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Volume 148, Issue 6

Role of the gene in amoebae Free

Abstract

infects humans, causing Legionnaires’ disease, from aerosols generated by domestic and environmental water sources. In aquatic environments is thought to replicate primarily in protozoa. A ‘repeats in structural toxin’ (RTX) gene, , from was identified recently that plays a role in entry and replication in human macrophages and also has the ability to infect mice. However, the role of this gene in the interaction of with environmental protozoa and its distribution in different species has not been examined. Southern analyses demonstrated that is present in all isolates tested and correlates with species that have been shown to cause disease in humans. To evaluate the importance of in the interaction with protozoa a series of studies was carried out in an environmental host for , . The gene plays a role in both adherence and entry into similar to that observed in human monocytic cells. Furthermore, it was found that is involved in intracellular survival and trafficking. In addition to demonstrating involvement of in the interaction of with host cells, these data support a role for this gene both during disease in humans and in environmental reservoirs.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): amoeba , LY, lucifer yellow , lysosomes , pathogenesis , phagocytosis , pneumonia , RhR, rhodamine red and RTX, repeats in structural toxin
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2002-06-01
2024-04-26
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References

  1. Abu Kwaik Y. 1996; The phagosome containing Legionella pneumophila within the protozoan Hartmannella vermiformis is surrounded by the rough endoplasmic reticulum. Appl Environ Microbiol 62:2022–2028
     [Google Scholar]
  2. Adams S. A., Robson S. C., Gathiram V., Jackson T. F., Pillay T. S., Kirsch R. E., Makgoba M. W. 1993; Immunological similarity between the 170 kD amoebic adherence glycoprotein and human beta 2 integrins. Lancet 341:17–19 [CrossRef]
     [Google Scholar]
  3. Allen P. G., Dawidowicz E. A. 1990a; Phagocytosis in Acanthamoeba : I. A mannose receptor is responsible for the binding and phagocytosis of yeast. J Cell Physiol 145:508–513 [CrossRef]
     [Google Scholar]
  4. Allen P. G., Dawidowicz E. A. 1990b; Phagocytosis in Acanthamoeba : II. Soluble and insoluble mannose-rich ligands stimulate phosphoinositide metabolism. J Cell Physiol 145:514–521 [CrossRef]
     [Google Scholar]
  5. Ambagala T. C., Ambagala A. P. N., Srikumaran S. 1999; The leukotoxin of Pasteurella haemolytica binds to β2 integrins on bovine leukocytes. FEMS Microbiol Lett 179:161–167
     [Google Scholar]
  6. Anand C. M., Skinner A. R., Malic A., Kurtz J. B. 1983; Interaction of L. pneumophila and a free living amoeba ( Acanthamoeba palestinensis) . J Hyg 91:167–178 [CrossRef]
     [Google Scholar]
  7. Armstrong J. A., Hart P. D. A. 1971; Response of cultured macrophages to Mycobacterium tuberculosis with observations on fusion of lysosomes with phagosomes. J Exp Med 134:713–740 [CrossRef]
     [Google Scholar]
  8. Behl C., Davis J. B., Lesley R., Schubert D. 1994; Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 77:817–827 [CrossRef]
     [Google Scholar]
  9. Berger K. H., Merriam J. J., Isberg R. R. 1994; Altered intracellular targeting properties associated with mutations in the Legionella pneumophila dotA gene. Mol Microbiol 14:809–822 [CrossRef]
     [Google Scholar]
  10. Bhakdi S., Muhly M., Korom S., Schmidt G. 1990; Effects of Escherichia coli hemolysin on human monocytes. Cytocidal action and stimulation of interleukin 1 release. J Clin Invest 85:1746–1753 [CrossRef]
     [Google Scholar]
  11. Bibb W. F., Sorg R. J., Thomason B. M., Hicklin M. D., Steigerwalt A. G., Brenner D. J., Wulf M. R. 1981; Recognition of a second serogroup of Legionella longbeachae . J Clin Microbiol 14:674–677
