The role of Legionella pneumophila-infected Hartmannella vermiformis as an infectious particle in a murine model of Legionnaire's disease

Brieland, Joan K.; Fantone, Joseph C.; Remick, Daniel G.; Legendre, Maureen; McClain, Mark S.; Engleberg, N. Cary

doi:10.1128/iai.65.12.5330-5333.1997

Cited by 97 publications

(47 citation statements)

References 26 publications

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“…Fourthly, infection of amoebae by legionellae may contribute to its virulence against human cells. This is supported by the finding that L. pneumophila grown within amoebae are severalfold more invasive for macrophages and for intrapulmonary replication in mice (Brieland et al, 1997) compared with bacteria From protozoa to mammalian cells 253 grown on agar plates . Furthermore, after replication within amoebae, L. pneumophila becomes 1000-fold more resistant to antimicrobial compounds (Barker and Brown, 1995).…”

Section: Legionellae: Ecology and Transmissionmentioning

confidence: 81%

“…Secondly, Acanthamoeba species are capable of excreting L. pneumophila-filled vesicles, which may act as infectious particles upon inhalation (Berk et al, 1998). Thirdly, amoebae themselves harbouring large quantities of L. pneumophila may be inhaled and cause disease (Brieland et al, 1997). Figure 2 depicts the environmental interaction between legionellae and protozoa and its transmission to humans.…”

Section: Legionellae: Ecology and Transmissionmentioning

confidence: 99%

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From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens

Harb¹,

Gao²,

Kwaik³

2000

Environmental Microbiology

201

166

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It is becoming apparent that several intracellular bacterial pathogens of humans can also survive within protozoa. This interaction with protozoa may protect these pathogens from harsh conditions in the extracellular environment and enhance their infectivity in mammals. This relationship has been clearly established in the case of the interaction between Legionella pneumophila and its protozoan hosts. In addition, the adaptation of bacterial pathogens to the intracellular life within the primitive eukaryotic protozoa may have provided them with the means to infect the more evolved mammalian cells. This is evident from the existence of several similarities, at both the phenotypic and the molecular levels, between the infection of mammalian and protozoan cells by L. pneumophila. Thus, protozoa appear to play a central role in the transition of bacteria from the environment to mammals. In essence, protozoa may be viewed as a ‘biological gym’, within which intracellular bacterial pathogens train for their encounters with the more evolved mammalian cells. Thus, intracellular bacterial pathogens have benefited from the structural and biochemical conservation of cellular processes in eukaryotes. The interaction of intracellular bacterial pathogens and protozoa highlights this conservation and may constitute a simplified model for the study of these pathogens and the evolution of cellular processes in eukaryotes. Furthermore, in addition to being environmental reservoirs for known intracellular pathogens of humans and animals, protozoa may be sources of emerging pathogenic bacteria. It is thus critical to re‐examine the relationship between bacteria and protozoa to further our understanding of current human bacterial pathogenesis and, possibly, to predict the appearance of emerging pathogens.

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Section: Legionellae: Ecology and Transmissionmentioning

confidence: 81%

Section: Legionellae: Ecology and Transmissionmentioning

confidence: 99%

From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens

Harb¹,

Gao²,

Kwaik³

2000

Environmental Microbiology

201

166

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“…Results are the mean and standard deviation of three independent experiments. (Brieland et al, 1997;reviewed by Harb et al, 2000). Infected protozoa harbour many hundreds of organisms and could release them inside alveoli.…”

Section: Discussionmentioning

confidence: 99%

Icm/Dot‐dependent upregulation of phagocytosis by Legionella pneumophila

Hilbi

Segal

Shuman³

2001

Molecular Microbiology

187

110

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SummaryLegionella pneumophila is the causative agent of Legionnaires' disease, a severe pneumonia. Dependent on the icm/dot loci, L. pneumophila survives and replicates in macrophages and amoebae within a specialized phagosome that does not fuse with lysosomes. Here, we report that phagocytosis of wild-type L. pneumophila is more efficient than uptake of icm/dot mutants. Compared with the wild-type strain JR32, about 10 times fewer icm/dot mutant bacteria were recovered from HL-60 macrophages in a gentamicin protection assay. The defect in phagocytosis of the mutants could be complemented by supplying the corresponding genes on a plasmid. Using fluorescence microscopy and green fluorescent protein (GFP)-expressing strains, 10 -20 times fewer icm/dot mutant bacteria were found to be internalized by HL-60 cells and human monocytederived macrophages (HMMF). Compared with icm/dot mutants, wild-type L. pneumophila infected two to three times more macrophages and yielded a population of highly infected host cells (15-70 bacteria per macrophage) that was not observed with icm/dot mutant strains. Wild-type and icmT mutant bacteria were found to adhere similarly and compete for binding to HMMF. In addition, wild-type L. pneumophila was also phagocytosed more efficiently by Acanthamoeba castellanii, indicating that the process is independent of adherence receptor(s). Wild-type L. pneumophila enhanced phagocytosis of an icmT mutant strain in a synchronous co-infection, suggesting that increased phagocytosis results from (a) secreted effector(s) acting in trans.

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“…By using various model systems it was shown that the interaction of Legionella and protozoa contributes to the infection process itself. After intracellular replication within protozoa L. pneumophila exhibits a higher stress resistance [3,29]. Mice inoculated with Legionella and Hartmannella develop more severe symptoms than those infected with either the bacterium or the amoeba alone [29].…”

Section: Legionella^protozoa Interactionsmentioning

confidence: 99%

“…After intracellular replication within protozoa L. pneumophila exhibits a higher stress resistance [3,29]. Mice inoculated with Legionella and Hartmannella develop more severe symptoms than those infected with either the bacterium or the amoeba alone [29]. However, the underlying mechanisms of this phenomenon are not yet understood.…”

Section: Legionella^protozoa Interactionsmentioning

confidence: 99%

Legionella pneumophila: an aquatic microbe goes astray

Steinert

2002

FEMS Microbiology Reviews

117

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Legionella pneumophila is naturally found in fresh water were the bacteria parasitize within protozoa. It also survives planctonically in water or biofilms. Upon aerosol formation via man-made water systems, L. pneumophila can enter the human lung and cause a severe form of pneumonia, called Legionnaires' disease. The pathogenesis of Legionnaires' disease is largely due to the ability of L. pneumophila to invade and grow within macrophages. An important characteristic of the intracellular survival strategy is the replication within the host vacuole that does not fuse with endosomes or lysosomes. In recent times a great number of bacterial virulence factors which affect growth of L. pneumophila in both macrophages and protozoa have been identified. The ongoing Legionella genome project and the use of genetically tractable surrogate hosts are expected to significantly contribute to the understanding of bacterium-host interactions and the regulation of virulence traits during the infection cycle. Since person-to-person transmission of legionellosis has never been observed, the measures for disease prevention have concentrated on eliminating the pathogen from water supplies. In this respect detection and analysis of Legionella in complex environmental consortia become increasingly important. With the availability of new molecular tools this area of applied research has gained new momentum.

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The role of Legionella pneumophila-infected Hartmannella vermiformis as an infectious particle in a murine model of Legionnaire's disease

Cited by 97 publications

References 26 publications

From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens

From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens

Icm/Dot‐dependent upregulation of phagocytosis by Legionella pneumophila

Legionella pneumophila: an aquatic microbe goes astray

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