1887

Abstract

is an obligate intracellular bacterium considered as a potential agent of abortion in both humans and bovines. This member of the order multiplies rapidly within human macrophages and induces lysis of the infected cells. To understand how this -like micro-organism invades and proliferates within host cells, we investigated its trafficking within monocyte-derived human macrophages. Vacuoles containing acquired the early endosomal marker EEA1 during the first 30 min following uptake. However, the live -containing vacuoles never co-localized with late endosome and lysosome markers. Instead of interacting with the endosomal pathway, immediately co-localized with mitochondria and, shortly after, with endoplasmic reticulum- (ER-) resident proteins such as calnexin and protein disulfide isomerase. The acquisition of mitochondria and ER markers corresponds to the beginning of bacterial replication. It is noteworthy that mitochondrion recruitment to inclusions is prevented only by simultaneous treatment with the microtubule and actin cytoskeleton-disrupting agents nocodazole and cytochalasin D. In addition, brefeldin A inhibits the replication of , supporting a role for COPI-dependent trafficking in the biogenesis of the bacterial replicating vacuole. probably survives within human macrophages by evading the endocytic pathway and by associating with mitochondria and the ER. The intracellular trafficking of in human macrophages represents a novel route that differs strongly from that used by other members of the order .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.034546-0
2010-02-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/2/340.html?itemId=/content/journal/micro/10.1099/mic.0.034546-0&mimeType=html&fmt=ahah

References

  1. Bandyopadhyay, P., Liu, S., Gabbai, C. B., Venitelli, Z. & Steinman, H. M. ( 2007; ). Environmental mimics and the Lvh type IVA secretion system contribute to virulence-related phenotypes of Legionella pneumophila. Infect Immun 75, 723–735.[CrossRef]
    [Google Scholar]
  2. Baud, D., Thomas, V., Arafa, A., Regan, L. & Greub, G. ( 2007; ). Waddlia chondrophila, a potential agent of human fetal death. Emerg Infect Dis 13, 1239–1243.[CrossRef]
    [Google Scholar]
  3. Bellaire, B. H., Roop, R. M., II & Cardelli, J. A. ( 2005; ). Opsonized virulent Brucella abortus replicates within nonacidic, endoplasmic reticulum-negative, LAMP-1-positive phagosomes in human monocytes. Infect Immun 73, 3702–3713.[CrossRef]
    [Google Scholar]
  4. Boldogh, I. R. & Pon, L. A. ( 2006; ). Interactions of mitochondria with the actin cytoskeleton. Biochim Biophys Acta 1763, 450–462.[CrossRef]
    [Google Scholar]
  5. Capo, C., Zugun, F., Stein, A., Tardei, G., Lepidi, H., Raoult, D. & Mege, J. L. ( 1996; ). Upregulation of tumor necrosis factor alpha and interleukin-1 beta in Q fever endocarditis. Infect Immun 64, 1638–1642.
    [Google Scholar]
  6. Casson, N., Medico, N., Bille, J. & Greub, G. ( 2006; ). Parachlamydia acanthamoebae enters and multiplies within pneumocytes and lung fibroblasts. Microbes Infect 8, 1294–1300.[CrossRef]
    [Google Scholar]
  7. Celli, J. & Gorvel, J. P. ( 2004; ). Organelle robbery: Brucella interactions with the endoplasmic reticulum. Curr Opin Microbiol 7, 93–97.[CrossRef]
    [Google Scholar]
  8. Celli, J., de Chastellier, C., Franchini, D. M., Pizarro-Cerda, J., Moreno, E. & Gorvel, J. P. ( 2003; ). Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J Exp Med 198, 545–556.[CrossRef]
    [Google Scholar]
  9. Chada, S. R. & Hollenbeck, P. J. ( 2004; ). Nerve growth factor signaling regulates motility and docking of axonal mitochondria. Curr Biol 14, 1272–1276.[CrossRef]
    [Google Scholar]
  10. Corsaro, D. & Greub, G. ( 2006; ). Pathogenic potential of novel Chlamydiae and diagnostic approaches to infections due to these obligate intracellular bacteria. Clin Microbiol Rev 19, 283–297.[CrossRef]
    [Google Scholar]
  11. Dilbeck-Robertson, P., McAllister, M. M., Bradway, D. & Evermann, J. F. ( 2003; ). Results of a new serologic test suggest an association of Waddlia chondrophila with bovine abortion. J Vet Diagn Invest 15, 568–569.[CrossRef]
    [Google Scholar]
  12. Duclos, S. & Desjardins, M. ( 2000; ). Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cell Microbiol 2, 365–377.[CrossRef]
    [Google Scholar]
  13. Eissenberg, L. G., Wyrick, P. B., Davis, C. H. & Rumpp, J. W. ( 1983; ). Chlamydia psittaci elementary body envelopes: ingestion and inhibition of phagolysosome fusion. Infect Immun 40, 741–751.
