The chlamydial inclusion preferentially intercepts basolaterally directed sphingomyelin-containing exocytic vacuoles

Traffic

Volumn 9, Issue 12, 2008, Pages 2130-2140

  Moore, Elizabeth R ^a   Fischer, Elizabeth R ^a   Mead, David J ^a   Hackstadt, Ted ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Chlamydia; Exocytosis; Lipid trafficking; Pathogenesis; Polarized cell; Sphingomyelin

Indexed keywords

6[[N (7 NITROBENZ 2 OXA 1,3 DIAZOL 4 YL)AMINO]HEXANOYL]SPHINGOSINE; CERAMIDE DERIVATIVE; GLUCOSYLCERAMIDE; SPHINGOMYELIN; SPHINGOSINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BASOLATERAL MEMBRANE; CELL DISRUPTION; CELL INCLUSION; CELL MIGRATION; CELL POLARITY; CELL VACUOLE; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; CORRELATION ANALYSIS; EPITHELIUM CELL; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; LIPID TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PURIFICATION; TRANSMISSION ELECTRON MICROSCOPY;

BIOLOGICAL TRANSPORT; CELL LINE; CHLAMYDIA TRACHOMATIS; EPITHELIAL CELLS; EXOCYTOSIS; HUMANS; LIPID METABOLISM; MICROSCOPY, ELECTRON, TRANSMISSION; VACUOLES;

EID: 56149120832     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00828.x     Document Type: Article

References (90)

