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Volume 157, Issue 3

The trans-Golgi SNARE syntaxin 6 is recruited to the chlamydial inclusion membrane Free

Abstract

is an obligate intracellular pathogen that replicates within a parasitophorous vacuole termed an inclusion. The chlamydial inclusion is isolated from the endocytic pathway but fusogenic with Golgi-derived exocytic vesicles containing sphingomyelin and cholesterol. Sphingolipids are incorporated into the chlamydial cell wall and are considered essential for chlamydial development and viability. The mechanisms by which chlamydiae obtain eukaryotic lipids are poorly understood but require chlamydial protein synthesis and presumably modification of the inclusion membrane to initiate this interaction. A polarized cell model of chlamydial infection has demonstrated that chlamydiae preferentially intercept basolaterally directed, sphingomyelin-containing exocytic vesicles. Here we examine the localization and potential function of trans-Golgi and/or basolaterally associated soluble -ethylmaleimide-sensitive factor attachment protein receptor (SNARE) proteins in chlamydia-infected cells. The trans-Golgi SNARE protein syntaxin 6 is recruited to the chlamydial inclusion in a manner that requires chlamydial protein synthesis and is conserved among all chlamydial species examined. The localization of syntaxin 6 to the chlamydial inclusion requires a tyrosine motif or plasma membrane retrieval signal (YGRL). Thus in addition to expression of at least two inclusion membrane proteins that contain SNARE-like motifs, chlamydiae also actively recruit eukaryotic SNARE-family proteins.

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  • Accepted:
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  • Published Online:
Keyword(s): EB, elementary body , FBS, fetal bovine serum , PMRS, plasma membrane retrieval signal and SNARE, soluble N-ethylmaleimide-sensitive factor attachment protein receptor
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2011-03-01
2024-04-18
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References

