infection of human epithelial cells by Chlamydia trachomatis. Antimicrob Agents Chemother 49, 1787-1793.
44. Rockey, D. D., Scidmore, M. A., Bannantine, J. P. & Brown, W. J. (2002). Proteins in the chlamydial inclusion membrane. Microbes Infect 4, 333-340.
45. Roth, A., König, P., van Zandbergen, G., Klinger, M., Hellwig-Bürgel, T., Daübener, W., Bohlmann, M. K. & Rupp, J. (2010). Hypoxia abrogates antichlamydial properties of IFN-c in human fallopian tube cells in vitro and ex vivo. Proc Natl Acad Sci U S A 107, 19502-19507.
46. Shaw, A. C., Vandahl, B. B., Larsen, M. R., Roepstorff, P., Gevaert, K., Vandekerckhove, J., Christiansen, G. & Birkelund, S. (2002). Characterization of a secreted Chlamydia protease. Cell Microbiol 4, 411-424.
47. Shen, L., Shi, Y., Douglas, A. L., Hatch, T. P., O'Connell, C. M. C., Chen, J.-M. & Zhang, Y.-X. (2000). Identification and characterization of promoters regulating tuf expression in Chlamydia trachomatis serovar F. Arch Biochem Biophys 379, 46-56.
48. Shen, L., Li, M. & Zhang, Y. X. (2004). Chlamydia trachomatis sigma28 recognizes the fliC promoter of Escherichia coli and responds to heat shock in chlamydiae. Microbiology 150, 205-215.
49. Stirling, P. & Richmond, S. J. (1980). Production of outer membrane blebs during chlamydial replication. FEMS Microbiol Lett 9, 103-105.
50. Ünal, C. M., Schaar, V. & Riesbeck, K. (2010). Bacterial outer membrane vesicles in disease and preventive medicine. Semin Immunopathol 1-14 doi:10.1007/s00281-010-0231-y.
51. Wang, Y., Berg, E. A., Feng, X., Shen, L., Smith, T., Costello, C. E. & Zhang, Y.-X. (2006). Identification of surface-exposed components of MOMP of Chlamydia trachomatis serovar F. Protein Sci 15, 122-134.
52. Wolf, K., Fischer, E. & Hackstadt, T. (2000). Ultrastructural analysis of developmental events in Chlamydia pneumoniae-infected cells. Infect Immun 68, 2379-2385.
53. Wyrick, P. (2006). Polarized epithelial cell culture for Chlamydia trachomatis. Wymondham, Norfolk, UK: Horizon Bioscience.
54. Wyrick, P. B. (2010). Chlamydia trachomatis persistence in vitro an overview. J Infect Dis 201 (Suppl. 2), S88-S95.
55. Wyrick, P. B. & Knight, S. T. (2004). Pre-exposure of infected human endometrial epithelial cells to penicillin in vitro renders Chlamydia trachomatis refractory to azithromycin. J Antimicrob Chemother 54, 79-85.
56. Zhong, G., Fan, T. & Liu, L. (1999). Chlamydia inhibits interferon gamma-inducible major histocompatibility complex class II expression by degradation of upstream stimulatory factor 1. J Exp Med 189, 1931-1938.
57. Zhong, G., Liu, L., Fan, T., Fan, P. & Ji, H. (2000). Degradation of transcription factor RFX5 during the inhibition of both constitutive and interferon gamma-inducible major histocompatibility complex class I expression in Chlamydia-infected cells. J Exp Med 191, 1525-1534.
58. Zhong, G., Fan, P., Ji, H., Dong, F. & Huang, Y. (2001). Identification of a chlamydial protease-like activity factor responsible for the degradation of host transcription factors. J Exp Med 193, 935-942.