Maturation of Coxiella burnetii parasitophorous vacuole requires bacterial protein synthesis but not replication

Cellular Microbiology

Volumn 5, Issue 7, 2003, Pages 469-480

  Howe, Dale ^a,c   Melnicáková, Jana ^b   Barák, Imrich ^b   Heinzen, Robert A ^a,c  

^a UNIVERSITY OF WYOMING   (United States)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

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

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; BIOCHEMICAL MARKER; CARBENICILLIN; CHLORAMPHENICOL; NALIDIXIC ACID; PROTEIN SYNTHESIS INHIBITOR; TETRACYCLINE;

ACIDITY; ANIMAL CELL; ANTIGENICITY; ARTICLE; BACTERIOSTASIS; CELL MATURATION; CELL SIZE; CELL TRANSPORT; CELL VACUOLE; CELL WALL; CONCENTRATION RESPONSE; CONTROLLED STUDY; COXIELLA BURNETII; DNA SYNTHESIS INHIBITION; DRUG WITHDRAWAL; ENDOCYTOSIS; FLUORESCENCE MICROSCOPY; FUSOBACTERIUM; LYSOSOME; MEMBRANE BINDING; MEMBRANE FUSION; MICROSCOPY; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN SYNTHESIS; VERO CELL;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIGENS, CD; BACTERIAL PROTEINS; CARBENICILLIN; CELL LINE; CERCOPITHECUS AETHIOPS; CHLORAMPHENICOL; COXIELLA BURNETII; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MACROPHAGES; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MICROSPHERES; PHAGOSOMES; PROTEIN SYNTHESIS INHIBITORS; VACUOLES; VERO CELLS;

ANIMALIA; BACTERIA (MICROORGANISMS); COXIELLA BURNETII; FUSOBACTERIUM;

EID: 0037711627     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1462-5822.2003.00293.x     Document Type: Article

References (60)

