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Controlling the maturation of pathogen-containing vacuoles: a matter of life and death

Nature Cell Biology volume 1, pages E183–E188 (1999)Cite this article

Abstract

Once considered to be contained, infectious diseases of bacterial origin are now making a comeback. A lack of innovative therapies and the appearance of drug-resistant pathogens are becoming increasingly serious problems. A better understanding of pathogen–host interactions at the cellular and molecular levels is necessary to define new targets in our fight against microorganisms. In the past few years, the merging of cell biology and microbiology has started to yield critical and often surprising new information on the interactions that occur between various pathogens and their mammalian host cells. Here we focus on the intracellular routing of vacuoles containing microorganisms, as well as on the bacterial effectors and their host-cell targets that control vacuole maturation. We also describe new approaches for isolating microorganism-containing vacuoles and analysing their molecular composition, which will help researchers to define the molecules and mechanisms governing vacuole biogenesis.

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Figure 1: Phagosome versus vacuole.
Figure 2: Salmonella induces spectacular reorganization of the host cytoskeleton and lysosomal compartments.

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References

  1. Sinai, A. P. & Joiner, K. A. Safe haven: the cell biology of nonfusogenic pathogen vacuoles. Annu. Rev. Microbiol. 51, 415–462 (1997).

    Article  CAS  PubMed  Google Scholar 

  2. Schlesinger, L. S. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors . J. Immunol. 150, 2920– 2930 (1993).

    CAS  PubMed  Google Scholar 

  3. Horwitz, M. A. Phagocytosis of the Legionnaires’ disease bacterium (Legionella pneumophila) occurs by a novel mechanism: engulfment within a pseudopod coil. Cell 36, 27–33 ( 1984).

    Article  CAS  PubMed  Google Scholar 

  4. Rittig, M. G. et al. Coiling phagocytosis of trypanosomatids and fungal cells. Infect. Immun. 66, 4331–4339 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Mengaud, J., Ohayon, H., Gounon, P., Mege, R. M. & Cossart, P. E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell 84, 923–932 ( 1996).

    Article  CAS  PubMed  Google Scholar 

  6. Lecuit, M. et al. A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J. 18, 3956–3963 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kubori, T. et al. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280, 602 –605 (1998).

    Article  CAS  PubMed  Google Scholar 

  8. Hueck, C. J. Type III protein secretion systems in bacterial pathogens of animals and plants . Microbiol. Mol. Biol. Rev. 62, 379– 433 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zhou, D., Mooseker, M. S. & Galan, J. E. Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 283, 2092–2095 (1999).

    Article  CAS  PubMed  Google Scholar 

  10. Hayward, R. D. & Koronakis, V. Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J. 18, 4926–4934 ( 1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Hardt, W. D., Chen, L. M., Schuebel, K. E., Bustelo, X. R. & Galan, J. E. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93, 815–826 (1998).

    Article  CAS  PubMed  Google Scholar 

  12. Nhieu, G. T. & Sansonetti, P. J. Mechanism of Shigella entry into epithelial cells. Curr. Opin. Microbiol. 2, 51–55 (1999).

    Article  CAS  PubMed  Google Scholar 

  13. Menard, R., Sansonetti, P., Parsot, C. & Vasselon, T. Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of S. flexneri. Cell 79, 515– 525 (1994).

    Article  CAS  PubMed  Google Scholar 

  14. Tran Van Nhieu, G., Caron, E., Hall, A. & Sansonetti, P. J. IpaC induces actin polymerization and filopodia formation during Shigella entry into epithelial cells. EMBO J. 18, 3249– 3262 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Desjardins, M., Huber, L. A., Parton, R. G. & Griffiths, G. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124, 677–688 (1994).

    Article  CAS  PubMed  Google Scholar 

  16. Novick, P. & Zerial, M. The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol. 9, 496–504 (1997).

    Article  CAS  PubMed  Google Scholar 

  17. Mayorga, L. S., Bertini, F. & Stahl, P. D. Fusion of newly formed phagosomes with endosomes in intact cells and in a cell-free system. J. Biol. Chem. 266, 6511–6517 (1991).

