Interaction of Legionella pneumophila with Amoeba

  • Maélle Molmeret
  • Marina Santic
  • Yousef Abu Kwaik
Part of the Infectious Diseases And Pathogenesis book series (IAPA)


Secretion System Dictyostelium Discoideum Coxiella Burnetii Intracellular Growth Intracellular Replication 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Abu Kwaik, Y. (1996) The phagosome containing Legionella pneumophila within the protozoan Hartmanella vermiformis is surrounded by the rough endoplasmic reticulum. Appl. Environ. Microbiol. 62: 2022–2028.PubMedGoogle Scholar
  2. Abu Kwaik, Y. (1998) Induced expression of the Legionella pneumophila gene encoding a 20-kilodalton protein during intracellular infection. Infect. Immun. 66: 203–212.PubMedGoogle Scholar
  3. Abu Kwaik, Y., Fields, B.S., and Engleberg, N.C. (1994) Protein expression by the protozoan Hartmannella vermiformis upon contact with its bacterial parasite Legionella pneumophila. Infect. Immun. 62: 1860–1866.PubMedGoogle Scholar
  4. Abu Kwaik, Y., Gao, L.-Y., Harb, O.S. and Stone, B.J. (1997) Transcriptional regulation of the macrophage-induced gene (gspA) of Legionella pneumophila and phenotypic characterization of a null mutant. Mol. Microbiol. 24: 629–642.PubMedCrossRefGoogle Scholar
  5. Abu Kwaik, Y., Venkataraman, C., Gao, L.-Y., and Harb, O.S. (1998a) Signal transduction in the protozoan host Hartmannella vermiformis upon attachment and invasion by its bacterial parasite, the Legionnaires’ disease agent, Legionella micdadei. Appl. Environ. Microbiol. 64: 3134–3139.Google Scholar
  6. Abu Kwaik, Y., Gao, L.-Y., Stone, B.J., Venkataraman, C. and Harb, O.S. (1998b) Invasion of protozoa by Legionella pneumophila and its role in bacterial ecology and pathogenesis. Appl. Environ. Microbiol. 64: 3127–3133.Google Scholar
  7. Adeleke, A., Pruckler, J., Benson, R., Rowbotham, T., Halablab, M., and Fields, B.S. (1996) Legionella-like amoebal pathogens-phylogenetic status and possible role in respiratory disease. Emerg. Infect. Dis. 2: 225–229.PubMedCrossRefGoogle Scholar
  8. Adeleke, A.A., Fields, B.S., Benson, R.F., Daneshvar, M.I., Pruckler, J.M., Ratcliff, R.M. (2001) Legionella drozanskii sp. nov., Legionella rowbothamii sp. nov. and Legionella fallonii sp. nov.: three unusual new Legionella species. Int. J. Syst. Evol. Microbiol. 51: 1151–1160.PubMedGoogle Scholar
  9. Alli, O.A., Zink, S., von Lackum, N.K., and Abu-Kwaik, Y. (2003) Comparative assessment of virulence traits in Legionella spp. Microbiology. 149: 631–641.PubMedCrossRefGoogle Scholar
  10. Bandyopadhyay, P., Xiao, H., Coleman, H.A., Price-Whelan, A., and Steinman, H.M. (2004) Icm/dot-independent entry of Legionella pneumophila into amoeba and macrophage hosts. Infect. Immun. 72: 4541–4551.PubMedCrossRefGoogle Scholar
  11. Bardill, J.P., Miller, J.L., and Vogel, J.P. (2005) IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol. Microbiol. 56: 90–103.PubMedCrossRefGoogle Scholar
  12. Barker, J. and Brown, M.R. (1994) Trojan horses of the microbial world: protozoa and the survival of bacterial pathogens in the environment. Microbiology. 140 (Pt 6): 1253–1259.PubMedGoogle Scholar
  13. Barker, J., Brown, M.R.W., Collier, P.J., Farrell, I., and Gilbert, P. (1992) Relationships between Legionella pneumophila and Acanthamoebae polyphaga: physiological status and susceptibility to chemical inactivation. Appl. Environ. Microbiol. 58: 2420–2425.PubMedGoogle Scholar
  14. Barker, J., Lambert, P.A., and Brown, M.R.W. (1993) Influence of intra-amoebic and other growth conditions on the surface properties of Legionella pneumophila. Infect. Immun. 61: 3503–3510.PubMedGoogle Scholar
