The trans-Golgi SNARE syntaxin 10 is required for optimal development of Chlamydia trachomatis

Frontiers in Cellular and Infection Microbiology

Volumn 5, Issue SEP, 2015, Pages

  Lucas, Andrea L ^a   Ouellette, Scot P ^a   Kabeiseman, Emily J ^a   Cichos, Kyle H ^a   Rucks, Elizabeth A ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

Chlamydia trachomatis; Chlamydial development; Lipid trafficking; Syntaxin 10; Trans Golgi SNARE

Indexed keywords

CHLORAMPHENICOL; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; SMALL INTERFERING RNA; SNARE PROTEIN; SYNTAXIN 10; SYNTAXIN 6; UNCLASSIFIED DRUG; SYNTAXIN;

ARTICLE; BACTERIAL GROWTH; CHLAMYDIA TRACHOMATIS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENSITOMETRY; GENETIC TRANSFECTION; GOLGI COMPLEX; HELA CELL LINE; HEP 2 CELL LINE; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNOFLUORESCENCE MICROSCOPY; LASER SCANNING CONFOCAL MICROSCOPY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PROGENY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; CELL INCLUSION; EPITHELIUM CELL; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

CHLAMYDIA TRACHOMATIS; EPITHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INCLUSION BODIES; QA-SNARE PROTEINS; RNA, SMALL INTERFERING;

EID: 85006210870     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2015.00068     Document Type: Article

References (48)