    Article  CAS  PubMed  Google Scholar 

  18. Desjardins, M. Biogenesis of phagolysosomes: the ‘kiss and run’ hypothesis. Trends Cell Biol. 5, 183–186 (1995).

    CAS  PubMed  Google Scholar 

  19. Andrews, N. W. Lysosome recruitment during host cell invasion by Trypanosoma cruzi. Trends Cell Biol. 5, 133–137 (1995).

    Article  CAS  PubMed  Google Scholar 

  20. Dramsi, S. & Cossart, P. Intracellular pathogens and the actin cytoskeleton. Annu. Rev. Cell Dev. Biol. 14, 137–166 (1998).

    Article  CAS  PubMed  Google Scholar 

  21. High, N., Mounier, J., Prevost, M. C. & Sansonetti, P. J. IpaB of Shigella flexneri causes entry into epithelial cells and escape from the phagocytic vacuole. EMBO J. 11, 1991 –1999 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Heinzen, R. A., Grieshaber, S. S., Van Kirk, L. S. & Devin, C. J. Dynamics of actin-based movement by Rickettsia rickettsii in vero cells. Infect. Immun. 67, 4201–4207 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Cossart, P. & Lecuit, M. Interactions of Listeria monocytogenes with mammalian cells during entry and actin-based movement: bacterial factors, cellular ligands and signaling. EMBO J. 17, 3797–3806 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Geoffroy, C., Gaillard, J. L., Alouf, J. E. & Berche, P. Purification, characterization, and toxicity of the sulfhydryl-activated hemolysin listeriolysin O from Listeria monocytogenes. Infect. Immun. 55, 1641–1646 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Alvarez-Dominguez, C., Barbieri, A. M., Beron, W., Wandinger-Ness, A. & Stahl, P. D. Phagocytosed live Listeria monocytogenes influences Rab5-regulated in vitro phagosome-endosome fusion. J. Biol. Chem. 271, 13834–13843 (1996).

    Article  CAS  PubMed  Google Scholar 

  26. Alvarez-Dominguez, C., Roberts, R. & Stahl, P. D. Internalized Listeria monocytogenes modulates intracellular trafficking and delays maturation of the phagosome. J. Cell Sci. 110, 731–743 ( 1997).

    Article  CAS  PubMed  Google Scholar 

  27. Alvarez-Dominguez, C. & Stahl, P. D. Increased expression of Rab5a correlates directly with accelerated maturation of Listeria monocytogenes phagosomes. J. Biol. Chem. 274, 11459– 11462 (1999).

    Article  CAS  PubMed  Google Scholar 

  28. Suss-Toby, E., Zimmerberg, J. & Ward, G. E. Toxoplasma invasion: the parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore . Proc. Natl Acad. Sci. USA 93, 8413– 8418 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. 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).

    Article  CAS  PubMed  Google Scholar 

  30. Schwab, J. C., Beckers, C. J. & Joiner, K. A. The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc. Natl Acad. Sci. USA 91, 509– 513 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Vogel, J. P. & Isberg, R. R. Cell biology of Legionella pneumophila . Curr. Opin. Microbiol. 2, 30– 34 (1999).

    Article  CAS  PubMed  Google Scholar 

  32. Segal, G. & Shuman, H. A. How is the intracellular fate of the Legionella pneumophila phagosome determined? Trends Microbiol. 6, 253–255 (1998).

    Article  CAS  PubMed  Google Scholar 

  33. Kirby, J. E. & Isberg, R. R. Legionnaires’ disease: the pore macrophage and the legion of terror within. Trends Microbiol. 6, 256–258 ( 1998).

    Article  CAS  PubMed  Google Scholar 

  34. Zuckman, D. M., Hung, J. B. & Roy, C. R. Pore-forming activity is not sufficient for legionella pneumophila phagosome trafficking and intracellular growth. Mol. Microbiol. 32, 990–1001 (1999).

    Article  CAS  PubMed  Google Scholar 

  35. Roy, C. R. & Isberg, R. R. Topology of Legionella pneumophila DotA: an inner membrane protein required for replication in macrophages. Infect. Immun. 65, 571–578 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Roy, C. R., Berger, K. H. & 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).

