Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites

Nature Cell Biology

Volumn 4, Issue 12, 2002, Pages 945-954

  Kagan, Jonathan C ^a   Roy, Craig R ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; CELL PROTEIN; GUANOSINE TRIPHOSPHATASE; PROTEIN SAR1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOGENESIS; CELL DESTRUCTION; CELL ORGANELLE; CONTROLLED STUDY; HOST CELL; HOST PATHOGEN INTERACTION; INTERNALIZATION; INTRACELLULAR TRANSPORT; LEGIONELLA PNEUMOPHILA; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN FUNCTION; ROUGH ENDOPLASMIC RETICULUM; SECRETORY VESICLE;

ANIMALS; BIOLOGICAL TRANSPORT; CELLS, CULTURED; COAT PROTEIN COMPLEX I; ENDOPLASMIC RETICULUM; LEGIONELLA; MACROPHAGES; MICE; PHAGOCYTOSIS; PHAGOSOMES;

ANIMALIA; LEGIONELLA; LEGIONELLA PNEUMOPHILA; NEGIBACTERIA;

EID: 0036903907     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb883     Document Type: Article

References (38)

1. Tilney, L. G., Harb, O. S., Connelly, P. S., Robinson, C. G. & Roy, C. R. How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane. J. Cell Sci. 114, 4637-4650 (2001).
2. Katz, S. M. & Hashemi, S. Electron microscopic examination of the inflammatory response to Legionella pneumophila in guinea pigs. Lab. Invest. 46, 24-32 (1982).
3. Horwitz, M. A. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella, pneumophila) in human monocytes. J. Exp. Med. 158, 1319-1331 (1983).
4. Abu Kwaik, Y. The phagosome containing Legionella pneumophila within the protozoan Hartmannella vermiformis is surrounded by the rough endoplasmic reticulum. Appl. Environ. Microbiol. 62, 2022-2028 (1996).
5. Swanson, M. S. & Isberg, R. R. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63, 3609-3620 (1995).
6. Vogel, J. P., Andrews, H. L., Wong, S. K. & Isberg, R. R. Conjugative transfer by the virulence system of Legionella pneumophila. Science 279, 873-876 (1998).
7. Segal, G., Purcell, M. & Shuman, H. A. 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 (1998).
8. Coers, J., Monahan, C. & Roy, C. R. Modulation of phagosome biogenesis by Legionella pneumophila creates an organelle permissive for intracellular growth. Nature Cell Biol. 1, 451-453 (1999).
9. Nagai, H., Kagan, J. C., Zhu, X., Kahn, R. A. & Roy, C. R. A bacterial guanine nucleoticle exchange factor activates ARF on Legionella phagosomes. Science 295, 679-682 (2002).
10. Wiater, L. A., Dunn, K., Maxfield, F. R. & Shuman, H. A. Early events in phagosome establishment are required for intracellular survival of Legionella pneumophila. Infect. Immun. 66, 4450-4460 (1998).
11. Roy, C. R., Berger, K. & Isberg, R. R. Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol. Microbiol. 28, 663-674 (1998).
12. Coers, J. et al. Identification of Icm protein complexes that play distinct roles in the biogenesis of an organelle permissive for Legionella pneumophila intracellular growth. Mol. Microbiol. 38, 719-736 (2000).
13. Roderick, H. L., Campbell, A. K. & Llewellyn, D. H. Nuclear localisation of calreticulin in vivo is enhanced by its interaction with glucocorticoid receptors. FEBS Lett. 405, 181-185 (1997).
14. Blum, R. et al. Intracellular localization and in vivo trafficking of p24A and p23. J. Cell Sci. 112, 537-548 (1999).
15. Lord, J. M. & Roberts, L. M. Toxin entry: retrograde transport through the secretory pathway. J. Cell Biol. 140, 733-736 (1998).
16. Linstedt, A. D. & Hauri, H. P. Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Mol. Biol. Cell 4, 679-693 (1993).