1. Abdelrahman, Y. M., and Belland, R. J. (2005). The chlamydial developmental cycle. FEMS Microbiol. Rev. 29, 949-959. doi: 10.1016/j.femsre.2005.03.002
2. Barenholz, Y., and Thompson, T. E. (1980). Sphingomyelins in bilayers and biological membranes. Biochim. Biophys. Acta 604, 129-158. doi: 10.1016/0005-2736(80)90572-6
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. doi: 10.1242/jcs.02733
4. Belland, R. J., Zhong, G., Crane, D. D., Hogan, D., Sturdevant, D., Sharma, J., et al. (2003). Gemomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc. Natl. Acad. Sci. U.S.A. 100, 8478-8483. doi: 10.1073/pnas.1331135100
5. Boncompain, G., Müller, C., Meas-Yedid, V., Schmitt-Kopplin, P., Lazarow, P. B., and Subtil, A. (2014). The intracellular bacteria Chlamydia hijack peroxisomes and utilize their enzymatic capacity to produce bacteria-specific phospholipids. PLoS ONE 9:e86196. doi: 10.1371/journal.pone.0086196
6. Caldwell, H. D., Kromhout, J., and Schachter, J. (1981). Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 31, 1161-1176.
7. Capmany, A., and Damiani, M. T. (2010). Chlamydia trachomatis intercepts Golgi-derived sphingolipids through a rab 14-mediated transport required for bacterial development and replication. PLoS ONE 5:e14084. doi: 10.1371/journal.pone.0014084
8. Centers for Disease Control and Prevention. (2012). Sexually Transmitted Disease Surveillance 2013. Atlanta, GA: Department of Health and Human Services.
9. Chiu, S. W., Vasudevan, S., Jakobsson, E., Mashl, R. J., and Scott, H. L. (2003). Structure of sphingomyelin bilayers: a simulation study. Biophys. J. 85, 3624-3635. doi: 10.1016/S0006-3495(03)74780-8
10. Cocchiaro, J. L., Kumar, Y., Fischer, E. R., Hackstadt, T., and Valdivia, R. H. (2008). Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc. Natl. Acad. Sci. U.S.A. 105, 9379-9384. doi: 10.1073/pnas.0712241105
11. Cox, J. V., Naher, N., Abdelrahman, Y. M., and Belland, R. J. (2012). Host HDL biogenesis machinery is recruited to the inclusion of Chlamydia trachomatis-infected cells and regulates chlamydial growth. Cell. Microbiol. 14, 1497-1512. doi: 10.1111/j.1462-5822.2012.01823.x
12. Datta, S. D., Sternberg, M., Johnson, R. E., Berman, S., Papp, J. R., Mcquillan, G., et al. (2007). Gonorrhea and chlamydia in the United States among persons 14 to 39 years of age, 1999 to 2002. Ann. Intern. Med. 147, 89-97. doi: 10.7326/0003-4819-147-2-200707170-00007
13. Derré, I., Swiss, R., and Agaisse, H. (2011). The lipid transfer protein CERT interacts with the Chlamydia inclusion protein IncD and participates to ER-Chlamydia inclusion membrane contact sites. PLoS Pathog. 7:e1002092. doi: 10.1371/journal.ppat.1002092
14. Dessus-Babus, S., Moore, C. G., Whittimore, J. D., and Wyrick, P. B. (2008). Comparison of Chlamydia trachomatis serovar L2 growth in polarized genital epithelial cells grown in three-dimensional culture with non-polarized cells. Microbes Infect. 10, 563-570. doi: 10.1016/j.micinf.2008.02.002
15. Elwell, C. A., and Engel, J. N. (2012). Lipid acquisition by intracellular Chlamydiae. Cell. Microbiol. 14, 1010-1018. doi: 10.1111/j.1462-5822.2012.01794.x
16. Elwell, C. A., Jiang, S., Kim, J. H., Lee, A., Wittmann, T., Hanada, K., et al. (2011). Chlamydia trachomatis co-opts GBF-1 and CERT to acquire host sphingomyelin for distinct roles during intracellular development. PLoS Pathog. 7:e1002198. doi: 10.1371/journal.ppat.1002198
17. Fields, K. A., Mead, D. J., Dooley, C. A., and Hackstadt, T. (2003). Chlamydia trachomatis type III secretion: evidence for a functional apparatus during early-cycle development. Mol. Microbiol. 48, 671-683. doi: 10.1046/j.1365-2958.2003.03462.x
18. Furness, G., Graham, D. M., and Reeve, P. (1960). The titration of trachoma and inclusion blennorrhoea viruses in cell cultures. J. Gen. Microbiol. 23, 613-619. doi: 10.1099/00221287-23-3-613
19. Grieshaber, N. A., Grieshaber, S. S., Fischer, E. R., and Hackstadt, T. (2006). A small RNA inhibits translation of the histone-like protein Hc1 in Chlamydia trachomatis. Mol. Microbiol. 59, 541-550. doi: 10.1111/j.1365-2958.2005.04949.x
20. Hackstadt, T., Rockey, D. D., Heinzen, R. A., and Scidmore, M. A. (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.
21. Hackstadt, T., Scidmore, M. A., and Rockey, D. D. (1995). Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of golgi-derived sphingolipids to the chlamyidal inclusion. Proc. Natl. Acad. Sci. U.S.A. 92, 4877-4881. doi: 10.1073/pnas.92.11.4877
22. Hatch, T. P., Miceli, M., and Sublett, J. E. (1986). Synthesis of disulfide-bonded outer membrane proteins during the developmental cycle of Chlamydia psittaci and Chlamydia trachomatis. J. Bacteriol. 165, 379-385.
23. Heinzen, R. A., Scidmore, M. A., Rockey, D. D., and Hackstadt, T. (1996). Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis. Infect. Immun. 64, 796-809.
24. Heuer, D., Lipinski, A. R., Machuy, N., Karlas, A., Wehrens, A., Siedler, F., et al. (2009). Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457, 731-735. doi: 10.1038/nature07578