    Article  CAS  PubMed  Google Scholar 

  37. Coers, J., Monahan, C. & Roy, C. R. Modulation of phagosome biogenesis by Legionella pneumophila creates an organelle permissive for intracellular growth. Nature Cell Biol. (in the press).

  38. Andrews, H. L., Vogel, J. P. & Isberg, R. R. Identification of linked Legionella pneumophila genes essential for intracellular growth and evasion of the endocytic pathway. Infect. Immun. 66, 950–958 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Matsumoto, A., Bessho, H., Uehira, K. & Suda, T. Morphological studies of the association of mitochondria with chlamydial inclusions and the fusion of chlamydial inclusions. J. Electron Microsc. 40, 356–363 (1991).

    CAS  Google Scholar 

  40. Scidmore, M. A., Fischer, E. R. & Hackstadt, T. Sphingolipids and glycoproteins are differentially trafficked to the Chlamydia trachomatis inclusion. J. Cell Biol. 134, 363–374 (1996).

    Article  CAS  PubMed  Google Scholar 

  41. Boleti, H., Benmerah, A., Ojcius, D. M., Cerf-Bensussan, N. & Dautry-Varsat, A. Chlamydia infection of epithelial cells expressing dynamin and eps15 mutants: clathrin-independent entry into cells and dynamin-dependent productive growth. J. Cell Sci. 112, 1487–1496 (1999).

    Article  CAS  PubMed  Google Scholar 

  42. Scidmore-Carlson, M. A., Shaw, E. I., Dooley, C. A., Fischer, E. R. & Hackstadt, T. Identification and characterization of a Chlamydia trachomatis early operon encoding four novel inclusion membrane proteins. Mol. Microbiol. 33, 753– 765 (1999).

    Article  CAS  PubMed  Google Scholar 

  43. Pizarro-Cerda, J. et al. Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect. Immun. 66, 5711–5724 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Sola-Landa, A. et al. A two-component regulatory system playing a critical role in plant pathogens and endosymbionts is present in Brucella abortus and controls cell invasion and virulence. Mol. Microbiol. 29, 125–138 (1998).

    Article  CAS  PubMed  Google Scholar 

  45. O’Callaghan, D. et al. A homologue of the Agrobacterium tumefaciens BirB and Bordetella pertussis Ptl Type IV secretion system is essential for intracellular survival of Brucella suis. Mol. Microbiol. 33 , 1210–1220 (1999).

    Article  PubMed  Google Scholar 

  46. Hsia, R. C., Pannekoek, Y., Ingerowski, E. & Bavoil, P. M. Type III secretion genes identify a putative virulence locus of Chlamydia . Mol. Microbiol. 25, 351–359 (1997).

  47. Deretic, V. & Fratti, R. A. Mycobacterium tuberculosis phagosome . Mol. Microbiol. 31, 1603– 1609 (1999).

    Article  CAS  PubMed  Google Scholar 

  48. Sturgill-Koszycki, S. et al. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263, 678–681 (1994).

    Article  CAS  PubMed  Google Scholar 

  49. Via, L. E. et al. 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 (1997).

    Article  CAS  PubMed  Google Scholar 

  50. de Chastellier, C., Lang, T. & Thilo, L. Phagocytic processing of the macrophage endoparasite, Mycobacterium avium, in comparison to phagosomes which contain Bacillus subtilis or latex beads . Eur. J. Cell Biol. 68, 167– 182 (1995).

    CAS  PubMed  Google Scholar 

  51. Sturgill-Koszycki, S., Schaible, U. E. & Russell, D. G. Mycobacterium-containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis . EMBO J. 15, 6960–6968 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Ferrari, G., Langen, H., Naito, M. & Pieters, J. A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97, 435–447 ( 1999).

    Article  CAS  PubMed  Google Scholar 

  53. Rauchenberger, R., Hacker, U., Murphy, J., Niewohner, J. & Maniak, M. Coronin and vacuolin identify consecutive stages of a late, actin-coated endocytic compartment in Dictyostelium. Curr. Biol. 7, 215–218 ( 1997).