  15. Barker, J., Scaife, H., and Brown, M.R.W. (1995) Intraphagocytic growth induces an antibiotic-resistant phenotype of Legionella pneumophila. Antimicrob. Agents Chemother. 39: 2684–2688.PubMedGoogle Scholar
  16. Berger, K.H. and Isberg, R.R. (1993) Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7: 7–19.PubMedCrossRefGoogle Scholar
  17. Berk, S.G., Ting, R.S., Turner, G.W., and Ashburn, R.J. (1998) Production of respirable vesicles containing live Legionella pneumophila cells by two Acanthamoeba spp. Appl. Environ. Microbiol. 64: 279–286.PubMedGoogle Scholar
  18. Birtles, R.J., Rowbotham, T.J., Raoult, D., and Harrison, T.G. (1996) Phylogenetic diversity of intra-amoebal legionellae as revealed by 16S rRNA gene sequence comparison. Microbiology. 142: 3525–3530.PubMedCrossRefGoogle Scholar
  19. Biurrun, A., Caballero, L., Pelaz, C., Leon, E., and Gago, A. (1999) Treatment of a Legionella pneumophila-colonized water distribution system using copper-silver ionization and continuous chlorination. Infect. Control. Hosp. Epidemiol. 20: 426–428.PubMedCrossRefGoogle Scholar
  20. Bozue, J.A. and Johnson, W. (1996) Interaction of Legionella pneumophila with Acanthamoeba catellanii: uptake by coiling phagocytosis and inhibition of phagosome-lysosome fusion. Infect. Immun. 64: 668–673.PubMedGoogle Scholar
  21. Brand, B., Sadosky, A.B., and Shuman, H.A. (1994) The Legionella pneumophila icm locus: a set of genes required for intracellular multiplication in human macrophages. Mol.Microbiol. 14: 797–808.PubMedCrossRefGoogle Scholar
  22. Brieland, J.K., Fantone, J.C., Remick, D.G., LeGendre, M., McClain, M., and Engleberg, N.C. (1997) The role of Legionella pneumophila-infected Hartmanella vermiformis as an infectious particle in a murine model of Legionnaires’ disease. Infect. Immun. 65: 4892–4896.PubMedGoogle Scholar
  23. Chen, J., de Felipe, K.S., Clarke, M., Lu, H., Anderson, O.R., Segal, G., and Shuman, H.A. (2004) Legionella effectors that promote nonlytic release from protozoa. Science. 303: 1358–1361.PubMedCrossRefGoogle Scholar
  24. Christie, P.J. and Vogel, J.P. (2000) Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8: 354–360.PubMedCrossRefGoogle Scholar
  25. Cianciotto, N.P. and Fields, B.S. (1992) Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc. Natl. Acad. Sci. USA. 89: 5188–5191.PubMedCrossRefGoogle Scholar
  26. Cirillo, J.D., Tompkins, L.S., and Falkow, S. (1994) Growth of Legionella pneumophila in Acanthamoeba castellanii enhances invasion. Infect. Immun. 62: 3254–3261.PubMedGoogle Scholar
  27. Cirillo, J.D., Cirillo, S.L., Yan, L., Bermudez, L.E., Falkow, S., and Tompkins, L.S. (1999) Intracellular growth in acanthamoeba castellanii affects monocyte entry mechanisms and enhances virulence of legionella pneumophila. Infect. Immun. 67: 4427–4434.PubMedGoogle Scholar
  28. Cirillo, S.L., Lum, J., and Cirillo, J.D. (2000) Identification of novel loci involved in entry by Legionella pneumophila. Microbiology. 146: 1345–1359.PubMedGoogle Scholar
  29. Cirillo, S.L., Bermudez, L.E., El-Etr, S.H., Duhamel, G.E., and Cirillo, J.D. (2001) Legionella pneumophila entry gene rtxA is involved in virulence. Infect Immun. 69: 508–517.PubMedCrossRefGoogle Scholar
  30. Coers, J., Kagan, J.C., Matthews, M., Nagai, H., Zuckman, D.M. and Roy, C.R. (2000) 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.PubMedCrossRefGoogle Scholar
  31. Conover, G.M., Derre, I., Vogel, J.P., and Isberg, R.R. (2003) The Legionella pneumophila LidA protein: a translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity. Mol. Microbiol. 48: 305–321.PubMedCrossRefGoogle Scholar