     [Google Scholar]
  12. Bibb W. F., Arnow P. M., Dellinger D. L., Perryman S. R. 1983; Isolation and characterization of a seventh serogroup of Legionella pneumophila . J Clin Microbiol 17:346–348
     [Google Scholar]
  13. Bizal C. L., Butler J. P., Feldman H. A., Valberg P. A. 1991; Kinetics of phagocytosis and phagosome–lysosome fusion in hamster lung and peritoneal macrophages. J Leukoc Biol 50:229–239
     [Google Scholar]
  14. Bowers B., Korn E. D. 1968; The fine structure of Acanthamoeba castellanii . I. The trophozoite. J Cell Biol 39:95–111 [CrossRef]
     [Google Scholar]
  15. Bozue J. A., Johnson W. 1996; Interaction of Legionella pneumophila with Acanthamoeba castellanii : Uptake by coiling phagocytosis and inhibition of phagosome–lysosome fusion. Infect Immun 64:668–673
     [Google Scholar]
  16. Brander C., Wyss-Coray T., Mauri D., Bettens F., Pichler W. J. 1993; Carrier-mediated uptake and presentation of a major histocompatibility complex class I-restricted peptide. Eur J Immunol 23:3217–3223 [CrossRef]
     [Google Scholar]
  17. Brenner D. J., Steigerwalt A. G., Gorman G. W. 8 other authors 1980; Legionella bozemanii sp. nov. and Legionella dumoffii sp. nov.: classification of two additional species of Legionella associated with human pneumonia. Curr Microbiol 4:111–116 [CrossRef]
     [Google Scholar]
  18. Brieland J., McClain M., Heath L., Chrisp C., Huffnagle G., LeGendre M., Hurley M., Fantone J., Engleberg C. 1996; Coinoculation with Hartmannella vermiformis enhances replicative Legionella pneumophila lung infection in a murine model of Legionnaires’ disease. Infect Immun 64:2449–2456
     [Google Scholar]
  19. Brieland J., McClain M., LeGendre M., Engleberg C. 1997a; Intrapulmonary Hartmannella vermiformis : a potential niche for Legionella pneumophila replication in a murine model of legionellosis. Infect Immun 65:4892–4896
     [Google Scholar]
  20. Brieland J. K., Fantone J. C., Remick D. G., LeGendre M., McClain M., Engleberg N. C. 1997b; The role of Legionella pneumophila -infected Hartmannella vermiformis as an infectious particle in a murine model of Legionnaires’ disease. Infect Immun 65:5330–5333
     [Google Scholar]
  21. Brower D. L., Brower S. M., Hayward D. C., Ball E. E. 1997; Molecular evolution of integrins: Genes encoding integrin β subunits from a coral and a sponge. Proc Natl Acad Sci USA 94:9182–9187 [CrossRef]
     [Google Scholar]
  22. Brown R. C., Bass H., Coombs J. P. 1975; Carbohydrate binding proteins involved in phagocytosis by Acanthamoeba . Nature 254:434–435 [CrossRef]
     [Google Scholar]
  23. Campbell J., Bibb W. F., Lambert M. A., Eng S., Steigerwalt A. G., Allard J., Moss C. W., Brenner D. J. 1984; Legionella sainthelensi : a new species of Legionella isolated from water near Mt. St. Helens. Appl Environ Microbiol 47:369–373
     [Google Scholar]
  24. Cianciotto N. P., Fields B. S. 1992; Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc Natl Acad Sci USA 89:5188–5191 [CrossRef]
     [Google Scholar]
  25. Cirillo J. D., Falkow S., Tompkins L. S. 1994; Growth of Legionella pneumophila in Acanthamoeba castellanii enhances invasion. Infect Immun 62:3254–3261
     [Google Scholar]
  26. Cirillo J. D., Falkow S., Tompkins L. S., Bermudez L. E. 1997; Interaction of Mycobacterium avium with environmental amoebae enhances virulence. Infect Immun 65:3759–3767
     [Google Scholar]
  27. Cirillo J. D., Cirillo S. L. G., Yan L., Bermudez L. E., Falkow S., Tompkins L. S. 1999; Intracellular growth in Acanthamoeba castellanii affects monocyte entry mechanisms and enhances virulence of Legionella pneumophila . Infect Immun 67:4427–4434
     [Google Scholar]
  28. Cirillo S. L. G., Lum J., Cirillo J. D. 2000; Identification of novel loci involved in entry by Legionella pneumophila . Microbiology 146:1345–1359
