Chlamydia trachomatis interrupts an exocytic pathway to acquire endogenously synthesized sphingomyelin in transit from the Golgi apparatus to the plasma membrane

EMBO Journal

Volumn 15, Issue 5, 1996, Pages 964-977

  Hackstadt, Ted ^a   Rockey, Daniel D ^a   Heinzen, Robert A ^a   Scidmore, Marci A ^a  

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

Author keywords

Chlamydia trachomatis; Exocytosis; Golgi apparatus; Sphingolipids

Indexed keywords

ANTIBODY; CERAMIDE; DIAMINOBENZIDINE; GLYCOPROTEIN; LECTIN; SPHINGOLIPID;

ARTICLE; CELL MEMBRANE; CELL TRANSPORT; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; ENDOCYTOSIS; EXOCYTOSIS; GOLGI COMPLEX; HUMAN; HUMAN CELL; NONHUMAN; PHOTOOXIDATION; PRIORITY JOURNAL;

CHLAMYDIA TRACHOMATIS; CHLAMYDIAE;

EID: 0029871027     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00433.x     Document Type: Article

References (40)

1. 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.
2. Campadelli, G., Brandimarti, R., Di Lazzaro, C., Ward, P.L., Roizman, B and Torrisi, M.R. (1993) Fragmentation and dispersal of Golgi proteins and redistribution of glycoproteins and glycolipids processed through the Golgi apparatus, after infection with herpes simplex virus 1. Proc. Natl Acad. Sci. USA, 90, 2798-2802.
3. Clemens, D.L. and Horwitz, M A. (1992) Membrane sorting during phagocytosis: selective exclusion of major histocompatibility complex molecules but not complement receptor CR3 during conventional and coiling phagocytosis. J. Exp. Med., 175, 1317-1326.
4. Falkow, S., Isberg, R.R. and Portnoy, D.A. (1992) The interaction of bacteria with mammalian cells. Annu. Rev. Cell Biol., 8, 333-363.
5. 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.
6. Futerman, A.H., Stieger, B., Hubbard, A L and Pagano, R.E. (1990) Sphingomyelin synthesis in rat liver occurs predominantly at the cis and medial cisternae of the Golgi apparatus. J. Biol. Chem., 265, 8650-8657.
7. Hackstadt, T. and Williams, J.C (1981) Biochemical strategem for obligate parasitism of eukaryotic cells hy Coxiella hurnetii. Proc. Natl Acad. Sci. USA, 78, 3240-3244.
8. 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 chlamydial inclusion. Proc. Natl Acad. Sci. USA, 92, 4877-4881.
9. 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 burnetu and Chlamydia trachomatis. Infect. Immun., in press.
10. Higashi, N (1965) Electron microscopic studies on the mode of reproduction of trachoma virus and psittacosis virus in cell cultures. Exp. Mol. Pathol., 4, 24-39.
11. Klausner, R.D., Donaldson, J.G. and Lippincott-Schwartz, J. (1992) Brefeldin A: Insights into the control of membrane traffic and organelle structure. J Cell Biol , 116, 1071-1080
12. Kornfeld, R. and Kornfeld, S. (1985) Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem., 54, 631-634.
13. Koval, M. and Pagano, R E. (1989) Lipid recycling between the plasma membrane and intracellular compartments: transport and metabolism of fluorescent sphingomyelin analogues in cultured fibroblasts. J. Cell Biol., 108, 2169-2181.
14. Koval, M. and Pagano, R.E. (1991) Intracellular transport and metabolism of sphingomyelin. Biochim. Biophys. Acta, 1082, 113-125.
15. Kremer, J.M.H., Esker, M.W.J.v.d , Pathmamanoharan, C. and Wiersema, P.H (1977) Vesicles of variable diameter prepared by a modified injection method. Biochemistry, 16, 3932-3935.
16. Lipsky, N.G. and Pagano, R.E. (1985a) A vital stain for the Golgi apparatus. Science, 228, 745-747.
17. Lipsky, N.G. and Pagano, R.E. (1985b) 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.
18. Martin, O.C. and Pagano, R.E. (1994) Internalization and sorting of a fluorescent analogue of glucosylceramide to the Golgi apparatus of human skin fibroblasts: utilization of endocytic and nonendocytic transport mechanisms J. Cell Biol , 125, 769-781.
19. Matsumoto, A. (1988) Structural characteristics of chlamydial bodies. In Barron, A L. (ed.), Microbiology of Chlamydia. CRC Press, Inc., Boca Raton, FL, pp. 21-45.
