Comparison of guinea pig and protozoan models for determining virulence of Legionella species

Fields, Barry S.; Barbaree, James M.; Shotts, Emmett B.; Feeley, James C.; Morrill, William E.; Sanden, Gary N.; Dykstra, Michael J.

doi:10.1128/iai.53.3.553-559.1986

Cited by 114 publications

(57 citation statements)

References 22 publications

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“…Amoeba serves as a reservoir for the amplification and dissemination of L. pneumophila and is considered the natural host for the bacteria. Moreover, growth of L. pneumophila in amoeba enhances its virulence (Fields et al, 1986). In contrast, it has been shown that L. longbeachaea is unable to replicate in Acanthamoeba castillanii and Hartmannella vermiformis but shows moderate growth in the protozoan Tetrahymena pyriformis (Wadowsky et al, 1991;Steele and McLennan, 1996;Neumeister et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

Early trafficking and intracellular replication of Legionella longbeachaea within an ER-derived late endosome-like phagosome

Asare¹,

Kwaik²

2007

Cell Microbiol

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SummaryLegionella pneumophila is the predominant cause of Legionnaires' disease in the USA and Europe in contrast to Legionella longbeachaea, which is the leading cause of the disease in Western Australia. The ability of L. pneumophila to replicate intracellularly is triggered at the post-exponential phase along with expression of other virulence traits, such as motility. We show that while motility of L. longbeachaea is triggered upon growth transition into postexponential phase, its ability to proliferate intracellularly is totally independent of the bacterial growth phase. Within macrophages, L. pneumophila replicates in a phagosome that excludes early and late endocytic markers and is surrounded by the rough endoplasmic reticulum (RER). In contrast, the L. longbeachaea phagosome colocalizes with the early endosomal marker early endosomal antigen 1 (EEA1) and the late endosomal markers lysosomal associated membrane glycoprotein 2 (LAMP-2) and mannose 6-phosphate receptor (M6PR), and is surrounded by the RER. The L. longbeachaea phagosome does not colocalize with the vacuolar ATPase (vATPase) proton pump, and the lysosomal luminal protease Cathepsin D, or the lysosomal tracer Texas red Ovalbumin (TROV). Intracellular proliferation of L. longbeachaea occurs in LAMP-2-positive phagosomes that are remodelled by the RER. Despite their distinct trafficking, both L. longbeachaea and L. pneumophila can replicate in communal phagosomes whose biogenesis is predominantly modulated by L. longbeachaea into LAMP-2-positive phagosomes. In addition, the L. pneumophila dotA mutant is rescued for intracellular replication if it co-inhabits the phagosome with L. longbeachaea. During late stages of infection, L. longbeachaea escape into the cytoplasm, prior to lysis of the macrophage, similar to L. pneumophila. We conclude that the L. longbeachaea phagosome matures to a non-acidified late endosome-like stage that is remodelled by the RER, indicating an idiosyncratic trafficking of L. longbeachaea compared with other intracellular pathogens, and a divergence in its intracellular lifestyle from L. pneumophila. In addition, re-routing biogenesis of the L. pneumophila phagosome into a late endosome controlled by L. longbeachaea has no effect on intracellular replication.

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Section: Introductionmentioning

confidence: 99%

Early trafficking and intracellular replication of Legionella longbeachaea within an ER-derived late endosome-like phagosome

Asare¹,

Kwaik²

2007

Cell Microbiol

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“…Grouping of Legionella species has been carried out by Neuminster et al [13] according to the bacterial doubling time in Mono Mac 6 cells and A. castellanii and by Fields et al [14] based on the ability to infect guinea pigs and growth in T. pyriformis. Their data are summarized in the right half of Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Neumeister et al [13] rami¢ed Legionella species into seven clusters according to the bacterial doubling time in Mono Mac 6 cells and Acanthamoeba castellanii. Fields et al [14] categorized Legionella species into four clusters based on their abilities to infect guinea pigs and to multiply within Tetrahymena pyriformis. These approaches are useful to elucidate both virulence factors and tactics for survival in the environment.…”

Section: Introductionmentioning

confidence: 99%

“…b A.B Lgn1, the Lgn1 r congenic mice between A/J and C57BL/6 ; Bcg r , the Bcg r congenic mice between C57BL/6 and DBA/2. c GP, in vivo test of virulence in guinea pigs by Field et al[14]; U937, infectivity for U937 cells by O'Connel et al[23]; MM6, infectivity for Mono Mac 6 cells by Neumeister et al[13]. d The strains were di¡erent from the strains used in this study.…”

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Grouping of 20 reference strains of Legionella species by the growth ability within mouse and guinea pig macrophages