     [Google Scholar]
  29. Cirillo S. L. G., Bermudez L. E., El-Etr S. H., Duhamel G. E., Cirillo J. D. 2001; Legionella pneumophila entry gene rtxA is involved in virulence. Infect Immun 69:508–517 [CrossRef]
     [Google Scholar]
  30. Davies B., Edwards S. W. 1991; Chemiluminescence and superoxide production in Acanthamoeba castellanii : free radicals generated during oxidative stress. J Gen Microbiol 137:1021–1027 [CrossRef]
     [Google Scholar]
  31. Davies B., Chattings L. S., Edwards S. W. 1991; Superoxide generation during phagocytosis by Acanthamoeba castellanii : similarities to the respiratory burst of immune phagocytes. J Gen Microbiol 137:705–710 [CrossRef]
     [Google Scholar]
  32. Davis G. S., Winn W. C. Jr, Gump D. W., Beaty H. N. 1983; The kinetics of early inflammatory events during experimental pneumonia due to Legionella pneumophila in guinea pigs. J Infect Dis 148:823–825 [CrossRef]
     [Google Scholar]
  33. Edelstein P. H. 1981; Improved semiselective medium for isolation of Legionella pneumophila from contaminated clinical and environmental specimens. J Clin Microbiol 14:298–303
     [Google Scholar]
  34. Engleberg N. C., Drutz D. J., Eisenstein B. I. 1984; Cloning and expression of Legionella pneumophila antigens in Escherichia coli . Infect Immun 44:222–227
     [Google Scholar]
  35. Falkow S. 1988; Molecular Koch’s postulates applied to microbial pathogenicity. Rev Infect Dis 10:S274–S276 [CrossRef]
     [Google Scholar]
  36. Fields B. S., Barbaree J. M., Shotts E. B. Jr, Feeley J. C., Morrill W. E., Sanden G. N., Dykstra M. J. 1986; Comparison of guinea pig and protozoan models for determining virulence of Legionella species. Infect Immun 53:553–559
     [Google Scholar]
  37. Fields P. I., Swanson R. V., Haidaris C. G., Heffron F. 1986; Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 83:5189–5193 [CrossRef]
     [Google Scholar]
  38. Fliermans C. B., Cherry W. B., Orrison L. H., Smith S. J., Tison D. L., Pope D. H. 1981; Ecological distribution of Legionella pneumophila . Appl Environ Microbiol 41:9–16
     [Google Scholar]
  39. Francis C. L., Ryan T. A., Jones B. D., Smith S. J., Falkow S. 1993; Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 364:639–642 [CrossRef]
     [Google Scholar]
  40. Gao L. Y., Harb O. S., Abu Kwaik Y. 1997; Utilization of similar mechanisms by Legionella pneumophila to parasitize two evolutionarily distant host cells, mammalian macrophages and protozoa. Infect Immun 65:4738–4746
     [Google Scholar]
  41. Goodwin M. S., Weiss A. A. 1990; Adenylate cyclase toxin is critical for colonization and pertussis toxin is critical for lethal infection by Bordetella pertussis in infant mice. Infect Immun 58:3445–3447
     [Google Scholar]
  42. Gorman G. W., Feeley J. C., Steigerwalt A., Edelstein P. H., Moss C. W., Brenner D. J. 1985; Legionella anisa : a new species of Legionella isolated from potable waters and a cooling tower. Appl Environ Microbiol 49:305–309
     [Google Scholar]
  43. Heinzen R. A., Scidmore M. A., Rockey D. D. 1996; Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of Coxiella burnettii and Chlamydia trachomatis . Infect Immun 64:796–809
     [Google Scholar]
  44. Henke M., Seidel K. M. 1986; Association between Legionella pneumophila and amoebae in water. Isr J Med Sci 22:690–695
     [Google Scholar]
  45. Herwaldt L. A., Gorman G. W., McGrath T. 12 other authors 1984; A new Legionella species, Legionella feeleii species nova, causes Pontiac fever in an automobile plant. Ann Intern Med 100:333–338 [CrossRef]
     [Google Scholar]
  46. Horwitz M. A. 1983; Formation of a novel phagosome by the Legionnaires’ disease bacterium ( Legionella pneumophila) in human monocytes. J Exp Med 158:1319–1331 [CrossRef]
     [Google Scholar]
  47. 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 [CrossRef]