1. Datta SD, Sternberg M, Johnson RE, Berman S, Papp JR, McQuillan G, Weinstock H. Gonorrhea and chlamydia in the United States among persons 14 to 39 years of age, 1999 to 2002. Ann Intern Med 2007; 147: 89-97.
2. Burton MJ. Trachoma: An overview. Br Med Bull 2007; 84: 99-116.
3. Mandell GL, Bennett JE, Dolin R, editors. Principles and Practice of Infectious Diseases, 6th edn. Philadelphia: Churchill Livingstone 2005; 2236-2239.
4. Hatch TP. Utilization of L-cell nucleoside triphosphates by Chlamydia psittaci for ribonucleic acid synthesis. J Bacteriol 1975; 122: 393-400.
5. McClarty G. Chlamydiae and biochemistry of intracellular parasitism. Trends Microbiol 1994; 2: 157-164.
6. Wylie JL, Hatch GM, McClarty G. Host cell phospholipids are trafficked to and then modified by Chlamydia trachomatis. J Bacteriol 1997; 179: 7233-7242.
7. Clausen JD, Christiansen G, Holst HU, Birkelund S. Chlamydia trachomatis utilizes the host cell microtubule network during early events of infection. Mol Microbiol 1997; 25: 441-449.
8. Grieshaber SS, Grieshaber NA, Hackstadt T. Chlamydia trachomatis uses host cell dynein to traffic to the microtubule-organizing center in a p50 dynamitin-independent process. J Cell Sci 2003; 116: 3793-3802.
9. Heinzen RA, Scidmore MA, Rockey DD, Hackstadt T. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnetti and Chlamydia trachomatis. Infect Immun 1996; 64: 796-809.
10. Scidmore MA, Fischer ER, Hackstadt T. Restricted fusion of Chlamydia trachomatis vesicles with endocytic compartments during the initial stages of infection. Infect Immun 2003; 71: 973-984.
11. vanOoij C, Apodaca G, Engel J. Characterization of the Chlamydia trachomatis vacuole and its interaction with the host endocytic pathway in HeLa cells. Infect Immun 1997; 65: 758-766.
12. Carabeo RA, Mead DJ, Hackstadt T. Golgi-dependent transport of cholesterol to the Chlamydia trachomatis inclusion. Proc Natl Acad Sci U S A 2003; 100: 6771-6776.
13. Hackstadt T, Scidmore MA, Rockey DD. Lipid metabolism in Chlamydia trachomatis-infected cells: Directed trafficking of Golgi-derived sphingolipids to the chlamyidal inclusion. Proc Natl Acad Sci U S A 1995; 92: 4877-4881.
14. Hackstadt T, Rockey DD, Heinzen RA, Scidmore MA. Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane. EMBO J 1996; 15: 964-977.
15. Beatty WL, Trafficking from CD63-positive late endocytic multivesicular bodies is essential for intracellular development of Chlamydia trachomatis. J Cell Sci 2006; 119: 350-359.
16. Kumar Y, Cocchiaro J, Valdivia RH. The obligate intracellular pathogen Chlamdyia trachomatis targets host lipid droplets. Curr Biol 2006; 16: 1646-1651.
17. vanMeer G, Stelzer EHK, Wijnaendts-van-Resandt RW, Simons K. Sorting of sphingolipids in epithelial (Madin-Darby canine kidney) cells. J Cell Biol 1987; 105: 1623-1635.
18. van'tHof W, vanMeer G. 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 1990; 111: 977-986.
19. Davis CH, Raulston JE, Wyrick PB. 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 2002; 70: 3413-3418.
20. Davis CH, Wyrick PB. 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 1997; 65: 2914-2924.
21. Wyrick PB, Choong J, Davis CH, Knight ST, Royal MO, Maslow AS, Bagnell CR. Entry of genital Chlamydia trachomatis into polarized human epithelial cells. Infect Immun 1989; 57: 2378-2389.
22. Wyrick PB, Davis CH, Knight ST, Choong J, Raulston JE, Schramm N. An in vitro human epithelial cell culture system for studying the pathogenesis of Chlamydia trachomatis. Sex Transm Dis 1993; 20: 248-256.
23. Giles DK, Whittimore JD, LaRue RW, Raulston JE, Wyrick PB. Ultrastructural analysis of chlamydial antigen-containing vesicles everting from the Chlamydia trachomatis inclusion. Microbes Infect 2006; 8: 1579-1591.