25. Kabeiseman, E. J., Cichos, K., Hackstadt, T., Lucas, A., and Moore, E. R. (2013). Vesicle-associated membrane protein 4 and syntaxin 6 interactions at the chlamydial inclusion. Infect. Immun. 81, 3326-3337. doi: 10.1128/IAI.00584-13
26. Lippincott-Schwartz, J., Yuan, L., Bonifacino, J., and Klausner, R. (1989). Rapid redistribution of Golgi proteins in the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801-813. doi: 10.1016/0092-8674(89)90685-5
27. McClarty, G. (2004). "Chlamydial metabolism as inferred from the complete genome sequence," in Chlamydia: Intracellular Biology, Pathogenesis and Immunity, ed R. S. Stephens (Washington, DC: ASM Press), 69-100.
28. Moore, E. R. (2012). Sphingolipid trafficking and purification in Chlamydia trachomatis-infected cells. Curr. Protoc. Microbiol. 11. doi: 10.1002/9780471729259.mc11a02s27
29. Moore, E. R., Fischer, E. R., Mead, D. J., and Hackstadt, T. (2008). The chlamydial inclusion preferentially intercepts basolaterally directed sphingomyelin-containing exocytic vacuoles. Traffic 9, 2130-2140. doi: 10.1111/j.1600-0854.2008.00828.x
30. Moore, E. R., Mead, D. J., Dooley, C. A., Sager, J., and Hackstadt, T. (2011). The trans-Golgi SNARE syntaxin 6 is recruited to the chlamydial inclusion membrane. Microbiology 157, 830-838. doi: 10.1099/mic.0.045856-0
31. Moore, E. R., and Ouellette, S. P. (2014). Reconceptualizing the chlamydial inclusion as a pathogen-specified parasitic organelle: an expanded role for Inc proteins. Front. Cell. Infect. Microbiol. 4:157. doi: 10.3389/fcimb.2014.00157
32. Mygind, P., Christiansen, G., and Birkelund, S. (1998). Topological analysis of Chlamydia trachomatis L2 outer membrane protein 2. J. Bacteriol. 180, 5784-5787.
33. Newhall, W. J. (1988). "Macromolecular and antigenic composition of chlamydiae," in Microbiology of Chlamydiae, ed A. L. Baron (Boca Raton, FL: CRC Press), 47-70.
34. Nicholson, T. L., Olinger, L., Chong, K., Schoolnik, G., and Stephens, R. S. (2003). Global stage-specific gene regulation during the developmental cycle of Chlamydia trachomatis. J. Bacteriol. 185, 3179-3189. doi: 10.1128/JB.185.10.3179-3189.2003
35. Ouellette, S. P., and Carabeo, R. A. (2010). A functional slow recycling pathway of transferrin is required for growth of Chlamydia. Front. Microbiol. 1:112. doi: 10.3389/fmicb.2010.00112
36. Ouellette, S. P., Hatch, T. P., Abdelrahman, Y. M., Rose, L. A., Belland, R. J., and Byrne, G. I. (2006). Global transcriptional upregulation in the absence of increased translation in Chlamydia during IFNgamma-mediated host cell tryptophan starvation. Mol. Microbiol. 62, 1387-1401. doi: 10.1111/j.1365-2958.2006.05465.x
37. Ouellette, S. P., Rueden, K. J., Gauliard, E., Persons, L., De Boer, P. A., and Ladant, D. (2014). Analysis of MreB interactors in Chlamydia reveals a RodZ homolog but fails to detect an interaction with MraY. Front. Microbiol. 5:279. doi: 10.3389/fmicb.2014.00279
38. Robertson, D. K., Gu, L., Rowe, R. K., and Beatty, W. L. (2009). Inclusion biogenesis and reactivation of persistant Chlamydia trachomatis requires host cell sphingolipid biosynthesis. PLoS Pathog. 5:e1000664. doi: 10.1371/journal.ppat.1000664
39. Schachter, J. (1999). "Infection and disease epidemiology," in Chlamydia: Intracellular Biology, Pathogenesis, and Immunity American Society for Microbiology, ed R. S. Stephens (Washington, DC: American Society for Microbiology), 139-169. doi: 10.1128/9781555818203.ch6
40. Scidmore, M. A. (2005). Cultivation and laboratory maintenance of Chlamydia trachomatis. Curr. Protoc. Microbiol. 11. doi: 10.1002/9780471729259.mc11a01s00
41. Scidmore, M. A., Fischer, E. R., and Hackstadt, T. (2003). Restricted fusion of Chlamydia trachomatis vesicles with endocytic compartments during the initial stages of infection. Infect. Immun. 71, 973-984. doi: 10.1128/IAI.71.2.973-984.2003
42. Scidmore, M. A., Rockey, D. D., Fischer, E. R., Heinzen, R. A., and Hackstadt, T. (1996). Vesicular interactions of the Chlamydia trachomatis inclusion are determined by chlamydial early protein synthesis rather than route of entry. Infect. Immun. 64, 5366-5372.
43. Stephens, R. S., Kalman, S., Lammel, C., Fan, J., Marathe, R., Aravind, L., et al. (1998). Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282, 754-759. doi: 10.1126/science.282.5389.754
44. Taraska, T., Ward, D. M., Ajioka, R. S., Wyrick, P. B., Davis-Kaplan, S. R., Davis, C. H., et al. (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.
45. Van Blitterswijk, W. J., Van Hoeven, R. P., and Van Der Meer, B. W. (1981). Lipid structural order parameters (reciprocal of fluidity) in biomembranes derived from steady-state fluorescence polarization measurements. Biochim. Biophys. Acta 644, 323-332. doi: 10.1016/0005-2736(81)90390-4
46. Van Ooij, C., Apodaca, G., and Engel, J. (1997). Characterization of the Chlamydia trachomatis vacuole and its interaction with the host endocytic pathway in HeLa cells. Infect. Immun. 65, 758-766.
47. Ward, M. E. (1988). "The Chlamydial developmental cycle," in Microbiology of Chlamydia, ed A. L. Barron. (Boca Raton, FL: CRC Press Inc.), 71-95.
48. Wylie, J. L., Hatch, G. M., and Mcclarty, G. (1997). Host cell phospholipids are trafficked to and then modified by Chlamydia trachomatis. J. Bacteriol. 179, 7233-724