Flotillin and RacH modulate the intracellular immunity of Dictyostelium to Mycobacterium marinum infection

Cellular Microbiology

Volumn 9, Issue 11, 2007, Pages 2716-2733

  Hagedorn, Monica ^a   Soldati, Thierry ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; COPPER; FLOTILLIN 1; GUANOSINE TRIPHOSPHATASE; ISOPROTEIN; PROTEIN P80; RAC PROTEIN; VACUOLATING TOXIN;

ANIMAL CELL; ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; CELL PROLIFERATION; CELL SPREADING; CELL VACUOLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOSOL; DICTYOSTELIUM DISCOIDEUM; EXPERIMENTAL MODEL; FLUORESCENCE ACTIVATED CELL SORTING; HOST; HUMAN; HUMAN CELL; INFECTION RESISTANCE; INFECTION SENSITIVITY; INHIBITION KINETICS; MONOCYTE; MYCOBACTERIUM MARINUM; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PHAGOSOME; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY; TUBERCULOSIS;

ANIMALS; CELLS, CULTURED; CYTOSKELETAL PROTEINS; DICTYOSTELIUM; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNITY, NATURAL; MEMBRANE PROTEINS; MONOCYTES; MONOMERIC GTP-BINDING PROTEINS; MUTATION; MYCOBACTERIUM INFECTIONS, ATYPICAL; MYCOBACTERIUM MARINUM; PROMOTER REGIONS (GENETICS); PROTOZOAN PROTEINS;

DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM; MYCOBACTERIUM MARINUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 34848871338     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2007.00993.x     Document Type: Article

References (58)