  32. Darelid, J., Lofgren, S., and Malmvall, B.E. (2002) Control of nosocomial Legionnaires’ disease by keeping the circulating hot water temperature above 55 degrees C: experience from a 10-year surveillance programme in a district general hospital. J. Hosp. Infect. 50: 213–219.PubMedCrossRefGoogle Scholar
  33. Derre, I. and Isberg, R.R. (2004) Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system. Infect. Immun. 72: 3048–3053.PubMedCrossRefGoogle Scholar
  34. Fajardo, M., Schleicher, M., Noegel, A., Bozzaro, S., Killinger, S., Heuner, K. (2004) Calnexin, calreticulin and cytoskeleton-associated proteins modulate uptake and growth of Legionella pneumophila in Dictyostelium discoideum. Microbiology. 150: 2825–2835.PubMedCrossRefGoogle Scholar
  35. Feldman, M.F. and Cornelis, G.R. (2003) The multitalented type III chaperones: all you can do with 15 kDa. FEMS Microbiol Lett. 219: 151–158.PubMedCrossRefGoogle Scholar
  36. Feldman, M., Zusman, T., Hagag, S., and Segal, G. (2005) Coevolution between nonhomologous but functionally similar proteins and their conserved partners in the Legionella pathogenesis system. Proc. Natl. Acad. Sci. U S A. 102: 12206–12211.PubMedCrossRefGoogle Scholar
  37. Fields, B.S. (1996) The molecular ecology of legionellae. Trends. Microbiol. 4: 286–290.PubMedCrossRefGoogle Scholar
  38. Fields, B.S., Nerad, T.A., Sawyer, T.K., King, C.H., Barbaree, J.M., Martin, W.T. , et al. (1990) Characterization of an axenic strain of Hartmannella vermiformis obtained from an investigation of nosocomial legionellosis. J. Protozool. 37: 581–583.Google Scholar
  39. Fields, B.S., Benson, R.F. and Besser, R.E. (2002) Legionella and Legionnaires’ disease: 25 years of investigation. Clin. Microbiol. Rev. 15: 506–526.PubMedCrossRefGoogle Scholar
  40. Fliermans, C.B. (1996) Ecology of Legionella: From data to knowledge with a little wisdom. Microb. Ecol. 32: 203–228.PubMedCrossRefGoogle Scholar
  41. Fraser, D.W., Tsai, T.R., Orenstein, W., Parkin, W.E., Beecham, H.J., Sharrar, R.G., et al. (1977) Legionnaires’ disease: description of an epidemic of pneumonia. N. Engl. J. Med. 297: 1189–1197.PubMedCrossRefGoogle Scholar
  42. Gao, L.-Y., Harb, O.S., and Abu Kwaik, Y. (1997) Utilization of similar mechanisms by Legionella pneumophila to parasitize two evolutionarily distant hosts, mammalian and protozoan cells. Infect. Immun. 65: 4738–4746.PubMedGoogle Scholar
  43. Gao, L.-Y., Harb, O.S., and Abu Kwaik, Y. (1998) Identification of macrophage-specific infectivity loci (mil) of Legionella pneumophila that are not required for infectivity of protozoa. Infect. Immun. 66: 883–892.PubMedGoogle Scholar
  44. Gao, L.-Y., Susa, M., Ticac, B., and Abu Kwaik, Y. (1999) Heterogeneity in intracellular replication and cytopathogenicity of Legionella pneumophila and Legionella micdadei in mammalian and protozoan cells. Microb. Pathog. 27: 273–287.PubMedCrossRefGoogle Scholar
  45. 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.Google Scholar
  46. Harb, O.S., Venkataraman, C., Haack, B.J., Gao, L.-Y., and Abu Kwaik, Y. (1998) Heterogeneity in the attachment and uptake mechanisms of the Legionnaires’ disease bacterium, Legionella pneumophila, by protozoan hosts. Appl. Environ. Microbiol. 64: 126–132.PubMedGoogle Scholar
  47. Harb, O.S., Gao, L.-Y., and Abu Kwaik, Y. (2000) From protozoa to mammalian cells: A new paradigm in the life cycle of intracellular bacterial pathogens. Environ. Microbiol. 2: 251–265.PubMedCrossRefGoogle Scholar
  48. Hilbi, H., Segal, G., and Shuman, H.A. (2001) Icm/dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol. Microbiol. 42: 603–617.Google Scholar
  49. Hoebe, C.J. and Kool, J.L. (2000) Control of legionella in drinking-water systems. Lancet. 355: 2093–2094.PubMedCrossRefGoogle Scholar