24. Paul TR, Knight ST, Raulston JE, Wyrick PB. Delivery of azithromycin to Chlamydia trachomatis-infected polarized human endometrial epithelial cells by polymorphonuclear leucocytes. J Antimicrob Chemother 1997; 39: 623-630.
25. Raulston JE, Pharmacokinetics of azithromycin and erythromycin in human endometrial epithelial cells and in cells infected with Chlamydia trachomatis. J Antimicrob Chemother 1994; 34: 765-776.
26. Wyrick PB, Davis CH, Knight ST, Choong J. In-vitro activity of azithromycin on Chlamydia trachomatis infected, polarized human endometrial epithelial cells. J Antimicrob Chemother 1993; 31: 139-150.
27. Wyrick PB, Knight ST. Pre-exposure of infected human endometrial epithelial cells to penicillin in vitro renders Chlamydia trachomatis refractory to azithromycin. J Antimicrob Chemother 2004; 54: 79-85.
28. Guseva NV, Knight ST, Whittimore JD, Wyrick PB. Primary cultures of female swine genital epithelial cells in vitro: A new approach for the study of hormonal modulation of Chlamydia infection. Infect Immun 2003; 71: 4700-4710.
29. Maslow AS, Davis CH, Choong J, Wyrick PB. Estrogen enhances attachment of Chlamydia trachomatis to human endometrial epithelial cells in vitro. Am J Obstet Gynecol 1988; 159: 1006-1114.
30. Igietseme JU, Wyrick PB, Goyeau D, Rank RG. An in vitro model for immune control of chlamydial growth in polarized epithelial cells. Infect Immun 1994; 62: 3528-3535.
31. Kane CD, Byrne GI. Differential effects of gamma interferon on Chlamydia trachomatis growth in polarized and nonpolarized human epithelial cells in culture. Infect Immun 1998; 66: 2349-2351.
32. Kane CD, Vena RM, Ouellette SP, Byrne GI. Intracellular tryptophan pool sizes may account for differences in gamma interferon-mediated inhibition and persistence of chlamydial growth in polarized and nonpolarized cells. Infect Immun 1999; 67: 1666-1671.
33. Kaushic C, Grant K, Crane M, Wira CR. Infection of polarized primary epithelial cells from rat uterus with Chlamydia trachomatis: Cell-cell interaction and cytokine secretion. Am J Reprod Immunol 2000; 44: 73-79.
34. Dessus-Babus S, Knight ST, Wyrick PB. Chlamydial infection of polarized HeLa cells induces PMN chemotaxis but the cytokine profile varies between disseminating and non-disseminating strains. Cell Microbiol 2000; 2: 317-327.
35. Bacallao R, Antony C, Dotti C, Karsenti E, Stelzer EHK, Simons K. The subcellular organization of madin-darby canine kidney cells during the formation of a polarized epithelium. J Cell Biol 1989; 109: 2817-2832.
36. Balcarova-Stander J, Pfeiffer SE, Fuller SD, Simons K. Development of cell surface polarity in the epithelial Madin-Darby canine kidney (MDCK) cell line. EMBO J 1984; 3: 2687-2694.
37. Cereijido M, Robbins ES, Dolan WJ, Rotunno CA, Sabatini DD. Polarized monolayers formed by epithelial cells on a permeable and translucent support. J Cell Biol 1978; 77: 853-880.
38. Slimane TA, Hoekstra D. Sphingolipid trafficking and protein sorting in epithelial cells. FEBS Lett 2002; 529: 54-59.
39. Schiller A, Forssman WG, Taugner R. The tight junctions of renal tubules in the cortex and outer medulla: A quantitative study of the kidneys of six species. Cell Tissue Res 1980; 212: 395-413.
40. Peterson MD, Mooseker MS. Characterization of the enterocyte-like brush border cytoskeleton of the C2 BBe clones of the human intestinal cell line, Caco-2. J Cell Sci 1992; 102: 581-600.
41. Zegers MMP, Hoekstra D. Mechanisms and functional features of polarized membrane traffick in epithelial and hepatic cells. Biochem J 1998; 336: 257-269.
42. Kazmierczak BI, Mostov K, Engel JN. Interaction of bacterial pathogens with polarized epithelium. Annu Rev Microbiol 2001; 55: 407-435.
43. Fuller SD, Simons K. Transferrin receptor polarity and recycling accuracy in. "tight" and "leaky" strains of Madin-Darby canine kidney cells. J Cell Biol 1986; 103: 1767-1779.