1. Aniento, F., Emans, N., Griffiths, G., and Gruenberg, J. (1993) Cytoplasmic dynein-dependent vesicular transport from early to late endosomes. J Cell Biol 123: 1373-1387.
2. Arellano-Reynoso, B., Lapaque, N., Salcedo, S., Briones, G., Ciocchini, A.E., Ugalde, R., et al. (2005) Cyclic beta-1,2-glucan is a Brucella virulence factor required for intracellular survival. Nat Immunol 6: 618-625.
3. Barker, L.P., George, K.M., Falkow, S., and Small, P.L. (1997) Differential trafficking of live and dead Mycobacterium marinum organisms in macrophages. Infect Immun 65: 1497-1504.
4. Bauer, M., and Pelkmans, L. (2006) A new paradigm for membrane-organizing and -shaping scaffolds. FEBS Lett 580: 5559-5564.
5. Byrd, T.F., Green, G.M., Fowlston, S.E., and Lyons, C.R. (1998) Differential growth characteristics and streptomycin susceptibility of virulent and avirulent Mycobacterium tuberculosis strains in a novel fibroblast-mycobacterium microcolony assay. Infect Immun 66: 5132-5139.
6. Cosma, C.L., Klein, K., Kim, R., Beery, D., and Ramakrishnan, L. (2006) Mycobacterium marinum Erp is a virulence determinant required for cell wall integrity and intracellular survival. Infect Immun 74: 3125-3133.
7. Cosson, P., Zulianello, L., Join-Lambert, O., Faurisson, F., Gebbie, L., Benghezal, M., et al. (2002) Pseudomonas aeruginosa virulence analyzed in a Dictyostelium discoideum host system. J Bacteriol 184: 3027-3033.
8. Dermine, J.F., Duclos, S., Garin, J., St-Louis, F., Rea, S., Parton, R.G., and Desjardins, M. (2001) Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J Biol Chem 276: 18507-18512.
9. Dionne, M.S., Ghori, N., and Schneider, D.S. (2003) Drosophila melanogaster is a genetically tractable model host for Mycobacterium marinum. Infect Immun 71: 3540-3550.
10. Ferrari, G., Langen, H., Naito, M., and Pieters, J. (1999) A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97: 435-447.
11. Fivaz, M., Vilbois, F., Thurnheer, S., Pasquali, C., Abrami, L., Bickel, P.E., et al. (2002) Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J 21: 3989-4000.
12. Fratti, R.A., Chua, J., Vergne, I., and Deretic, V. (2003) Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci USA 100: 5437-5442.
13. Gao, L.Y., Groger, R., Cox, J.S., Beverley, S.M., Lawson, E.H., and Brown, E.J. (2003a) Transposon mutagenesis of Mycobacterium marinum identifies a locus linking pigmentation and intracellular survival. Infect Immun 71: 922-929.
14. Gao, L.Y., Guo, S., McLaughlin, B., Morisaki, H., Engel, J.N., and Brown, E.J. (2004) A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 53: 1677-1693.
15. Gao, L.Y., Pak, M., Kish, R., Kajihara, K., and Brown, E.J. (2006) A mycobacterial operon essential for virulence in vivo and invasion and intracellular persistence in macrophages. Infect Immun 74: 1757-1767.
16. Gotthardt, D., Warnatz, H.J., Henschel, O., Bruckert, F., Schleicher, M., and Soldati, T. (2002) High-resolution dissection of phagosome maturation reveals distinct membrane trafficking phases. Mol Biol Cell 13: 3508-3520.
17. Gotthardt, D., Blancheteau, V., Bosserhoff, A., Ruppert, T., Delorenzi, M., and Soldati, T. (2006) Proteomic fingerprinting of phagosome maturation and evidence for the role of a Galpha during uptake. Cell Microbiol 5: 2228-2243
18. Grode, L., Seiler, P., Baumann, S., Hess, J., Brinkmann, V., Nasser Eddine, A., et al. (2005) Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis bacille Calmette-Guerin mutants that secrete listeriolysin. J Clin Invest 115: 2472-2479.
19. Hagedorn, M., Neuhaus, E.M., and Soldati, T. (2006) Optimised fixation and immunofluorescence staining methods for Dictyostelium cells. Methods Mol Biol 346: 327-338.
20. Hagele, S., Kohler, R., Merkert, H., Schleicher, M., Hacker, J., and Steinert, M. (2000) Dictyostelium discoideum: A new host model system for intracellular pathogens of the genus Legionella. Cell Microbiol 2: 165-171.
21. Hiller, N.L., Akompong, T., Morrow, J.S., Holder, A.A., and Haldar, K. (2003) Identification of a stomatin orthologue in vacuoles induced in human erythrocytes by malaria parasites. A role for microbial raft proteins in apicomplexan vacuole biogenesis. J Biol Chem 278: 48413-48421.
22. Jenne, N., Rauchenberger, R., Hacker, U., Kast, T., and Maniak, M. (1998) Targeted gene disruption reveals a role for vacuolin B in the late endocytic pathway and exocytosis. J Cell Sci 111: 61-70.
23. Journet, A., Chapel, A., Jehan, S., Adessi, C., Freeze, H., Klein, G., and Garin, J. (1999) Characterization of Dictyostelium discoideum cathepsin D. Molecular cloning, gene disruption, endo-lysosomal localization and sugar modifications. J Cell Sci 112: 3833-3843.
24. Kobayashi, T., Stang, E., Fang, K.S., de Moerloose, P., Parton, R.G., and Gruenberg, J. (1998) A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392: 193-197.
25. Maniak, M. (2002) Conserved features of endocytosis in Dictyostelium. Int Rev Cytol 221: 257-287.
26. Maniak, M. (2003) Fusion and fission events in the endocytic pathway of Dictyostelium. Traffic 4: 1-5.
27. McDonough, K.A., Kress, Y., and Bloom, B.R. (1993) Pathogenesis of tuberculosis: Interaction of Mycobacterium tuberculosis with macrophages. Infect Immun 61: 2763-2773.
28. Neuhaus, E.M., Horstmann, H., Almers, W., Maniak, M., and Soldati, T. (1998) Ethane-freezing/methanol-fixation of cell monolayers. A procedure for improved preservation of structure and antigenicity for light and electron microscopies. J Struct Biol 121: 326-342.