  1. Al-Younes H. M., Rudel T., Meyer T. F. 1999; Characterization and intracellular trafficking pattern of vacuoles containing Chlamydia pneumoniae in human epithelial cells. Cell Microbiol 1:237–247
     [Google Scholar]
  2. Arasaki K., Roy C. R. 2010; Legionella pneumophila promotes functional interactions between plasma membrane syntaxins and Sec22b. Traffic 11:587–600
     [Google Scholar]
  3. Bock J. B., Matern H. T., Peden A. A., Scheller R. H. 2001; A genomic perspective on membrane compartment organization. Nature 409:839–841
     [Google Scholar]
  4. Brumell J. H., Scidmore M. A. 2007; Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol Mol Biol Rev 71:636–652
     [Google Scholar]
  5. Caldwell H. D., Kromhout J., Schachter J. 1981; Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis . Infect Immun 31:1161–1176
     [Google Scholar]
  6. Carabeo R. A., Mead D. J., Hackstadt T. 2003; Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc Natl Acad Sci U S A 100:6771–6776
     [Google Scholar]
  7. Cheung H. T., Terry D. S. 1980; Effects of nocodazole, a new synthetic microtubule inhibitor, on movement and spreading of mouse peritoneal macrophages. Cell Biol Int Rep 4:1125–1129
     [Google Scholar]
  8. Clausen J. D., Christiansen G., Holst H. U., Birkelund S. 1997; Chlamydia trachomatis utilizes the host cell microtubule network during early events of infection. Mol Microbiol 25:441–449
     [Google Scholar]
  9. Cortes C., Rzomp K. A., Tvinnereim A., Scidmore M. A., Wizel B. 2007; Chlamydia pneumoniae inclusion membrane protein Cpn0585 interacts with multiple Rab GTPases. Infect Immun 75:5586–5596
     [Google Scholar]
  10. Delevoye C., Nilges M., Dautry-Varsat A., Subtil A. 2004; Conservation of the biochemical properties of IncA from Chlamydia trachomatis and Chlamydia caviae : oligomerization of IncA mediates interaction between facing membranes. J Biol Chem 279:46896–46906
     [Google Scholar]
  11. Delevoye C., Nilges M., Dehoux P., Paumet F., Perrinet S., Dautry-Varsat A., Subtil A. 2008; SNARE protein mimicry by an intracellular bacterium. PLoS Pathog 4:e1000022
     [Google Scholar]
  12. Fasshauer D., Sutton R. B., Brunger A. T., Jahn R. 1998; Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci U S A 95:15781–15786
     [Google Scholar]
  13. Fields K. A., Hackstadt T. 2002; The chlamydial inclusion: escape from the endocytic pathway. Annu Rev Cell Dev Biol 18:221
     [Google Scholar]
  14. Fields K. A., Mead D., Dooley C. A., Hackstadt T. 2003; Chlamydia trachomatis type III secretion: evidence for a functional apparatus during early-cycle development. Mol Microbiol 48:671–683
     [Google Scholar]
  15. Fratti R. A., Chua J., Vergne I., Deretic V. 2003; Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci U S A 100:5437–5442
     [Google Scholar]
  16. Furness G., Graham D. M., Reeve P. 1960; The titration of trachoma and inclusion blennorrhoea viruses in cell cultures. J Gen Microbiol 23:613–619
     [Google Scholar]
  17. Grieshaber S. S., Grieshaber N., Hackstadt T. 2003; Chlamydia trachomatis uses host cell dynein to traffic to the microtube organizing center in a p50 dynamitin-independent process. J Cell Sci 116:3793–3802
     [Google Scholar]
  18. Hackstadt T. 1999; Cell Biology. In Chlamydia: Intracellular Biology, Pathogenesis, and Immunity pp 101–138 Edited by Stephens R. S. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  19. Hackstadt T., Messer R., Cieplak W., Peacock M. G. 1992; Evidence for the proteolytic cleavage of the 120-kilodalton outer membrane protein of rickettsiae: identification of an avirulent mutant deficient in processing. Infect Immun 60:159–165
     [Google Scholar]
  20. Hackstadt T., Scidmore M. A., Rockey D. D. 1995; Lipid metabolism in Chlamydia trachomatis -infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc Natl Acad Sci U S A 92:4877–4881
     [Google Scholar]
  21. Hackstadt T., Rockey D. D., Heinzen R. A., 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
     [Google Scholar]
  22. Hatch T. P. 1975a; Utilization of L-cell nucleoside triphosphates by Chlamydia psittaci for ribonucleic acid synthesis. J Bacteriol 122:393–400
     [Google Scholar]
  23. Hatch T. P. 1975b; Competition between Chlamydia psittaci and L cells for host isoleucine pools: a limiting factor in chlamydial multiplication. Infect Immun 12:211–220
     [Google Scholar]
  24. Heinzen R. A., Scidmore M. A., Rockey D. D., Hackstadt T. 1996; Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetii and Chlamydia trachomatis . Infect Immun 64:796–809
     [Google Scholar]
  25. Lippincott-Schwartz J., Yuan L. C., Bonifacino J. S., Klausner R. D. 1989; Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56:801–813
     [Google Scholar]
  26. Low S. H., Chapin S. J., Weimbs T., Kornuves L. G., Bennett M. K., Mostov K. E. 1996; Differential localization of syntaxin isoforms in polarized Madin-Darby canine kidney cells. Mol Biol Cell 7:2007–2018
     [Google Scholar]
  27. Mallard F., Tang B. L., Galli T., Tenza D., Saint-Pol A., Yue X., Antony C., Hong W., Goud B., Johannes L. 2002; Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J Cell Biol 156:653–664
     [Google Scholar]
  28. McClarty G. 1994; Chlamydiae and the biochemistry of intracellular parasitism. Trends Microbiol 2:157–164
     [Google Scholar]
  29. Moore E. R., Fischer E. R., Mead D. J., Hackstadt T. 2008; The chlamydial inclusion preferentially intercepts basolaterally directed sphingomyelin-containing exocytic vacuoles. Traffic 9:2130–2140
     [Google Scholar]
