1887

Abstract

is a facultative intracellular pathogen that accounts for the majority of cases of Legionnaires' disease in the USA and Europe, but other spp. have been shown to cause disease. In contrast, is the leading cause of Legionnaires' disease in Australia. The hallmark of Legionnaires' disease caused by is the intracellular replication within phagocytes in the alveolar spaces, and the Dot/Icm type IV secretion system is essential for intracellular replication. Although it has been presumed that intracellular replication within phagocytes is the hallmark of other virulent legionellae, the virulence traits of spp. apart from are not well defined. In this study, 27 strains of spp. belonging to 16 species that have been isolated from humans or from the environment were examined for five virulence traits exhibited by : cytopathogenicity, intracellular replication within macrophages, induction of apoptosis/DNA fragmentation, pore-formation-mediated cytolysis of the host cell, and the presence of the / loci. The strains were divided into two broad groups (low and high cytopathogenic groups) based on cytopathogenicity assays using U937 human-derived macrophages. The other four virulence traits were evaluated in the low and high cytopathogenic groups of species. Most serogroup 1 strains were highly cytopathogenic after 72 h, manifested high levels of intracellular growth, induced apoptosis/DNA fragmentation, and exhibited pore-forming activity. The majority of the other species were the low cytopathogenic group that did not induce apoptosis, neither did they exhibit pore-forming activity. All the species of legionellae tested have all the / loci, when examined by DNA hybridization. No correlation was found between cytopathogenicity and the other four pathogenic traits.

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2003-03-01
2019-10-21
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References

  1. Abu Kwaik, Y. ( 1998; ). Fatal attraction of mammalian cells to Legionella pneumophila. Mol Microbiol 30, 689–696.[CrossRef]
    [Google Scholar]
  2. Abu Kwaik, Y. & Pederson, L. L. ( 1996; ). The use of differential display-PCR to isolate and characterize a Legionella pneumophila locus induced during the intracellular infection of macrophages. Mol Microbiol 21, 543–556.[CrossRef]
    [Google Scholar]
  3. Abu Kwaik, Y., Gao, L.-Y., Harb, O. S. & 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.[CrossRef]
    [Google Scholar]
  4. Abu Kwaik, Y., Gao, L.-Y., Stone, B. J. & Harb, O. S. ( 1998; ). Invasion of mammalian and protozoan cells by Legionella pneumophila.: Bull Inst Pasteur 96, 237–247.[CrossRef]
    [Google Scholar]
  5. Adeleke, A., Pruckler, J., Benson, R., Rowbotham, T., Halablab, M. & Fields, B. S. ( 1996; ). Legionella-like amoebal pathogens – phylogenetic status and possible role in respiratory disease. Emerg Infect Dis 2, 225–229.[CrossRef]
    [Google Scholar]
  6. Alli, O. A. T., Gao, L.-Y., Pedersen, L. L., Zink, S., Radulic, M., Doric, M. & Abu Kwaik, Y. ( 2000; ). Temporal pore formation-mediated egress from macrophages and alveolar epithelial cells by Legionella pneumophila. Infect Immun 68, 6431–6440.[CrossRef]
    [Google Scholar]
  7. Arakaki, N., Higa, F., Koide, M., Tateyama, M. & Saito, A. ( 2002; ). Induction of apoptosis of human macrophages in vitro by Legionella longbeachae through activation of the caspase pathway. J Med Microbiol 51, 159–168.
    [Google Scholar]
  8. Benin, A. L., Benson, R. F. & Besser, R. E. ( 2002; ). Trends in Legionnaires' disease, 1980–1998: declining mortality and new patterns of diagnosis. Clin Infect Dis 35, 1039–1046.[CrossRef]
    [Google Scholar]
  9. Benson, R. F. & Fields, B. S. ( 1998; ). Classification of the genus Legionella. Semin Respir Infect 13, 90–99.
    [Google Scholar]
  10. Byrne, B. & Swanson, M. S. ( 1998; ). Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun 66, 3029–3034.
    [Google Scholar]
  11. Den Boer, J. W., Yzerman, E. P., Schellekens, J. & 11 other authors ( 2002; ). A large outbreak of Legionnaires' disease at a flower show, the Netherlands, 1999. Emerg Infect Dis 8, 37–43.[CrossRef]
    [Google Scholar]
  12. Dowling, J. N., Kroboth, F. J., Karpf, M., Yee, R. B. & Pasculle, A. W. ( 1983; ). Pneumonia and multiple lung abscesses caused by dual infection with Legionella micdadei and Legionella pneumophila. Am Rev Respir Dis 127, 121–125.
    [Google Scholar]
  13. Doyle, R. M., Steele, T. W., McLennan, A. M., Parkinson, I. H., Manning, P. A. & Heuzenroeder, M. W. ( 1998; ). Sequence analysis of the mip gene of the soilborne pathogen Legionella longbeachae. Infect Immun 66, 1492–1499.