    Article  CAS  PubMed  Google Scholar 

  54. de Hostos, E. L. The coronin family of actin-associated proteins. Trends Cell Biol. 9, 345–350 ( 1999).

    Article  CAS  PubMed  Google Scholar 

  55. Scianimanico, S. et al. Impaired recruitment of the small GTPase rab7 correlates with the inhibition of phagosome maturation by Leishmania donovani promastigotes . Cell. Microbiol. 1, 19– 32 (1999).

    Article  CAS  PubMed  Google Scholar 

  56. Desjardins, M. & Descoteaux, A. Inhibition of phagolysosomal biogenesis by the Leishmania lipophosphoglycan. J. Exp. Med. 185, 2061–2068 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Russell, D. G., Xu, S. & Chakraborty, P. Intracellular trafficking and the parasitophorous vacuole of Leishmania mexicana-infected macrophages. J. Cell Sci. 103, 1193–1210 (1992).

    Article  PubMed  Google Scholar 

  58. Steele-Mortimer, O., Méresse, S., Toh, B.-H., Gorvel, J.-P. & Finlay, B. B. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell. Microbiol. 1, 33– 50 (1999).

    Article  CAS  PubMed  Google Scholar 

  59. Garcia-del Portillo, F. & Finlay, B. B. Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J. Cell Biol. 129, 81–97 ( 1995).

    Article  CAS  PubMed  Google Scholar 

  60. Méresse, S., Steele-Mortimer, O., Finlay, B. B. & Gorvel, J.-P. The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuole in HeLa cells. EMBO J. 18, 4394– 4403 (1999).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Garcia-del Portillo, F., Zwick, M. B., Leung, K. Y. & Finlay, B. B. Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells. Proc. Natl Acad. Sci. USA 90, 10544–10548 ( 1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Cuervo, A. M. & Dice, J. F. A receptor for the selective uptake and degradation of proteins by lysosomes. Science 273 , 501–503 (1996).

    Article  CAS  PubMed  Google Scholar 

  63. Hensel, M. et al. Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol. Microbiol. 30, 163–174 (1998).

    Article  CAS  PubMed  Google Scholar 

  64. Uchiya, K. et al. A Salmonella virulence protein that inhibits cellular trafficking . EMBO J. 18, 3924–3933 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Schiavo, G. et al. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359, 832–835 (1992).

    Article  CAS  PubMed  Google Scholar 

  66. Schaible, U. E., Sturgill-Koszycki, S., Schlesinger, P. H. & Russell, D. G. Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J. Immunol. 160, 1290–1296 ( 1998).

    CAS  PubMed  Google Scholar 

  67. Via, L. E. et al. Effects of cytokines on mycobacterial phagosome maturation . J. Cell Sci. 111, 897– 905 (1998).

    Article  CAS  PubMed  Google Scholar 

  68. Alvarez-Dominguez, C. & Stahl, P. D. Interferon-gamma selectively induces Rab5a synthesis and processing in mononuclear cells. J. Biol. Chem. 273, 33901–33904 (1998).

    Article  CAS  PubMed  Google Scholar 

  69. Tanaka, T. et al. Targeted disruption of the NF-IL6 gene discloses its essential role in bacteria killing and tumor cytotoxicity by macrophages. Cell 80, 353–361 ( 1995).

    Article  CAS  PubMed  Google Scholar 

  70. Pizarro-Cerda, J., Desjardins, M., Moreno, E., Akira, S. & Gorvel, J. P. Modulation of endocytosis in nuclear factor IL-6(–/–) macrophages is responsible for a high susceptibility to intracellular bacterial infection. J. Immunol. 162 , 3519–3526 (1999).

    CAS  PubMed  Google Scholar 

  71. Skamene, E. Genetic control of susceptibility to infections with intracellular pathogens . Pathol. Biol. 46, 689– 692 (1998).