1. Akporiaye, E.T., Rowatt, J.D., Aragon, A.A., and Baca, O.G. (1983) Lysosomal response of a murine macrophage-like cell line persistently infected with Coxiella burnetii. Infect Immun 40: 1155-1162.
2. Alpuche-Aranda, C.M., Racoosin, E.L., Swanson, J.A., and Miller, S.I. (1994) Salmonella stimulate macrophage macropinocytosis and persist within spacious phagosomes. J Exp Med 179: 601-608.
3. Andrews, H.L., Vogel, J.P., and Isberg, R.R. (1998) Identification of linked Legionella pneumophila genes essential for intracellular growth and evasion of the endocytic pathway. Infect Immun 66: 950-958.
4. Barnewall, R.E., Rikihisa, Y., and Lee, E.H. (1997) Ehrlichia chaffeensis inclusions are early endosomes which selectively accumulate transferrin receptor. Infect Immun 65: 1455-1461.
5. Beron, W., Gutierrez, M.G., Rabinovitch, M., and Colombo, M.I. (2002) Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics. Infect Immun 70: 5816-5821.
6. Beuzon, C.R., Meresse, S., Unsworth, K.E., Ruiz-Albert, J., Garvis, S., Waterman, S. R., et al. (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19: 3235-3249.
7. Burton, P.R., Kordova, N., and Paretsky, D. (1971) Electron microscopic studies of the rickettsia Coxiella burnetii: entry, lysosomal response, and fate of rickettsial DNA in L-cells. Can J Microbiol 17: 143-150.
8. Burton, P.R., Stueckemann, J., Welsh, R.M., and Paretsky, D. (1978) Some ultrastructural effects of persistent infections by the rickettsia Coxiella burnetii in mouse L cells and green monkey kidney (Vero) cells. Infect Immun 21: 556-566.
9. Byrne, B., and Swanson, M.S. (1998) Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun 66: 3029-3034.
10. de Chastellier, C., Thibon, M., and Rabinovitch, M. (1999) Construction of chimeric phagosomes that shelter Mycobacterium avium and Coxiella burnetii (phase II) in doubly infected mouse macrophages: an ultrastructural study. Eur J Cell Biol 78: 580-592.
11. Clemens, D.L., and Horwitz, M.A. (1995) Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med 181: 257-270.
12. Clemens, D.L., Lee, B.Y., and Horwitz, M.A. (2000a) Deviant expression of Rab5 on phagosomes containing the intracellular pathogens Mycobacterium, tuberculosis and Legionella pneumophila is associated with altered phagosomal fate. Infect Immun 68: 2671-2684.
13. Clemens, D.L., Lee, B.Y., and Horwitz, M.A. (2000b) Mycobacterium tuberculosis and Legionella pneumophila phagosomes exhibit arrested maturation despite acquisition of Rab7. Infect Immun 68: 5154-5166.
14. Clemens, D.L., Lee, B.Y., and Horwitz, M.A. (2002) The Mycobacterium tuberculosis phagosome in human macrophages is isolated from the host cell cytoplasm. Infect Immun 70: 5800-5807.
15. Coers, J., Monahan, J.J., and Roy, C.R. (1999) Modulation of phagosome biogenesis by Legionella pneumophila creates an organelle permissive for intracellular growth. Nat Cell Biol 1: 183-188.
16. Desai, S.A., Krogstad, D.J., and McCleskey, E.W. (1993) A nutrient-permeable channel on the intraerythrocytic malaria parasite. Nature 362: 643-646.
17. Dorn, B.R., Dunn, W.A., Jr, and Progulske-Fox, A. (2002) Bacterial interactions with the autophagic pathway. Cell Microbiol 4: 1-10.
18. Garcia-del Portillo, F., and Finlay, B.B. (1995) Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J Cell Biol 129: 81-97.
19. Ghigo, E., Capo, C., Tung, C.H., Raoult, D., Gorvel, J.P., and Mege, J.L. (2002) Coxiella burnetii survival in THP-1 monocytes involves the impairment of phagosome maturation: IFN-γ mediates its restoration and bacterial killing. J Immunol 169: 4488-4495.
20. Gomes, M.S., Paul, S., Moreira, A.L., Appelberg, R., Rabinovitch, M., and Kaplan, G. (1999) Survival of Mycobacterium avium and Mycobacterium tuberculosis. acidified vacuoles of murine macrophages. Infect Immun 67: 3199-3206.
21. Hackstadt, T., and Williams, J.C. (1981) Biochemical stratagem for obligate parasitism of eukaryotic cells by Coxiella burnetii. Proc Natl Acad Sci USA 78: 3240-3244.
22. Hackstadt, T., Messer, R., Cieplak, W., and Peacock, M.G. (1992) Evidence for proteolytic cleavage of the 120-kilodalton outer membrane protein of rickettsiae: identification of an avirulent mutant deficient in processing. Infect Immun 60: 159-165.
23. 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.
24. Hackstadt, T., Scidmore-Carlson, M.A., Shaw, E.I., and Fischer, E.R. (1999) The Chlamydia trachomatis IncA protein is required for homotypic vesicle fusion. Cell Microbiol 1: 119-130.
25. Hammer, B.K., and Swanson, M.S. (1999) Co-ordination of Legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol Microbiol 33: 721-731.
26. Hashim, S., Mukherjee, K., Raje, M., Basu, S.K., and Mukhopadhyay, A. (2000) Live Salmonella modulate expression of Rab proteins to persist in a specialized compartment and escape transport to lysosomes. J Biol Chem 275: 16281-16218.
27. Heinzen, R.A., and Hackstadt, T. (1997) The Chlamydia trachomatis parasitophorous vacuolar membrane is not passively permeable to low-molecular-weight compounds. Infect Immun 65: 1088-1094.
28. Heinzen, R.A., Scidmore, M.A., Rockey, D.D., and Hackstadt, T. (1996) Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxielia burnetii and Chlamydia trachomatis. Infect Immun 64: 796-809.
29. Heinzen, R.A., Hackstadt, T., and Samuel, J.E. (1999) Developmental biology of Coxiella burnetii. Trends Microbiol 7: 149-154.