    [Google Scholar]
  14. Doyle, R. M., Cianciotto, N. P., Banvi, S., Manning, P. A. & Heuzenroeder, M. W. ( 2001; ). Comparison of virulence of Legionella longbeachae strains in guinea pigs and U937 macrophage-like cells. Infect Immun 69, 5335–5344.[CrossRef]
    [Google Scholar]
  15. Gao, L.-Y. & Abu Kwaik, Y. ( 1999a; ). Activation of caspase-3 in Legionella pneumophila-induced apoptosis in macrophages. Infect Immun 67, 4886–4894.
    [Google Scholar]
  16. Gao, L.-Y. & Abu Kwaik, Y. ( 1999b; ). Apoptosis in macrophages and alveolar epithelial cells during early stages of infection by Legionella pneumophila and its role in cytopathogenicity. Infect Immun 67, 862–870.
    [Google Scholar]
  17. Gao, L.-Y. & Abu Kwaik, Y. ( 2000a; ). Hijacking the apoptotic pathways of the host cell by bacterial pathogens. Microb Infect 2, 1705–1719.[CrossRef]
    [Google Scholar]
  18. Gao, L.-Y. & Abu Kwaik, Y. ( 2000b; ). The mechanism of killing and exiting the protozoan host Acanthamoeba polyphaga by Legionella pneumophila. Environ Microbiol 2, 79–90.[CrossRef]
    [Google Scholar]
  19. Gao, L.-Y., Stone, B. J., Brieland, J. K. & Abu Kwaik, Y. ( 1998; ). Different fates of Legionella pneumophila pmi and mil mutants within human-derived macrophages and alveolar epithelial cells. Microb Pathog 25, 291–306.[CrossRef]
    [Google Scholar]
  20. Halberstam, M., Isenberg, H. D. & Hilton, E. ( 1992; ). Abscess and empyema caused by Legionella micdadei. J Clin Microbiol 30, 512–513.
    [Google Scholar]
  21. Harb, O. S., Gao, L.-Y. & 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.[CrossRef]
    [Google Scholar]
  22. Hebert, G. A., Thomason, B. M., Harris, P. P., Hicklin, M. D. & McKinney, R. M. ( 1980; ). “Pittsburgh pneumonia agent”: a bacterium phenotypically similar to Legionella pneumophila and identical to the TATLOCK bacterium. Ann Intern Med 92, 53–54.[CrossRef]
    [Google Scholar]
  23. Hilbi, H., Segal, G. & Shuman, H. A. ( 2001; ). Icm/Dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol Microbiol 42, 603–617.
    [Google Scholar]
  24. 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]
  25. Izu, K., Yoshida, S., Miyamoto, H., Chang, B., Ogawa, M., Yamamoto, H., Goto, Y. & Taniguchi, H. ( 1999; ). Grouping of 20 reference strains of Legionella species by the growth ability within mouse and guinea pig macrophages. FEMS Immunol Med Microbiol 26, 61–68.[CrossRef]
    [Google Scholar]
  26. Jaulhac, B., Nowicki, M., Bornstein, N., Meunier, O., Prevost, G., Piemont, Y., Fleurette, J. & Moteil, H. ( 1992; ). Detection of Legionella spp. in bronchoalveolar lavage fluids by DNA amplification. J Clin Microbiol 30, 920–924.
    [Google Scholar]
  27. Joseph, C. A., Hutchinson, E. J., Dedman, D., Birtles, R. J., Watson, J. M. & Bartlett, C. L. ( 1995; ). Legionnaires' disease surveillance: England and Wales 1994. Commun Dis Rep CDR Rev 5, R180–R183.
    [Google Scholar]
  28. Joseph, C. A., Harrison, T. G., Ilijic-Car, D. & Bartlett, C. L. ( 1997; ). Legionnaires' disease in residents of England and Wales: 1996. Commun Dis Rep CDR Rev 7, R153–R159.
    [Google Scholar]
  29. Joshi, A. D. & Swanson, M. S. ( 1999; ). Comparative analysis of Legionella pneumophila and Legionella micdadei virulence traits. Infect Immun 67, 4134–4142.
    [Google Scholar]
  30. Kirby, J. E., Vogel, J. P., Andrews, H. L. & Isberg, R. R. ( 1998; ). Evidence for pore-forming ability by Legionella pneumophila. Mol Microbiol 27, 323–336.[CrossRef]
    [Google Scholar]
  31. Koide, M. & Saito, A. ( 1995; ). Diagnosis of Legionella pneumophila infection by polymerase chain reaction. Clin Infect Dis 21, 199–201.[CrossRef]
    [Google Scholar]
  32. Levi, M. H., Pasculle, A. W. & Dowling, J. N. ( 1987; ). Role of the alveolar macrophage in host defense and immunity to Legionella micdadei pneumonia in guinea pig. Microb Pathog 2, 269–282.[CrossRef]
    [Google Scholar]
  33. Lo Presti, F., Riffard, S., Meugnier, H. & 8 other authors ( 1999; ). Legionella taurinensis sp. nov., a new species antigenically similar to Legionella spiritensis. Int J Syst Bacteriol 49, 397–403.[CrossRef]
    [Google Scholar]
  34. Lo Presti, F., Riffard, S., Meugnier, H. & 9 other authors ( 2001; ). Legionella gresilensis sp. nov. and Legionella beliardensis sp. nov., isolated from water in France. Int J Syst Evol Microbiol 51, 1949–1957.[CrossRef]
    [Google Scholar]