    CAS  PubMed  Google Scholar 

  72. Cellier, M. et al. Nramp defines a family of membrane proteins. Proc. Natl Acad. Sci. USA 92, 10089–10093 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Gruenheid, S., Pinner, E., Desjardins, M. & Gros, P. Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome. J. Exp. Med. 185, 717–730 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Cellier, M., Belouchi, A. & Gros, P. Resistance to intracellular infections: comparative genomic analysis of Nramp. Trends Genet. 12, 201–204 (1996).

    Article  CAS  PubMed  Google Scholar 

  75. Agranoff, D. D. & Krishna, S. Metal ion homeostasis and intracellular parasitism. Mol. Microbiol. 28, 403–412 (1998).

    Article  CAS  PubMed  Google Scholar 

  76. Hensel, M. et al. Simultaneous identification of bacterial virulence genes by negative selection. Science 269, 400– 403 (1995).

    Article  CAS  PubMed  Google Scholar 

  77. Valdivia, R. H. & Falkow, S. Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277, 2007–2011 ( 1997).

    Article  CAS  PubMed  Google Scholar 

  78. Strauss, E. J. & Falkow, S. Microbial pathogenesis: genomics and beyond. Science 276, 707– 712 (1997).

    Article  CAS  PubMed  Google Scholar 

  79. Shea, J. E., Hensel, M., Gleeson, C. & Holden, D. W. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl Acad. Sci. USA 93, 2593–2597 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Wilkins, M. R., Sanchez, J. C., Williams, K. L. & Hochstrasser, D. F. Current challenges and future applications for protein maps and post-translational vector maps in proteome projects. Electrophoresis 17 , 830–838 (1996).

    Article  CAS  PubMed  Google Scholar 

  81. Chakraborty, P., Sturgill-Koszycki, S. & Russell, D. G. Isolation and characterization of pathogen-containing phagosomes. Methods Cell Biol. 45, 261– 276 (1994).

    Article  CAS  PubMed  Google Scholar 

  82. Mills, S. D. & Finlay, B. B. Isolation and characterization of Salmonella typhimurium and Yersinia pseudotuberculosis-containing phagosomes from infected mouse macrophages: Y. pseudotuberculosis traffics to terminal lysosomes where they are degraded. Eur. J. Cell Biol. 77, 35–47 (1998).

    Article  CAS  PubMed  Google Scholar 

  83. Lindberg, A. A. Vaccination against enteric pathogens: from science to vaccine trials. Curr. Opin. Microbiol. 1, 116–124 (1998).

    Article  CAS  PubMed  Google Scholar 

  84. Russmann, H. et al. Delivery of epitopes by the Salmonella type III secretion system for vaccine development. Science 281, 565–568 (1998).

    Article  CAS  PubMed  Google Scholar 

  85. Kaufmann, S. H. & Hess, J. Impact of intracellular location of and antigen display by intracellular bacteria: implications for vaccine development. Immunol. Lett. 65, 81–84 (1999).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank J. Ewbank, A. Labrousse and M.J. Martinez for helpful comments and suggestions. This work was supported by the CNRS (PICS 558), INSERM (J.-P.G., S.M. and E.M.) and grants from the Medical Research Council of Canada (M.D. and B.F.).

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Authors and Affiliations

  1. Centre d’Immunologie de Marseille Luminy, Parc scientifique de Luminy, Case 906, Marseille, 13288, Cedex 9, France

    Stéphane Méresse & Jean-Pierre Gorvel

  2. Biotechnology Laboratory, University of British Columbia , 237-6174 University Blvd, Vancouver, V6T-1Z3, British Columbia, Canada

    Olivia Steele-Mortimer & Brett Finlay

  3. Programa de Investigacion en Enfermedades tropicales, Universidad nacional, Heredia, Costa Rica

    Edgardo Moreno

  4. Département de Pathologie et biologie cellulaire Université de Montréal, CP 6128, succ. Centre ville, Montréal, H3C 3J7, Québec, Canada

    Michel Desjardins

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  1. Stéphane Méresse
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Correspondence to Jean-Pierre Gorvel.

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Méresse, S., Steele-Mortimer, O., Moreno, E. et al. Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nat Cell Biol 1, E183–E188 (1999). https://doi.org/10.1038/15620

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