     [Google Scholar]
  48. Horwitz M. A., Maxfield F. R. 1984; Legionella pneumophila inhibits acidification of its phagosome in human monocytes. J Cell Biol 99:1936–1943 [CrossRef]
     [Google Scholar]
  49. Joly J. R., McKinney R. M., Tobin J. O., Bibb W. F., Watkins I. D., Ramsay D. 1986; Development of a standardized subgrouping scheme for Legionella pneumophila serogroup 1 using monoclonal antibodies. J Clin Microbiol 23:768–771
     [Google Scholar]
  50. Joshi A. D., Sturgill-Koszycki S., Swanson M. S. 2001; Evidence that Dot-dependent and -independent factors isolate the Legionella pneumophila phagosome from the endocytic network in mouse macrophages. Cell Microbiol 3:99–114 [CrossRef]
     [Google Scholar]
  51. Keane W. F., Welch R., Gekker G., Peterson P. K. 1987; Mechanism of Escherichia coli alpha-hemolysin-induced injury to isolated renal tubular cells. Am J Pathol 126:350–357
     [Google Scholar]
  52. Kirby J. E., Vogel J. P., Andrews H. L., Isberg I. I. 1998; Evidence for pore forming ability by Legionella pneumophila . Mol Microbiol 27:323–336 [CrossRef]
     [Google Scholar]
  53. Lally E. T., Kieba I. R., Sato A. 8 other authors 1997; RTX toxins recognize a β2 integrin on the surface of human target cells. J Biol Chem 272:30463–30469 [CrossRef]
     [Google Scholar]
  54. Lock R., Öhman L., Dahlgren C. 1987; Phagocytic recognition mechanisms in human granulocytes and Acanthamoeba castellanii using type 1 fimbriated Escherichia coli as phagocytic prey. FEMS Microbiol Lett 44:135–140 [CrossRef]
     [Google Scholar]
  55. Marston B. J., Plouffe J. F., Breiman R. F. 9 other authors 1993; Preliminary findings of a community-based pneumonia incidence study. In Legionella Current Status and Emerging Perspectives pp 36–37 Edited by Barbaree J. M., Breiman R. F., Dufour A. P. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  56. Marston B. J., Lipman H. B., Breiman R. F. 1994; Surveillance for Legionnaires’ disease. Arch Intern Med 154:2417–2422 [CrossRef]
     [Google Scholar]
  57. McClure C. D., Schiller N. L. 1996; Inhibition of macrophage phagocytosis by Pseudomonas aeruginosa rhamnolipids in vitro and in vivo . Curr Microbiol 33:109–117 [CrossRef]
     [Google Scholar]
  58. Moffat J. F., Tompkins L. S. 1992; A quantitative model of intracellular growth of Legionella pneumophila in Acanthamoeba castellanii . Infect Immun 60:296–301
     [Google Scholar]
  59. Morris G. K., Patton C. M., Feeley J. C. 7 other authors 1979; Isolation of Legionnaires’ disease bacterium from environmental samples. Ann Intern Med 90:664–666 [CrossRef]
     [Google Scholar]
  60. Morris G. K., Steigerwalt A., Feeley J. C., Wong E. S., Martin W. T., Patton C. M., Brenner D. J. 1980; Legionella gormanii sp. nov. J Clin Microbiol 12:718–721
     [Google Scholar]
  61. Nash T. W., Libby D. M., Horwitz M. A. 1984; Interaction between the Legionnaires’ disease bacterium ( Legionella pneumophila) and human alveolar macrophages. J Clin Invest 74:771–782 [CrossRef]
     [Google Scholar]
  62. Newsome A. L., Baker R. L., Miller R. D., Arnold R. D. 1985; Interactions between Naegleria fowleri and Legionella pneumophila . Infect Immun 50:449–452
     [Google Scholar]
  63. Niszl I. A., Markus M. B. 1989; Processing of free-living amoebae for transmission electron microscopy. Stain Tech 64:259–260
     [Google Scholar]
  64. Pruckler J. M., Benson R. F., Moyenuddin M., Martin W. T., Fields B. S. 1995; Association of flagellum expression and intracellular growth of Legionella pneumophila . Infect Immun 63:4928–4932
     [Google Scholar]
  65. Reingold A. L., Thomason B. M., Brake B. J., Thacker L., Wilkinson H. W., Kuritsky J. N. 1984; Legionella pneumonia in the United States: the distribution of serogroups and species causing human illness. J Infect Dis 149:819 [CrossRef]
     [Google Scholar]