    [Google Scholar]
  14. Everett, K. D., Bush, R. M. & Andersen, A. A. ( 1999; ). Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. Int J Syst Bacteriol 49, 415–440.[CrossRef]
    [Google Scholar]
  15. Frederick, R. L. & Shaw, J. M. ( 2007; ). Moving mitochondria: establishing distribution of an essential organelle. Traffic 8, 1668–1675.[CrossRef]
    [Google Scholar]
  16. Friis, R. R. ( 1972; ). Interaction of L cells and Chlamydia psittaci: entry of the parasite and host responses to its development. J Bacteriol 110, 706–721.
    [Google Scholar]
  17. Goy, G., Croxatto, A. & Greub, G. ( 2008; ). Waddlia chondrophila enters and multiplies within human macrophages. Microbes Infect 10, 556–562.[CrossRef]
    [Google Scholar]
  18. Greub, G. & Raoult, D. ( 2002; ). Crescent bodies of Parachlamydia acanthamoeba and its life cycle within Acanthamoeba polyphaga: an electron micrograph study. Appl Environ Microbiol 68, 3076–3084.[CrossRef]
    [Google Scholar]
  19. Greub, G. & Raoult, D. ( 2003; ). History of the ADP/ATP-translocase-encoding gene, a parasitism gene transferred from a Chlamydiales ancestor to plants 1 billion years ago. Appl Environ Microbiol 69, 5530–5535.[CrossRef]
    [Google Scholar]
  20. Greub, G., Mege, J. L., Gorvel, J. P., Raoult, D. & Meresse, S. ( 2005; ). Intracellular trafficking of Parachlamydia acanthamoebae. Cell Microbiol 7, 581–589.[CrossRef]
    [Google Scholar]
  21. 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.[CrossRef]
    [Google Scholar]
  22. Henning, K., Schares, G., Granzow, H., Polster, U., Hartmann, M., Hotzel, H., Sachse, K., Peters, M. & Rauser, M. ( 2002; ). Neospora caninum and Waddlia chondrophila strain 2032/99 in a septic stillborn calf. Vet Microbiol 85, 285–292.[CrossRef]
    [Google Scholar]
  23. Hollenbeck, P. J. & Saxton, W. M. ( 2005; ). The axonal transport of mitochondria. J Cell Sci 118, 5411–5419.[CrossRef]
    [Google Scholar]
  24. Horn, M. ( 2008; ). Chlamydiae as symbionts in eukaryotes. Annu Rev Microbiol 62, 113–131.[CrossRef]
    [Google Scholar]
  25. Horn, M., Collingro, A., Schmitz-Esser, S., Beier, C. L., Purkhold, U., Fartmann, B., Brandt, P., Nyakatura, G. J., Droege, M. & other authors ( 2004; ). Illuminating the evolutionary history of chlamydiae. Science 304, 728–730.[CrossRef]
    [Google Scholar]
  26. Kagan, J. C. & Roy, C. R. ( 2002; ). Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 4, 945–954.[CrossRef]
    [Google Scholar]
  27. Kocan, K. M., Crawford, T. B., Dilbeck, P. M., Evermann, J. F. & McGuire, T. C. ( 1990; ). Development of a rickettsia isolated from an aborted bovine fetus. J Bacteriol 172, 5949–5955.