29. Neuhaus, E.M., Almers, W., and Soldati, T. (2002) Morphology and dynamics of the endocytic pathway in Dictyostelium discoideum. Mol Biol Cell 13: 1390-1407.
30. Nose, Y., Rees, E.M., and Thiele, D.J. (2006) Structure of the Ctr1 copper trans 'PORE' ter reveals novel architecture. Trends Biochem Sci 31: 604-607.
31. Peracino, B., Wagner, C., Balest, A., Balbo, A., Pergolizzi, B., Noegel, A.A., et al. (2006) Function and mechanism of action of Dictyostelium Nramp1 (Slc11a1) in bacterial infection. Traffic 7: 22-38.
32. Philips, J.A., Rubin, E.J., and Perrimon, N. (2005) Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 309: 1251-1253.
33. Piddington, D.L., Fang, F.C., Laessig, T., Cooper, A.M., Orme, I.M., and Buchmeier, N.A. (2001) Cu,Zn superoxide dismutase of Mycobacterium tuberculosis contributes to survival in activated macrophages that are generating an oxidative burst. Infect Immun 69: 4980-4987.
34. van Pittius, N.C.G., Sampson, L.S., Lee, H., Kim, Y., van Helden, P.D., and Warren, R.M. (2006) Evolution and expansion of the Mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the ESAT-6 (esx) gene cluster regions. BMC Evol Biol 6: 1471-2148.
35. Pozos, T.C., and Ramakrishnan, L. (2004) New models for the study of Mycobacterium - host interactions. Curr Opin Immunol 16: 499-505.
36. Pukatzki, S., Kessin, R.H., and Mekalanos, J.J. (2002) The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc Natl Acad Sci USA 99: 3159-3164.
37. Pukatzki, S., Ma, A.T., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W.C., et al. (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA 103: 1528-1533.
38. Ramakrishnan, L., Federspiel, N.A., and Falkow, S. (2000) Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 288: 1436-1439.
39. Rauchenberger, R., Hacker, U., Murphy, J., Niewohner, J., and Maniak, M. (1997) Coronin and vacuolin identify consecutive stages of a late, actin-coated endocytic compartment in Dictyostelium. Curr Biol 7: 215-218.
40. Ravanel, K., de Chassey, B., Cornillon, S., Benghezal, M., Zulianello, L., Gebbie, L., et al. (2001) Membrane sorting in the endocytic and phagocytic pathway of Dictyostelium discoideum. Eur J Cell Biol 80: 754-764.
41. Russell, D.G. (2001) Mycobacterium tuberculosis: Here today, and here tomorrow. Nat Rev Mol Cell Biol 2: 569-577.
42. Schuller, S., Neefjes, J., Ottenhoff, T., Thole, J., and Young, D. (2001) Coronin is involved in uptake of Mycobacterium bovis BCG in human macrophages but not in phagosome maintenance. Cell Microbiol 3: 785-793.
43. Solomon, J.M., Rupper, A., Cardelli, J.A., and Isberg, R.R. (2000) Intracellular growth of Legionella pneumophila in Dictyostelium discoideum, a system for genetic analysis of host-pathogen interactions. Infect Immun 68: 2939-2947.
44. Solomon, J.M., Leung, G.S., and Isberg, R.R. (2003) Intracellular replication of Mycobacterium marinum within Dictyostelium discoideum: efficient replication in the absence of host coronin. Infect Immun 71: 3578-3586.
45. Somesh, B.P., Neffgen, C., Iijima, M., Devreotes, P., and Rivero, F. (2006) Dictyostelium RacH regulates endocytic vesicular trafficking and is required for localization of vacuolin. Traffic 7: 1194-1212.
46. Stamm, L.M., Morisaki, J.H., Gao, L.Y., Jeng, R.L., McDonald, K.L., Roth, R., et al. (2003) Mycobacterium marinum escapes from phagosomes and is propelled by actin-based motility. J Exp Med 198: 1361-1368.
47. Stamm, L.M., Pak, M.A., Morisaki, J.H., Snapper, S.B., Rottner, K., Lommel, S., and Brown, E.J. (2005) Role of the WASP family proteins for Mycobacterium marinum actin tail formation. Proc Natl Acad Sci USA 102: 14837-14842.
48. Sturgill-Koszycki, S., Schlesinger, P.H., Chakraborty, P., Haddix, P.L., Collins, H.L., Fok, A.K., et al. (1994) Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263: 678-681.
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. Swaim, L.E., Connolly, L.E., Volkman, H.E., Humbert, O., Born, D.E., and Ramakrishnan, L. (2006) Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infect Immun 74: 6108-6117.
51. Tan, T., Lee, W.L., Alexander, D.C., Grinstein, S., and Liu, J. (2006) The ESAT-6/CFP-10 secretion system of Mycobacterium marinum modulates phagosome maturation. Cell Microbiol 8: 1417-1429.
52. Vergne, I., Chua, J., Singh, S.B., and Deretic, V. (2004a) Cell biology of mycobacterium tuberculosis phagosome. Annu Rev Cell Dev Biol 20: 367-394.
53. Vergne, I., Fratti, R.A., Hill, P.J., Chua, J., Belisle, J., and Deretic, V. (2004b) Mycobacterium tuberculosis phagosome maturation arrest: Mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion. Mol Biol Cell 15: 751-760.
54. Vergne, I., Singh, S., Roberts, E., Kyei, G., Master, S., Harris, J., et al. (2006) Autophagy in immune defense against mycobacterium tuberculosis. Autophagy 2: 175-178.
55. Volkman, H.E., Clay, H., Beery, D., Chang, J.C., Sherman, D.R., and Ramakrishnan, L. (2004) Tuberculous granuloma formation is enhanced by a mycobacterium virulence determinant. PLoS Biol 2: E367.
56. Weber, S.S., Ragaz, C., Reus, K., Nyfeler, Y., and Hilbi, H. (2006) Legionella pneumophila exploits PI(4)P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog 2: E46.
57. van der Wel, N., Hava, D., Houben, D., Fluitsma, D., van Zon, M., Brenner, M., and Peters, P. (2007) M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell (in press).
58. Wienke, D., Drengk, A., Schmauch, C., Jenne, N., and Maniak, M. (2006) Vacuolin, a flotillin/reggie-related protein from Dictyostelium oligomerizes for endosome association. Eur J Cell Biol 85: 991-1000.