  35. Marston, B. J. ( 1995; ). Epidemiology of community-acquired pneumonia. Infect Dis Clin Pract 4, S232–S239.
    [Google Scholar]
  36. Marston, B. J., Lipman, H. B. & Breiman, R. F. ( 1994; ). Surveillance for Legionnaires' disease: risk factors for mortality and morbidity. Arch Intern Med 154, 2417–2422.[CrossRef]
    [Google Scholar]
  37. Matthews, M. & Roy, C. R. ( 2000; ). Identification and subcellular localization of the Legionella pneumophila IcmX protein: a factor essential for establishment of a replicative organelle in eukaryotic host cells. Infect Immun 68, 3971–3982.[CrossRef]
    [Google Scholar]
  38. 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]
  39. Molmeret, M. & Abu Kwaik, Y. ( 2002; ). How does Legionella pneumophila exit the host cell? Trends Microbiol 10, 258–60.[CrossRef]
    [Google Scholar]
  40. Molmeret, M., Alli, O. A. T., Marina, R., Milorad, S., Mijenko, D. & Abu Kwaik, Y. ( 2002a; ). The C-terminus of icmT is essential for the pore formation and for intracellular trafficking of L. pneumophila within A. polyphaga. Mol Microbiol 43, 1139–1150.[CrossRef]
    [Google Scholar]
  41. Molmeret, M., Alli, O. A., Zink, S., Flieger, A., Cianciotto, N. P. & Kwaik, Y. A. ( 2002b; ). icmT is essential for pore formation-mediated egress of Legionella pneumophila from mammalian and protozoan cells. Infect Immun 70, 69–78.[CrossRef]
    [Google Scholar]
  42. Neumeister, B., Schoniger, S., Faigle, M., Eichner, M. & Dietz, K. ( 1997; ). Multiplication of different Legionella species in Mono Mac 6 cells and in Acanthamoeba castellanii. Appl Environ Microbiol 63, 1219–1224.
    [Google Scholar]
  43. O'Connell, W. A., Bangsborg, J. M. & Cianciotto, N. P. ( 1995; ). Characterization of a Legionella micdadei mip mutant. Infect Immun 63, 2840–2845.
    [Google Scholar]
  44. O'Connell, W. A., Dhand, L. & Cianciotto, N. P. ( 1996; ). Infection of macrophage-like cells by Legionella species that have not been associated with disease. Infect Immun 64, 4381–4384.
    [Google Scholar]
  45. Pasculle, A. W., Feeley, J. C., Gibson, R. J. & 7 other authors ( 1980; ). Pittsburgh pneumonia agent: direct isolation from human lung tissue. J Infect Dis 141, 727–732.[CrossRef]
    [Google Scholar]
  46. Segal, G., Purcell, M. & 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 U S A 95, 1669–1674.[CrossRef]
    [Google Scholar]
  47. Thacker, W. L., Benson, R. F., Schifman, R. B., Pugh, E., Steigerwalt, A. G., Mayberry, W. R., Brenner, D. J. & Wilkinson, H. W. ( 1989; ). Legionella tucsonensis sp. nov. isolated from a renal transplant recipient. J Clin Microbiol 27, 1831–1834.
    [Google Scholar]
  48. Vogel, J. P., Andrews, H. L., Wong, S. K. & Isberg, R. R. ( 1998; ). Conjugative transfer by the virulence system of Legionella pneumophila. Science 279, 873–876.[CrossRef]
    [Google Scholar]
  49. Watarai, M., Derre, I., Kirby, J., Growney, J. D., Dietrich, W. F. & 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.[CrossRef]
    [Google Scholar]
  50. Wilkinson, H. W., Thacker, W. L., Benson, R. F., Polt, S. S., Brookings, E., Mayberry, W. R., Brenner, D. J., Gilley, R. G. & Kirklin, J. K. ( 1987; ). Legionella birminghamensis sp. nov. isolated from a cardiac transplant recipient. J Clin Microbiol 25, 2120–2122.
    [Google Scholar]
  51. Zink, S. D., Pedersen, L., Cianciotto, N. P. & Abu Kwaik, Y. ( 2002; ). The Dot/Icm type iv secretion system of Legionella pneumophila is essential for the induction of apoptosis in human macrophages. Infect Immun 70, 1657–1663.[CrossRef]
    [Google Scholar]
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