    [Google Scholar]
  28. Ligon, L. A. & Steward, O. ( 2000; ). Role of microtubules and actin filaments in the movement of mitochondria in the axons and dendrites of cultured hippocampal neurons. J Comp Neurol 427, 351–361.[CrossRef]
    [Google Scholar]
  29. Matsumoto, A., Bessho, H., Uehira, K. & Suda, T. ( 1991; ). Morphological studies of the association of mitochondria with chlamydial inclusions and the fusion of chlamydial inclusions. J Electron Microsc (Tokyo) 40, 356–363.
    [Google Scholar]
  30. McClarty, G. ( 1994; ). Chlamydiae and the biochemistry of intracellular parasitism. Trends Microbiol 2, 157–164.[CrossRef]
    [Google Scholar]
  31. Mege, J. L., Sanguedolce, M. V., Jacob, T., Bongrand, P., Capo, C., Myssiakine, E. B. & Barot-Ciorbaru, R. ( 1993; ). Nocardia fractions, NLD and NWSM, induce tumor necrosis factor-alpha secretion in human monocytes: role of protein kinase C. Eur J Immunol 23, 1582–1587.[CrossRef]
    [Google Scholar]
  32. Michel, R., Steinert, M., Zöller, L., Hauröder, B. & Henning, K. ( 2004; ). Free-living amoebae may serve as hosts for the Chlamydia-like bacterium Waddlia chondrophila isolated from an aborted bovine foetus. Acta Protozool 43, 37–42.
    [Google Scholar]
  33. Morris, R. L. & Hollenbeck, P. J. ( 1995; ). Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J Cell Biol 131, 1315–1326.[CrossRef]
    [Google Scholar]
  34. Moulder, J. W. ( 1991; ). Interaction of chlamydiae and host cells in vitro. Microbiol Rev 55, 143–190.
    [Google Scholar]
  35. Pitts, K. R., Yoon, Y., Krueger, E. W. & McNiven, M. A. ( 1999; ). The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondria in mammalian cells. Mol Biol Cell 10, 4403–4417.[CrossRef]
    [Google Scholar]
  36. Roy, C. R. & Tilney, L. G. ( 2002; ). The road less traveled: transport of Legionella to the endoplasmic reticulum. J Cell Biol 158, 415–419.[CrossRef]
    [Google Scholar]
  37. Rurangirwa, F. R., Dilbeck, P. M., Crawford, T. B., McGuire, T. C. & McElwain, T. F. ( 1999; ). Analysis of the 16S rRNA gene of micro-organism WSU 86-1044 from an aborted bovine foetus reveals that it is a member of the order Chlamydiales: proposal of Waddliaceae fam. nov., Waddlia chondrophila gen. nov., sp. nov. Int J Syst Bacteriol 49, 577–581.[CrossRef]
    [Google Scholar]
  38. Scidmore, M. A., Rockey, D. D., Fischer, E. R., Heinzen, R. A. & 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.
    [Google Scholar]
  39. Sinai, A. P., Webster, P. & Joiner, K. A. ( 1997; ). Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high affinity interaction. J Cell Sci 110, 2117–2128.
    [Google Scholar]
  40. Stephens, R. S., Kalman, S., Lammel, C., Fan, J., Marathe, R., Aravind, L., Mitchell, W., Olinger, L., Tatusov, R. L. & other authors ( 1998; ). Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282, 754–759.[CrossRef]
    [Google Scholar]
  41. Trotter, P. J. & Voelker, D. R. ( 1994; ). Lipid transport processes in eukaryotic cells. Biochim Biophys Acta 1213, 241–262.[CrossRef]
    [Google Scholar]
  42. Vance, J. E. & Shiao, Y. J. ( 1996; ). Intracellular trafficking of phospholipids: import of phosphatidylserine into mitochondria. Anticancer Res 16, 1333–1339.
    [Google Scholar]
  43. Via, L. E., Fratti, R. A., McFalone, M., Pagan-Ramos, E., Deretic, D. & Deretic, V. ( 1998; ). Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 111, 897–905.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.034546-0
Loading
/content/journal/micro/10.1099/mic.0.034546-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error