  66. Rowbotham T. J. 1980; Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoeba. J Clin Pathol 33:1179–1183 [CrossRef]
     [Google Scholar]
  67. Rowbotham T. J. 1986; Current views on the relationships between amoebae, legionellae and man. Isr J Med Sci 22:678–689
     [Google Scholar]
  68. Rowbotham T. J. 1993; Legionella -like amoebal pathogens. In Legionella: Current Status and Emerging Perspectives pp 137–140 Edited by Barbaree J. M., Breiman R. F., Dufour A. P. Washington, DC: ASM Press;
     [Google Scholar]
  69. Roy C. R., Berger K. H., Isberg R. R. 1998; Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol Microbiol 28:663–674 [CrossRef]
     [Google Scholar]
  70. Scheffer J., Konig W., Hacker J., Goebel W. 1985; Bacterial adherence and hemolysin production from Escherichia coli induces histamine and leukotriene release from various cells. Infect Immun 50:271–278
     [Google Scholar]
  71. Segal G., Shuman H. A. 1999; Legionella pneumophila utilizes the same genes to multiply within Acanthamoeba castellanii and human macrophages. Infect Immun 67:2117–2124
     [Google Scholar]
  72. Straub M., Bredschneider M., Thumm M. 1997; AUT3 , a serine/threonine kinase gene, is essential for autophagocytosis in Saccharomyces cerevisiae . J Bacteriol 179:3875–3883
     [Google Scholar]
  73. Swanson J. 1989; Fluorescent labeling of endocytic compartments. Methods Cell Biol 29:137–151
     [Google Scholar]
  74. Swanson M. S., Isberg R. R. 1995; Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 63:3609–3620
     [Google Scholar]
  75. Swanson M. S., Isberg R. R. 1996; Identification of Legionella pneumophila mutants that have aberrant intracellular fates. Infect Immun 64:2585–2594
     [Google Scholar]
  76. Venkataraman C., Haack B. J., Bondada S., Abu Kwaik Y. 1997; Identification of a Gal/GalNAc lectin in the protozoan Hartmanella vermiformis as a potential receptor for attachment and invasion by the Legionnaires’ disease bacterium, Legionella pneumophila . J Exp Med 186:537–547 [CrossRef]
     [Google Scholar]
  77. Vines R. R., Ramakrishnan G., Rogers J. B., Lockhart L. A., Mann B. J., Petri W. A. Jr 1998; Regulation of adherence and virulence by the Entamoeba histolytica lectin cytoplasmic domain, which contains a β2 integrin motif. Mol Biol Cell 9:2069–2079 [CrossRef]
     [Google Scholar]
  78. Welch R. A. 1991; Pore-forming cytolysin of Gram-negative bacteria. Mol Microbiol 5:521–528 [CrossRef]
     [Google Scholar]
  79. Wiater L. A., Dunn K., Maxfield F. R., Shuman H. A. 1998; Early events in phagosome establishment are required for intracellular survival of Legionella pneumophila . Infect Immun 66:4450–4460
     [Google Scholar]
  80. Wilkinson H. W., Drasar V., Thacker W. L., Benson R. F., Schindler J., Potuznikova B., Mayberry W. R., Brenner D. J. 1988; Legionella moravica sp. nov. and Legionella brunensis sp. nov. isolated from cooling-tower water. Ann Inst Pasteur Microbiol 139:393–402 [CrossRef]
     [Google Scholar]
  81. Winn W. C. Jr, Myerowitz R. L. 1981; The pathology of Legionella pneumonias. A review of 74 cases and the literature. Human Pathol 12:401–422 [CrossRef]
     [Google Scholar]
  82. Yu V. L., Zuravleff J. J., Gavlik L., Magnussen M. H. 1983; Lack of evidence for person-to-person transmission of Legionnaires’ disease. J Infect Dis 147:362 [CrossRef]
     [Google Scholar]
  83. Zuckman D. M., Hung J. B., Roy C. R. 1999; Pore-forming activity is not sufficient for Legionella pneumophila phagosome trafficking and intracellular growth. Mol Microbiol 32:990–1001 [CrossRef]
     [Google Scholar]
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Role of the Legionella pneumophila rtxA gene in amoebae
Microbiology 148, 1667 (2002); https://doi.org/10.1099/00221287-148-6-1667
/content/journal/micro/10.1099/00221287-148-6-1667
/content/journal/micro/10.1099/00221287-148-6-1667
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