  30. Moorhead A. M., Jung J. Y., Smirnov A., Kaufer S., Scidmore M. A. 2010; Multiple host proteins that function in phosphatidylinositol-4-phosphate metabolism are recruited to the chlamydial inclusion. Infect Immun 78:1990–2007
     [Google Scholar]
  31. Moulder J. W. 1991; Interaction of chlamydiae and host cells in vitro. Microbiol Rev 55:143–190
     [Google Scholar]
  32. Novick P., Zerial M. 1997; The diversity of Rab proteins in vesicle transport. Curr Opin Cell Biol 9:496–504
     [Google Scholar]
  33. Parlati F., Varlamov O., Paz K., McNew J. A., Hurtado D., Sollner T. H., Rothman J. E. 2002; Distinct SNARE complexes mediating membrane fusion in Golgi transport based on combinatorial specificity. Proc Natl Acad Sci U S A 99:5424–5429
     [Google Scholar]
  34. Paumet F., Wesolowski J., Garcia-Diaz A., Delevoye C., Aulner N., Shuman H. A., Subtil A., Rothman J. E. 2009; Intracellular bacteria encode inhibitory SNARE-like proteins. PLoS ONE 4:e7375
     [Google Scholar]
  35. Perskvist N., Roberg K., Kulyte A., Stendahl O. 2002; Rab5a GTPase regulates fusion between pathogen-containing phagosomes and cytoplasmic organelles in human neutrophils. J Cell Sci 115:1321–1330
     [Google Scholar]
  36. Pocard T., Bivic A. L., Galli T., Zurzolo C. 2007; Distinct v-SNAREs regulate direct and indirect apical delivery in polarized epithelial cells. J Cell Sci 120:3309–3320
     [Google Scholar]
  37. Rockey D. D., Heinzen R. A., Hackstadt T. 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
     [Google Scholar]
  38. Rockey D. D., Fischer E. R., Hackstadt T. 1996; Temporal analysis of the developing Chlamydia psittaci inclusion by use of fluorescence and electron microscopy. Infect Immun 64:4269–4278
     [Google Scholar]
  39. Rockey D. D., Scidmore M. A., Bannantine J. P., Brown W. J. 2002; Proteins in the chlamydial inclusion membrane. Microbes Infect 4:333–340
     [Google Scholar]
  40. Rothman J. E., Wieland F. T. 1996; Protein sorting by transport vesicles. Science 272:227–234
     [Google Scholar]
  41. Rzomp K. A., Scholtes L. D., Briggs B. J., Whittaker G. R., Scidmore M. A. 2003; Rab GTPases are recruited to chlamydial inclusions in both a species-dependent and species-independent manner. Infect Immun 71:5855–5870
     [Google Scholar]
  42. Rzomp K. A., Moorhead A. R., Scidmore M. A. 2006; The GTPase Rab4 interacts with Chlamydia trachomatis inclusion membrane protein CT229. Infect Immun 74:5362–5373
     [Google Scholar]
  43. Schachter J. 1999; Infection and disease epidemiology. In Chlamydia; Intracellular Biology, Pathogenesis, and Immunity pp 139–169 Edited by Stephens R. S. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  44. Schimmöller F., Simon I., Pfeffer S. R. 1998; Rab GTPases, directors of vesicle docking. J Biol Chem 273:22161–22164
     [Google Scholar]
  45. Scidmore M. A., Fischer E. R., Hackstadt T. 1996a; Sphingolipids and glycoproteins are differentially trafficked to the Chlamydia trachomatis inclusion. J Cell Biol 134:363–374
     [Google Scholar]
  46. Scidmore M. A., Rockey D. D., Fischer E. R., Heinzen R. A., Hackstadt T. 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
     [Google Scholar]
  47. Scidmore M. A., Fischer E. R., Hackstadt T. 2003; Restricted fusion of Chlamydia trachomatis vesicles with endocytic compartments during the initial stages of infection. Infect Immun 71:973–984
     [Google Scholar]
  48. Shaw E. I., Dooley C. A., Fischer E. R., Scidmore M. A., Fields K. A., Hackstadt T. 2000; Three temporal classes of gene expression during the Chlamydia trachomatis developmental cycle. Mol Microbiol 37:913–925
     [Google Scholar]
  49. Smith A. C., Cirulis J. T., Casanova J. E., Scidmore M. A., Brumell J. H. 2005; Interaction of the Salmonella -containing vacuole with the endocytic recycling system. J Biol Chem 280:24634–24641
     [Google Scholar]
  50. Sutton R. B., Fasshauer D., Jahn R., Brunger A. T. 1998; Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature 395:347–353
     [Google Scholar]
  51. Taraska T., Ward D. M., Ajioka R. S., Wyrick P. B., Davis-Kaplan S. R., Davis C. H., Kaplan J. 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
     [Google Scholar]
  52. Tassin A. M., Paintrand M., Berger E. G., Bornens M. 1985; The Golgi apparatus remains associated with microtubule organizing centers during myogenesis. J Cell Biol 101:630–638
     [Google Scholar]
  53. Teng F. Y. H., Wang Y., Tang B. L. 2001; The syntaxins. Genome Biol 2:REVIEWS3012
     [Google Scholar]
  54. van Ooij C., Apodaca G., 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
     [Google Scholar]
  55. Watson R. T., Pessin J. E. 2000; Functional cooperation of two independent targeting domains in syntaxin 6 is required for its efficient localization in the trans-Golgi network of 3T3L1 adipocytes. J Biol Chem 275:1261–1268
     [Google Scholar]
  56. Wendler F., Tooze S. 2001; Syntaxin 6: the promiscuous behavior of a SNARE protein. Traffic 2:606–611
     [Google Scholar]
  57. Wolf K., Hackstadt T. 2001; Sphingomyelin trafficking in Chlamydia pneumoniae -infected cells. Cell Microbiol 3:145–152
     [Google Scholar]
  58. Wylie J. L., Hatch G. M., McClarty G. 1997; Host cell phospholipids are trafficked to and then modified by Chlamydia trachomatis . J Bacteriol 179:7233–7242
     [Google Scholar]
  59. Wyrick P. B. 2000; Intracellular survival by Chlamydia. Cell Microbiol 2:275–282
     [Google Scholar]
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The trans-Golgi SNARE syntaxin 6 is recruited to the chlamydial inclusion membrane
Microbiology 157, 830 (2011); https://doi.org/10.1099/mic.0.045856-0
/content/journal/micro/10.1099/mic.0.045856-0
/content/journal/micro/10.1099/mic.0.045856-0
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