Izu

1999

FEMS Immunology and Medical Microbiology

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20 Reference strains of Legionella species, isolated from human, were classified according to their ability to grow within thioglycolate-induced peritoneal macrophages of mice and guinea pigs. Inbred and congenic mice were used to study the effect of the natural resistance genes Lgn1 and Bcg that are expressed phenotypically in the mouse macrophages. The Lgn1 gene controlled the intracellular growth of Legionella pneumophila Philadelphia-1 and Legionella jordanis GIFU 12657, but the Bcg gene did not affect the intracellular growth of any organism examined. Based on these results and the growth ability in guinea pig macrophages, the 20 reference strains were divided into four groups. This grouping will help us to understand a variety of modes of interaction between Legionella species and macrophages.

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“…other than L. pneumophila have also been reported to be pathogenic to humans (3). These species proliferate as well as L. pneumophila in human monocytes (23), in macrophages of guinea pigs (4,5,12) and mice (12), in established cell lines (7,14,15,17), and in protozoa (4,5). In reference to intracellular entry and growth, there is diversity in Legionella spp., which can be described as follows.…”

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Morphological Variety of Intracellular Microcolonies of Legionella Species in Vero Cells

Ogawa

Takade

Miyamoto

et al. 2001

Microbiology and Immunology

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Intracellular microcolonies of six Legionella species growing in Vero cells showed distinctly varied morphologies. The varieties were observed by light microscopy of Gimenez-stained, Legionella-infected Vero cells and by electron microscopy (EM). Legionella pneumophila Philadelphia-l formed needle-shaped crystal-like microcolonies. Legionella bozemanii WIGA formed microcolonies like wool balls containing filamentous cells. In EM, these organisms proliferated in endosomes, which were adjacent to swollen rough endoplasmic reticula. Legionella oakridgensis OR-lO showed serpentine chains. Many mitochondria were observed around the microcolonies. Legionellajordanis BL-540 formed spherical moss-like microcolonies which were or were not surrounded by endoplasmic membranes. Legionella feeleii WO-44C spread throughout the cytoplasm without making clusters. Legionella dumojJii Tex-KL made big clusters that spread in the cytoplasm, a portion of which was outside the endosome membranes. These different morphologies imply diversity in modes of intracellular multiplication of Legionella spp. Key words: Legionella, Vero cells, Intracellular parasites, MorphologyForty three species of Legionella have been discovered and validated to date (http://www.bacterio.cicLfr/lI legionella.html). Surveillance studies have attributed 80 to 90% of Legionnaires' disease cases to Legionella pneumophila (1,3), and this species has been studied most frequently. However, Legionella spp. other than L. pneumophila have also been reported to be pathogenic to humans (3). These species proliferate as well as L. pneumophila in human monocytes (23), in macrophages of guinea pigs (4, 5, 12) and mice (12), in established cell lines (7,14,15,17), and in protozoa (4,5). In reference to intracellular entry and growth, there is diversity in Legionella spp., which can be described as follows. 1) L. pneumophila was phagocytosed by both coiling (11) and conventional (21) phagocytosis, and proliferated in ribosome-studded phagosomes (10), whereas L. micdadei was not (7,23). 2) L. anisa proliferated in a freeliving amoeba but could not proliferate in human monocytes (4). 3) L. dumoffii was internalized into Vero cells by receptor-mediated endocytosis, whereas L. pneumophila was internalized mainly via classical phagocytosis (15). 4) L. dumoffii could enter into and proliferate in the cytoplasm of epithelial cells of the respiratory tract, whereas L. pneumophila could not (14). 5) Among 20 reference strains of Legionella spp., only L. pneumophila and L. jordanis were affected by genetic control of the mouse macrophage resistance gene Lgnl (12). 6) Treatment of macrophages with 2-deoxy-D-glucose inhibited the intracellular growth of L. pneumophila (19) but not that of L. feeleii (Ogawa et al, unpublished observation). These results strongly suggest that modes of intracellular multiplication vary among Legionella spp.During the study to elucidate entry and growth in epitherial cell lines, we detected the morphological variety among the intracellular micro...

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Comparison of guinea pig and protozoan models for determining virulence of Legionella species

Cited by 114 publications

References 22 publications

Early trafficking and intracellular replication of Legionella longbeachaea within an ER-derived late endosome-like phagosome

Early trafficking and intracellular replication of Legionella longbeachaea within an ER-derived late endosome-like phagosome

Grouping of 20 reference strains of Legionella species by the growth ability within mouse and guinea pig macrophages

Morphological Variety of Intracellular Microcolonies of Legionella Species in Vero Cells

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