44. Wolf K, Hackstadt T. Sphingomyelin trafficking in Chlamydia pneumoniae-infected cells. Cell Microbiol 2001; 3: 145-152.
45. Rockey DD, Fischer ER, Hackstadt T. Temporal analysis of the developing Chlamydia psittaci inclusion by use of fluorescence and electron microscopy. Infect Immun 1996; 64: 4269-4278.
46. Lipsky NG, Pagano RE. A vital stain for the Golgi apparatus. Science 1985; 228: 745-747.
47. Scidmore MA, Fischer ER, Hackstadt T. Sphingolipids and glycoproteins are differentially trafficked to the Chlamydia trachomatis inclusion. J Cell Biol 1996; 134: 363-374.
48. Taraska T, Ward DM, Ajioka RS, Wyrick PB, Davis-Kaplan SR, Davis CH, Kaplan J. The late chlamydial inclusion membrane is not derived from the endocytic pathway and is relatively deficient in host proteins. Infect Immun 1996; 64: 3713-3727.
49. vanOoij C, Kalman L, vanIjzendoorn S, Nishijima M, Hanada K, Mostov K, Engel JN. Host cell-derived sphingolipids are required for the intracellular growth of Chlamydia trachomatis. Cell Microbiol 2000; 2: 627-637.
50. Doughri AM, Storz J, Altera KP. Mode of entry and release of chlamydiae in infections of intestinal epithelial cells. J Infect Dis 1972; 126: 652-657.
51. McCormick BA. The use of transepithelial models to examine host-pathogen interactions. Curr Opin Microbiol 2003; 6: 77-81.
52. Schachter J, Infection and disease epidemiology. In: Stephens RS, editor. Chlamydia: Intracellular Biology, Pathogenesis, and Immunity, Washington, DC: American Society for Microbiology 1999; 139-169.
53. Schachter J, Osoba AO. Lymphogranuloma venereum. Br Med Bull 1983; 39: 151-154.
54. Futerman AH, Pagano RE. Determination of the intracellular sites of topology of glucosylceramide synthesis in rat liver. Biochem J 1991; 280: 295-302.
55. Futerman AH, Stieger B, Hubbard AL, Pagano RE. Sphingomyelin synthesis in rat liver occurs predominately at the cis and medial cisternae of the Golgi apparatus. J Biol Chem 1990; 265: 8650-8657.
56. Kobayashi T, Pagano RE. Lipid transport during mitosis. J Biol Chem 1989; 264: 5966-5973.
57. Kobayashi T, Pimplikar SW, Parton RG, Bhakdi S, Simons K. Sphingolipid transport from the trans-Golgi network to the apical surface in permeabilized MDCK cells. FEBS Lett 1992; 300: 227-231.
58. vanMeer G, Burger KNJ. Sphingolipid trafficking-sorted out? Trends Cell Biol 1992; 2: 332-337.
59. Babia T, Kok JW, vanderHaar M, Kalicharan R, Hoekstra D. Transport of biosynthetic sphingolipids from Golgi to plasma membrane in HT-29 cells: involvement of different carrier vesicle populations. Eur J Cell Biol 1994; 63: 172-181.
60. vanMeer G. Lipid traffic in animal cells. Annu Rev Cell Biol 1989; 5: 247-275.
61. vanIJzendoorn SCD, Hoekstra D. Polarized sphingolipid transport from the subapical compartment: Evidence for distinct sphingolipid domains. Mol Biol Cell 1999; 10: 3449-3461.
62. Kok JW, Babia T, Hoekstra D. Sorting of sphingolipids in the endocytic pathway of HT29 cells. J Cell Biol 1991; 114: 231-239.
63. Koval M, Pagano RE. Intracellular transport and metabolism of sphingomyelin. Biochim Biophys Acta 1991; 1082: 113-125.
64. 6-NBD-sphingomyelin is translocated across the plasma membrane by a multidrug transporter activity. J Cell Sci 1997; 110: 75-83.
65. vanHelvoort A, Smith AJ, Sprong H, Fritzsche I, Schinkel AH, Borst P, vanMeer G. MDR1 p-glycoprotein is a lipid translocase of broad specificity, while MDR3 p-glycoprotein specifically transolcates phosphatidylcholine. Cell 1996; 87: 507-517.
66. Thiebaut F, Tsuruo T, Hamada H, Gottesman MM, Pastan I, Willingham MC. Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues. Proc Natl Acad Sci U S A 1987; 84: 7735-7738.
67. Higgins CF, Gottesman MM. Is the multidrug transporter a flippase? Trends Biochem Sci 1992; 17: 18-21.
68. 6-fold increased cell sensitivity to verocytotoxin. J Biol Chem 2000; 275: 6246-6251.