20. Misumi, Y., Miki, A., Takatsuki, A., Tamura, G. and Ikehara, Y (1986) Novel blockade by Brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes. J. Biol. Chem., 261, 11398-11403
21. Moulder, J.W. (1985) Comparative biology of intracellular parasitism. Microbiol. Rev , 49, 298-337
22. Moulder, J.W (1991) Interaction of chlamydiae and host cells in vitro. Microbiol. Rev., 55, 143-190.
23. Mukkada, A.J., Meade, J.C., Glaser, T.A. and Bonventre, P.F. (1985) Enhanced metabolism of Leishmania donovani amastigotes at acid pH an adaptation for intracellular growth. Science, 229, 1099-1101.
24. Newhall, W.J.V. (1988) Macromolecular and antigenic composition of chlamydiae. In Barron, A.L. (ed.), Microbiology of Chlamydia CRC Press, Inc., Boca Raton, FL, pp. 47-70.
25. Pagano, R.E. (1990) Lipid traffic in eukaryolic cells: mechanisms for intracellular transport and organelle-specific enrichment of lipids. Curr. Opin. Cell. Biol., 2, 652-663
26. Pagano, R.E. and Martin, O.C. (1988) A series of fluorescent N-acylsphingosines: synthesis, physical properties, and studies in cultured cells. Biochemistry, 27, 4439-4445
27. Pagano, R.E., Sepanski, M.A. and Martin, O.C. (1989) Molecular trapping of a fluorescent ceramide analogue at the Golgi apparatus of fixed cells: interaction with endogenous lipids provides a trans-Golgi marker for both light and electron microscopy J. Cell Biol., 109, 2067-2079.
28. Pagano, R E., Martin, O.C., Kang, H.C. and Haugland, R.P. (1991) A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor. J. Cell Biol. 113, 1267-1279.
29. Ridderhof, J.C and Barnes, R.C (1989) Fusion of inclusions following superinfection of HeLa cells by two serovars of Chlamydia trachomatis. Infect. Immun., 57, 3189-3193.
30. Rockey,D D., Heinzen, R.A. and Hackstadt, T. (1995) Cloning and characterization of a Chlamydia psittac i gene coding for a protein localized to the inclusion membrane of infected cells. Mol. Microbiol., 15, 617-626.
31. Rogalski, A.A. and Singer, S.J. (1984) Associations of elements of the Golgi apparatus with microtubules J. Cell Biol., 99, 1092-1100.
32. Rosenwald, A.G. and Pagano,R. E. (1993) Intracellular transport of ceramide and its metabolites at the Golgi complex: insights from short-chain analogs. Adv. Lipid Res., 26, 101-118.
33. Schachter, J. (1988) Overview of human diseases. In Barron, A.L. (ed.), Microbiology of Chlamydia, CRC Press, Inc., Boca Raton, FL, pp. 153-165.
34. Slomiany, A., Grabska, M., Slomiany, B.A., Grzelinska, E., Monta, M. and Slomiany, B.L. (1993) Intracellular transport, organelle biogenesis and establishment of Golgi identity: impact of Brefeldin A on the activity of lipid synthesizing enzymes. J. Biochem., 25, 891-901
35. Small, P.L.C., Ramakrishnan, L. and Falkow, S (1994) Remodeling schemes of intracellular pathogens. Science, 263, 637-639.
36. Sturgill-Koszycki, S., Schlesinger, P.H., Chakraborty, P., Haddix, P.L., Collins, H.L., Fok, A.K., Allen, R. D., Gluck, S.L. Heuser, J. and Russell, D.G. (1994) Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science, 263, 678-681.
37. Takizawa, P.A., Yucel, J.K., Veit, B., Faulkner, D.J., Deerinck, T., Soto, G., Ellisman, M. and Malhotra, V. (1993) Complete vesiculation of Golgi membranes and inhibition of protein transport by a novel sea sponge metabolite. Ilimaqumone. Cell, 73, 1079-1090.
38. Todd, W.J. and Caldwell, H D. (1985) The interaction of Chlamydia trachomatis with host cells: ultrastructural studies of the mechanism of release of a biovar II strain from HeLa 229 cells. J. Infect. Dis., 151, 1037-1044.
39. Turner, J.R. and Tartakoff, A.M. (1989) The response of the Golgi complex to microtubule alterations: the roles of metabolic energy and membrane traffic in Golgi complex organization. J. Cell Biol., 109, 2081-2088.
40. Virtanen, I., Ekblom, P. and Laurila, P. (1980) Subcellular compartmentalization of saccharide moieties in cultured normal and malignant cells. J. Cell Biol., 85, 429-434.