30. Howe, D., and Mallavia, L.P. (2000) Coxiella burnetii exhibits morphological change and delays phagolysosomal fusion after internalization by J774A.1 cells. Infect Immun 68: 3815-3821.
31. Howe, D., Barrows, L.F., Lindstrom, N.M., and Heinzen, R.A. (2002) Nitric oxide inhibits Coxiella burnetii replication and parasitophorous vacuole maturation. Infect Immun 70: 5140-5147.
32. Knodler, L.A., Celli, J., and Finlay, B.B. (2001) Pathogenic trickery: deception of host cell processes. Nat Rev Mol Cell Biol 2: 578-588.
33. Maurin, M., and Raoult, D. (1999) Q fever. Clin Microbiol Rev 12: 518-553.
34. Maurin, M., Benoliel, A.M., Bongrand, P., and Raoult, D. (1992) Phagolysosomes of Coxiella burnetii-infected cell lines maintain an acidic pH during persistent infection. Infect Immun 60: 5013-5016.
35. Meresse, S., Steele-Mortimer, O., Finlay, B.B., and Gorvel, J.P. (1999) The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells. EMBO J 18: 4394-4403.
36. Nagai, H., Kagan, J.C., Zhu, X., Kahn, R.A., and Roy, C.R. (2002) A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295: 679-682.
37. Peters, C., Stierhof, Y.D., and Ilg, T. (1997) Proteophosphoglycan secreted by Leishmania mexicana amastigotes causes vacuole formation in macrophages. Infect Immun 65: 783-786.
38. Rockey, D.D., Scidmore, M.A., Bannantine, J.P., and Brown, W.J. (2002) Proteins in the chlamydial inclusion membrane. Microbes Infect 4: 333-340.
39. Roy, C.R., Berger, K.H., and Isberg, R.R. (1998) Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol Microbiol 28: 663-674.
40. Russell, D.G. (2001) Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol 2: 569-577.
41. Schaible, U.E., Schlesinger, P.H., Steinberg, T.H., Mangel, W.F., Kobayashi, T., and Russell, D.G. (1999) Parasitophorous vacuoles of Leishmania mexicana acquire macromolecules from the host cell cytosol via two independent routes. J Cell Sci 112: 681-693.
42. Schwab, J.C., Beckers, C.J., and Joiner, K.A. (1994) The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc Natl Acad Sci USA 91: 509-513.
43. 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.
44. Segal, G., Purcell, M., and Shuman, H.A. (1998) Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc Natl Acad Sci USA 95: 1669-1674.
45. Sexton, J.A., and Vogel, J.P. (2002) Type IVB secretion by intracellular pathogens. Traffic 3: 178-185.
46. Sinai, A.P., Paul, S., Rabinovitch, M., Kaplan, G., and Joiner, K.A. (2000) Coinfection of fibroblasts with Coxiella burnetti and Toxoplasma gondii: to each their own. Microbes Infect 2: 727-736.
47. Steele-Mortimer, O., Meresse, S., Gorvel, J.P., Toh, B.H., and Finlay, B.B. (1999) Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1: 33-49.
48. Sturgill-Koszycki, S., and Swanson, M.S. (2000) Legionella pneumophila replication vacuoles mature into acidic, endocytic organelles. J Exp Med 192: 1261-1272.
49. Sturgill-Koszycki, S., Schaible, U.E., and Russell, D.G. (1996) Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J 15: 6960-6968.
50. Swanson, M.S., and Isberg, R.R. (1995) Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 63: 3609-3620.
51. Swanson, J., Yirinec, B., Burke, E., Bushnell, A., and Silverstein, S.C. (1986) Effect of alterations in the size of the vacuolar compartment on pinocytosis in J774.2 macrophages. J Cell Physiol 128: 195-201.
52. Teitelbaum, R., Cammer, M., Maitland, M.L., Freitag, N.E., Condeelis, J., and Bloom, B.R. (1999) Mycobacterial infection of macrophages results in membrane-permeable phagosomes. Proc Natl Acad Sci USA 96: 15190-15195.
53. Uchiya, K., Barbieri, M.A., Funato, K., Shah, A.H., Stahl, P.D., and Groisman, E.A. (1999) A Salmonella virulence protein that inhibits cellular trafficking. EMBO J 18: 3924-3933.
54. Veras, P.S., de Chastellier, C., Moreau, M.F., Villiers, V., Thibon, M., Mattei, D., and Rabinovitch, M. (1994) Fusion between large phagocytic vesicles: targeting of yeast and other particulates to phagolysosomes that shelter the bacterium Coxiella burnetii or the protozoan Leishmania amazonensis in Chinese hamster ovary cells. J Cell Sci 107: 3065-3076.
55. Veras, P.S., Moulia, C., Dauguet, C., Tunis, C.T., Thibon, M., and Rabinovitch, M. (1995) Entry and survival of Leishmania amazonensis amastigotes within phagolysosome-like vacuoles that shelter Coxiella burnetii in Chinese hamster ovary cells. Infect Immun 63: 3502-3506.
56. Via, L.E., Deretic, D., Ulmer, R.J., Hibler, N.S., Huber, L.A., and Deretic, V. (1997) Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J Biol Chem 272: 13326-13331.
57. Vieira, O.V., Botelho, R.J., and Grinstein, S. (2002) Phagosome maturation: aging gracefully. Biochem J 366: 689-704.
58. Vogel, J.P., Andrews, H.L., Wong, S.K., and Isberg, R.R. (1998) Conjugative transfer by the virulence system of Legionella pneumophila. Science 279: 873-876.
59. Watarai, M., Derre, I., Kirby, J., Growney, J.D., Dietrich, W.F., and Isberg, R.R. (2001) Legionella pneumophila is internalized by a macropinocytotic uptake pathway controlled by the Dot/lcm system and the mouse Lgn1 locus. J Exp Med 194: 1081-1096.
60. Wiater, L.A., Dunn, K., Maxfield, F.R., and Shuman, H.A. (1998) Early events in phagosome establishment are required for intracellular survival of Legionella pneumophila. Infect Immun 66: 4450-4460.