69. Simons K, Wandinger-Ness A. Polarized sorting in epithelia. Cell 1990; 62: 207-210.
70. Pocard T, Bivic AL, Galli T, Zurzolo C. Distinct v-SNAREs regulate direct and indirect apical delivery in polarized epithelial cells. J Cell Sci 2007; 120: 3309-3320.
71. Folsch H. The building blocks for basolateral vesicles in polarized epithelial cells. Trends Cell Biol 2005; 15: 222-228.
72. Scidmore-Carlson MA, Shaw EI, Dooley CA, Fischer ER, Hackstadt T. Identification and characterization of Chlamydia trachomatis early operon encoding four novel inclusion membrane proteins. Mol Microbiol 1999; 33: 753-765.
73. Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, Aravind L, Mitchell W, Olinger L, Tatusov RL, Zhao Q, Koonin EV, Davis RW. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 1998; 282: 754-759.
74. Bannantine JP, Stamm WE, Suchland RJ, Rockey DD. Chlamydia trachomatis IncA is localized to the inclusion membrane and is recognized by antisera from infected humans and primates. Infect Immun 1998; 66: 6017-6021.
75. Shaw EI, Dooley CA, Fischer ER, Scidmore MA, Fields KA, Hackstadt T. Three temporal classes of gene expression during the Chlamydia trachomatis developmental cycle. Mol Microbiol 2000; 37: 913-925.
76. Hackstadt T, Scidmore-Carlson MA, Shaw EI, Fischer ER. The Chlamydia trachomatis IncA protein is required for homotypic vesicle fusion. Cell Microbiol 1999; 1: 119-130.
77. Rockey DD, Grosenbach D, Hruby DE, Peacock MG, Heinzen RA, Hackstadt T. Chlamydia psittaci IncA is phosphorylated by the host cell and is exposed on the cytoplasmic face of the developing inclusion. Mol Microbiol 1997; 24: 217-228.
78. Scidmore MA, Rockey DD, Fischer ER, Heinzen RA, Hackstadt T. Vesicular interactions of the Chlamydia trachomatis inclusion are determined by chlamydial early protein synthesis rather than route of entry. Infect Immun 1996; 64: 5366-5372.
79. Delevoye C, Nilges M, Dautry-Varsat A, Subtil A. Conservation of the biochemical properties of IncA from Chlamydia trachomatis and Chlamydia caviae. J Biol Chem 2004; 279: 46896-46906.
80. Grosshans BL, Ortiz D, Novick P. Rabs and their effectors: Achieving specificity in membrane traffic. Proc Natl Acad Sci U S A 2006; 103: 11821-11827.
81. Rzomp KA, Scholtes LD, Briggs BJ, Whittaker GR, Scidmore MA. Rab GTPases are recruited to chlamydial inclusions in both a species-dependent and species-independent manner. Infect Immun 2003; 71: 5855-5870.
82. Rzomp KA, Moorhead AR, Scidmore MA. The GTPase Rab4 interacts with Chlamydia trachomatis inclusion membrane protein CT229. Infect Immun 2006; 74: 5362-5373.
83. Casanova JE, Wang X, Kumar R, Bhartur SG, Navarre J, Woodrum JE, Altschuler Y, Ray GS, Goldenring JR. Association of Rab25 and Rab11a with apical recycling system of polarized Madin-Darby canine kidney cells. Mol Biol Cell 1999; 10: 47-61.
84. Rodriguez-Boulan E, Kreitzer G, Musch A. Organization of vesicular trafficking in epithelia. Nat Rev Mol Cell Biol 2005; 6: 233-247.
85. Brumell JH, Scidmore MA. Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol Mol Biol Rev 2007; 71: 636-652.
86. Caldwell HD, Kromhout J, Schachter J. Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect Immun 1981; 31: 1161-1176.
87. Furness G, Graham DM, Reeve P. The titration of trachoma and inclusion blennorrhoea viruses in cell culture. J Gen Microbiol 1960; 23: 613-619.
88. Hackstadt T, Messer R, Cieplak W, Peacock MG. Evidence for proteolytic cleavage of the 120-kilodalton outer membrane protein of Rickettsiae: identification of an avirulent mutant deficient in processing. Infect Immun 1992; 60: 159-165.
89. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37: 911-917.
90. Bolduc GR, Baron MJ, Gravekamp C, Lachenauer CS, Madoff LC. The alpha C protein mediates internalization of group B Streptococcus within human cervical epithelial cells. Cell Microbiol 2002; 4: 751-758.