  50. Horwitz, M.A. (1983a) The Legionnaires’ disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J. Exp. Med. 158: 2108–2126.CrossRefGoogle Scholar
  51. Horwitz, M.A. (1983b) Formation of a novel phagosome by the Legionnaires’ disease bacterium (Legionella pneumophila) in human monocytes. J. Exp. Med. 158: 1319–1331.CrossRefGoogle Scholar
  52. Horwitz, M.A. (1984) Phagocytosis of the Legionnaires’ disease bacterium (Legionella pneumophila) occurs by a novel mechanism: engulfment within a pseudopod coil. Cell. 36: 27–33.PubMedCrossRefGoogle Scholar
  53. Horwitz, M.A. and Silverstein, S.C. (1981) Interaction of the legionnaires’ disease bacterium (Legionella pneumophila) with human phagocytes. II. Antibody promotes binding of L. pneumophila to monocytes but does not inhibit intracellular multiplication. J. Exp. Med. 153: 398–406.PubMedCrossRefGoogle Scholar
  54. Kagan, J.C. and Roy, C.R. (2002) Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat. Cell Biol. 4: 945–954.PubMedCrossRefGoogle Scholar
  55. Kagan, J.C., Stein, M.P., Pypaert, M., and Roy, C.R. (2004) Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle. J. Exp. Med. 199: 1201–1211.PubMedCrossRefGoogle Scholar
  56. Kirby, J.E. and Isberg, R.R. (1998) Legionnaires’ disease: the pore macrophage and the legion of terror within. Trends. Microbiol. 6: 256–258.PubMedCrossRefGoogle Scholar
  57. Kirby, J.E., Vogel, J.P., Andrews, H.L., and Isberg, R.R. (1998) Evidence for pore-forming ability by Legionella pneumophila. Mol. Microbiol. 27: 323–336.Google Scholar
  58. Komano, T., Yoshida, T., Narahara, K., and Furuya, N. (2000) The transfer region of IncI1 plasmid R64: similarities between R64 tra and legionella icm/dot genes. Mol. Microbiol. 35: 1348–1359.PubMedCrossRefGoogle Scholar
  59. Kool, J.L., Carpenter, J.C., and Fields, B.S. (1999) Effect of monochloramine disinfection of municipal drinking water on risk of nosocomial Legionnaires’ disease. Lancet. 353: 272–277.PubMedCrossRefGoogle Scholar
  60. Kusnetsov, J., Iivanainen, E., Elomaa, N., Zacheus, O. and Martikainen, P.J. (2001) Copper and silver ions more effective against legionellae than against mycobacteria in a hospital warm water system. Water Res. 35: 4217–4225.PubMedCrossRefGoogle Scholar
  61. Li, Z., Solomon, J.M., and Isberg, R.R. (2005) Dictyostelium discoideum strains lacking the RtoA protein are defective for maturation of the Legionella pneumophila replication vacuole. Cell. Microbiol. 7: 431–442.PubMedCrossRefGoogle Scholar
  62. Luo, Z.Q. and Isberg, R.R. (2004) Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc. Natl. Acad. Sci. U S A. 101: 841–846.PubMedCrossRefGoogle Scholar
  63. Mann, B.J., Torian, B.E., Vedvick, T.S., and Petri, W.A.J. (1991) Sequence of a cysteine-rich galactose-specific lectin of Entamoeba histolytica. Proc. Natl. Acad. Sci. USA. 88: 3248–3252.Google Scholar
  64. Marra, A., Horwitz, M.A., and Shuman, H.A. (1990) The HL-60 model for the interaction of human macrophages with the Legionnaires’ disease bacterium. J.Immunol. 144: 2738–2744.PubMedGoogle Scholar
  65. Marrie, T.J., Raoult, D., La Scola, B., Birtles, R.J. and de Carolis, E. (2001) Legionellalike and other amoebal pathogens as agents of community-acquired pneumonia. Emerg. Infect. Dis. 7: 1026–1029.PubMedCrossRefGoogle Scholar
  66. McDade, J.E., Shepard, C.C., Fraser, D.W., Tsai, T.R., Redus, M.A., and Dowdle, W.R. (1977) Legionnaires’ disease: isolation of a bacterium and demonstration of its role in other respiratory disease. N. Engl. J. Med. 297: 1197–1203.PubMedCrossRefGoogle Scholar