17. Seelig, H. P. et al. Molecular genetic analyses of a 376-kilodalton Golgi complex membrane protein (giantin). Mol. Cell. Biol. 14, 2564-2576 (1994).
18. Sonnichsen, B. et al. A role for giantin in docking COPI vesicles to Golgi membranes. J. Cell Biol. 140, 1013-1021 (1998).
19. Hauri, H. P., Kappeler, F., Andersson, H. & Appenzeller, C. ERGIC-53 and traffic in the secretory pathway. J. Cell Sci. 113, 587-596 (2000).
20. Lahtinen, U., Hellman, U., Wernstedt, C., Saraste, J. & Pettersson, R. F. Molecular cloning and expression of a 58-kDa cis-Golgi and intermediate compartment protein. J. Biol. Chem. 271, 4031-4037 (1996).
21. Scales, S. J., Pepperkok, R. & Kreis, T. E. Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 90, 1137-1148 (1997).
22. Ward, T. H., Polishchuk R. S., Caplan, S., Hirschberg, K. & Lippincott-Schwartz, J. Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155, 557-570 (2001).
23. Cole, N. B., Sciaky, N., Marotta, A., Song, J. & Lippincott-Schwartz, J. Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell 7, 631-650 (1996).
24. Hammond, A. T. & Glick, B. S. Dynamics of transitional endoplasmic reticulum sites in vertebrate cells. Mol. Biol. Cell 11, 3013-3030 (2000).
25. Donaldson, J. G., Finazzi, D. & Klausner, R. D. Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature 360, 350-352 (1992).
26. Barlowe, C. et al. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907 (1994).
27. Kuehn, M. J., Herrmann, J. M. & Schekman, R. COPII-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature 391, 187-190 (1998).
28. Aridor, M. et al. The Sar1 GTPase coordinates biosynthetic cargo selection with endoplasmic reticulum export site assembly. J. Cell Biol. 152, 213-229 (2001).
29. Aridor, M., Bannykh, S. I., Rowe, T. & Balch, W. E. Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport. J. Cell Biol. 131, 875-893 (1995).
30. Gagnon, E. et al. Endoplasmic reticulum-mediatied phagocytosis is a mechanism of entry into macrophages. Cell 110, 119-131 (2002).
31. Khelef, N., Shuman, H. A. & Maxfield, F. R. Phagocytosis of wild-type Legionella pneumophila occurs through a wortmannin-insensitive pathway. Infect. Immun. 69, 5157-5161 (2001).
32. Ramachandra, L. & Harding, C. V. Phagosomes acquire nascent and recycling class II MHC molecules but primarily use nascent molecules in phagocytic antigen processing. J. Immunol. 164, 5103-5112 (2000).
33. Naviaux, R. K., Costanzi, E., Haas, M. & Verma, I. M. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70, 5701-5705 (1996).
34. Al-Awar, O., Radhakrishna, H., Powell, N. N. & Donaldson, J. G. Separation of membrane trafficking and actin remodeling functions of ARF6 with an effector domain mutant. Mol Cell. Biol. 20, 5998-6007 (2000).
35. Celada, A., Gray, P. W., Rinderknecht, E. & Schreiber, R. D. Evidence for a gamma-interferon receptor that regulates macrophage tumoricidal activity. J. Exp. Med. 160, 55-74 (1984).
36. Joiner, K. A., Fuhrman, S. A., Miettinen, H. M., Kasper, L. H. & Mellman, I. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor-transfected fibroblasts. Science 249, 641-646 (1990).
37. Hammond, C. & Helenius, A. Quality control in the secretory pathway. retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J. Cell Biol. 126, 41-52 (1994).
38. Shugrue, C. A. et al. Identification of the putative mammalian orthologue of Sec31P, a component of the COPII coat. J. Cell Sci. 112, 4547-4556 (1999).