  67. Molmeret, M., Bitar, D.M., Han, L., and Kwaik, Y.A. (2004) Disruption of the phagosomal membrane and egress of Legionella pneumophila into the cytoplasm during the last stages of intracellular infection of macrophages and Acanthamoeba polyphaga. Infect. Immun. 72: 4040–4051.Google Scholar
  68. Molmeret, M., Horn, M., Wagner, M., Santic, M. and Abu Kwaik, Y. (2005) Amoebae as training grounds for intracellular bacterial pathogens. Appl. Environ. Microbiol. 71: 20–28.PubMedCrossRefGoogle Scholar
  69. Muraca, P., Stout, J.E., and Yu, V.L. (1987) Comparative assessment of chlorine, heat, ozone, and UV light for killing Legionella pneumophila within a model plumbing system. Appl. Environ. Microbiol. 53: 447–453.PubMedGoogle Scholar
  70. Murga, R., Forster, T.S., Brown, E., Pruckler, J.M., Fields, B.S., and Donlan, R.M. (2001) Role of biofilms in the survival of Legionella pneumophila in a model potable-water system. Microbiology. 147: 3121–3126.PubMedGoogle Scholar
  71. 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.PubMedCrossRefGoogle Scholar
  72. Nagai, H., Cambronne, E.D., Kagan, J.C., Amor, J.C., Kahn, R.A. and Roy, C.R. (2005) A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc. Natl. Acad. Sci. U S A. 102: 826–831.PubMedCrossRefGoogle Scholar
  73. Newsome, A.L., Baker, R.L., Miller, R.D., and Arnold, R.R. (1985) Interactions between Naegleria fowleri and Legionella pneumophila. Infect. Immun. 50: 449–452.Google Scholar
  74. Ninio, S., Zuckman-Cholon, D.M., Cambronne, E.D. and Roy, C.R. (2005) The Legionella IcmS-IcmW protein complex is important for Dot/Icm-mediated protein translocation. Mol. Microbiol. 55: 912–926.PubMedCrossRefGoogle Scholar
  75. O’Brein, S.J. and Bhopal, R.S. (1993) Legionnaires’ disease: the infective dose paradox. Lancet. 342: 5–6.CrossRefGoogle Scholar
  76. Otto, G.P., Wu, M.Y., Clarke, M., Lu, H., Anderson, O.R., Hilbi, H., et al. (2004) Macroautophagy is dispensable for intracellular replication of Legionella pneumophila in Dictyostelium discoideum. Mol. Microbiol. 51: 63–72.PubMedCrossRefGoogle Scholar
  77. Payne, N.R. and Horwitz, M.A. (1987) Phagocytosis of Legionella pneumophila is mediated by human monocyte complement receptors. J. Exp. Med. 166: 1377–1389.PubMedCrossRefGoogle Scholar
  78. Rodriguez-Zaragoza, S. (1994) Ecology of free-living amoebae. Crit Rev Microbiol. 20: 225–241.PubMedGoogle Scholar
  79. Rowbotham, T.J. (1980) Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J. Clin. Pathol. 33: 1179–1183.PubMedCrossRefGoogle Scholar
  80. Rowbotham, T.J. (1983) Isolation of Legionella pneumophila from clinical specimens via amoebae, and the interaction of those and other isolates with amoebae. J. Clin. Pathol. 36: 978–986.PubMedCrossRefGoogle Scholar
  81. Rowbotham, T.J. (1986) Current views on the relationships between amoebae, legionellae and man. Isr. J. Med. Sci. 22: 678–689.PubMedGoogle Scholar
  82. Roy, C.R. and Tilney, L.G. (2002) The road less traveled: transport of Legionella to the endoplasmic reticulum. J. Cell Biol. 158: 415–419.PubMedCrossRefGoogle Scholar
  83. Segal, G. and Shuman, H.A. (1997) Characterization of a new region required for macrophage killing by Legionella pneumophila. Infect. Immun. 65: 5057–5066.Google Scholar
  84. Segal, G. and Shuman, H.A. (1999) Legionella pneumophila utilizes the same genes to multiply within Acanthamoeba castellanii and human macrophages. Infect. Immun. 67: 2117–2124.PubMedGoogle Scholar
  85. 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 chromosome. Proc. Natl. Acad. Sci. USA. 95: 1669–1674.PubMedCrossRefGoogle Scholar
  86. Segal, G., Russo, J.J., and Shuman, H.A. (1999) Relationships between a new type IV secretion system and the icm/dot virulence system of Legionella pneumophila. Mol. Microbiol. 34: 799–809.Google Scholar
  87. Seshadri, R., Paulsen, I.T., Eisen, J.A., Read, T.D., Nelson, K.E., Nelson, W.C., et al. (2003) Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc Natl Acad Sci U S A. 100: 5455–5460.CrossRefGoogle Scholar
  88. Sexton, J.A. and Vogel, J.P. (2002) Type IVB secretion by intracellular pathogens. Traffic. 3: 178–185.PubMedCrossRefGoogle Scholar
  89. Shadrach, W.S., Rydzewski, K., Laube, U., Holland, G., Ozel, M., Kiderlen, A.F., and Flieger, A. (2005) Balamuthia mandrillaris, free-living ameba and opportunistic agent of encephalitis, is a potential host for Legionella pneumophila bacteria. Appl. Environ. Microbiol. 71: 2244–2249.PubMedCrossRefGoogle Scholar
  90. Sheehan, K.B., Henson, J.M., and Ferris, M.J. (2005) Legionella species diversity in an acidic biofilm community in Yellowstone National Park. Appl. Environ. Microbiol. 71: 507–511.PubMedCrossRefGoogle Scholar
  91. Solomon, J.M. and Isberg, R.R. (2000) Growth of Legionella pneumophila in Dictyostelium discoideum: a novel system for genetic analysis of host-pathogen interactions. Trends Microbiol. 8: 478–480.PubMedCrossRefGoogle Scholar
  92. 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.PubMedCrossRefGoogle Scholar
  93. Steinert, M., Emody, L., Amann, R., and Hacker, J. (1997) Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Appl. Environ. Microbiol. 63: 2047–2053.Google Scholar
  94. Stone, B.J., Brier, A., and Kwaik, Y.A. (1999) The Legionella pneumophila prp locus; required during infection of macrophages and amoebae. Microb. Pathog. 27: 369–376.PubMedCrossRefGoogle Scholar
  95. Swanson, M.S. and Isberg, R.R. (1995) Formation of the Legionella pneumophila replicative phagosome. Infect. Agents Dis. 2: 269–271.Google Scholar
  96. Tilney, L.G., Harb, O.S., Connelly, P.S., Robinson, C.G., and Roy, C.R. (2001) 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.PubMedGoogle Scholar
  97. Venkataraman, C., Haack, B.J., Bondada, S., and Abu Kwaik, Y. (1997) Identification of a Gal/GalNAc lectin in the protozoan Hartmannella vermiformis as a potential receptor for attachment and invasion by the Legionnaires’ disease bacterium, Legionella pneumophila. J. Exp. Med. 186: 537–547.CrossRefGoogle Scholar
  98. Venkataraman, C., Gao, L.-Y., Bondada, S., and Abu Kwaik, Y. (1998) Identification of putative cytoskeletal protein homologues in the protozoan Hartmannella vermiformis as substrates for induced tyrosine phosphatase activity upon attachment to the Legionnaires’ disease bacterium, Legionella pneumophila. J. Exp. Med. 188: 505–514.CrossRefGoogle Scholar
  99. 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.Google Scholar
  100. 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/Icm system and the mouse Lgn1 locus. J. Exp. Med. 194: 1081–1096.PubMedCrossRefGoogle Scholar
  101. Yamamoto, H., Ezaki, T., Ikedo, M., and Yabuuchi, E. (1991) Effects of biocidal treatments to inhibit the growth of legionellae and other microorganisms in cooling towers. Microbiol. Immunol. 35: 795–802.PubMedGoogle Scholar
  102. Zamboni, D.S., McGrath, S., Rabinovitch, M., and Roy, C.R. (2003) Coxiella burnetii express type IV secretion system proteins that function similarly to components of the Legionella pneumophila Dot/Icm system. Mol. Microbiol. 49: 965–976.PubMedCrossRefGoogle Scholar
  103. Zusman, T., Yerushalmi, G., and Segal, G. (2003) Functional similarities between the icm/dot pathogenesis systems of Coxiella burnetii and Legionella pneumophila. Infect. Immun. 71: 3714–3723.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Maélle Molmeret
  • Marina Santic
  • Yousef Abu Kwaik

There are no affiliations available

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