Identification of <i>Salmonella</i> functions critical for bacterial cell division within eukaryotic cells

Henry, Thomas; Portillo, Francisco García‐del; Gorvel, Jean‐Pierre

doi:10.1111/j.1365-2958.2005.04540.x

Cited by 41 publications

(39 citation statements)

References 76 publications

(90 reference statements)

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“…The comparison here of cells grown in human versus fetal bovine serum clearly demonstrates how different protocols can have profound impacts on the results. We also confirmed the findings of Henry et al (44), who showed that supplemental histidine is required for growth of the histidine auxotroph SL1344 in several cell types. To our knowledge, histidine is not routinely added during infection of murine macrophages or macrophage-like cell lines with SL1344.…”

Section: Discussionsupporting

confidence: 81%

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Replication of Salmonella enterica Serovar Typhimurium in Human Monocyte-Derived Macrophages

et al. 2015

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Salmonella enterica serovar Typhimurium is a common cause of food-borne gastrointestinal illness, but additionally it causes potentially fatal bacteremia in some immunocompromised patients. In mice, systemic spread and replication of the bacteria depend upon infection of and replication within macrophages, but replication in human macrophages is not widely reported or well studied. In order to assess the ability of Salmonella Typhimurium to replicate in human macrophages, we infected primary monocyte-derived macrophages (MDM) that had been differentiated under conditions known to generate different phenotypes. We found that replication in MDM depends greatly upon the phenotype of the cells, as M1-skewed macrophages did not allow replication, while M2a macrophages and macrophages differentiated with macrophage colony-stimulating factor (M-CSF) alone (termed M0) did. We describe how additional conditions that alter the macrophage phenotype or the gene expression of the bacteria affect the outcome of infection. In M0 MDM, the temporal expression of representative genes from Salmonella pathogenicity islands 1 and 2 (SPI1 and SPI2) and the importance of the PhoP/Q two-component regulatory system are similar to what has been shown in mouse macrophages. However, in contrast to mouse macrophages, where replication is SPI2 dependent, we observed early SPI2-independent replication in addition to later SPI2-dependent replication in M0 macrophages. Only SPI2-dependent replication was associated with death of the host cell at later time points. Altogether, our results reveal a very nuanced interaction between Salmonella and human macrophages.

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Section: Discussionsupporting

confidence: 81%

“…Although this does not appear to affect its virulence in mice, one study showed that intracellular replication is reduced in the absence of supplemental histidine in some cell types (44). In our hands, replication of SL1344 in M0 MDM was completely eliminated in the absence of supplemental histidine (Fig.…”

Section: Resultssupporting

confidence: 50%

Replication of Salmonella enterica Serovar Typhimurium in Human Monocyte-Derived Macrophages

et al. 2015

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“…For example, Salmonella enterica serovar Typhimurium growing in murine fibroblast cells (23) and contractile vacuoles of amoebae (11), S. enterica in macrophages (39), and uropathogenic E. coli in superficial bladder epithelial cells (26) are all filamentous. It is, however, pertinent to note that the filamentous cells of S. enterica serovar Typhimurium have distinct FtsZ bands at presumptive midcell locations, and a defect in the histidine biosynthetic pathway is correlated with the observed filamentation phenotype (16). The filamentation phenotype of M. tuberculosis during intracellular growth suggests that the pathogen's cell division process is delayed in response to infection, and this delay could be attributed to compromised function of FtsZ TB .…”

Section: Resultsmentioning

confidence: 99%

Mycobacterium tuberculosis Cells Growing in Macrophages Are Filamentous and Deficient in FtsZ Rings

et al. 2006

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FtsZ, a bacterial homolog of tubulin, forms a structural element called the FtsZ ring (Z ring) at the predivisional midcell site and sets up a scaffold for the assembly of other cell division proteins. The genetic aspects of FtsZ-catalyzed cell division and its assembly dynamics in Mycobacterium tuberculosis are unknown. Here, with an M. tuberculosis strain containing FtsZ TB tagged with green fluorescent protein as the sole source of FtsZ, we examined FtsZ structures under various growth conditions. We found that midcell Z rings are present in approximately 11% of actively growing cells, suggesting that the low frequency of Z rings is reflective of their slow growth rate. Next, we showed that SRI-3072, a reported FtsZ TB inhibitor, disrupted Z-ring assembly and inhibited cell division and growth of M. tuberculosis. We also showed that M. tuberculosis cells grown in macrophages are filamentous and that only a small fraction had midcell Z rings. The majority of filamentous cells contained nonring, spiral-like FtsZ structures along their entire length. The levels of FtsZ in bacteria grown in macrophages or in broth were comparable, suggesting that Z-ring formation at midcell sites was compromised during intracellular growth. Our results suggest that the intraphagosomal milieu alters the expression of M. tuberculosis genes affecting Z-ring formation and thereby cell division.Mycobacterium tuberculosis, the causative agent of tuberculosis, is an important infectious agent that globally causes more than three million new infections each year (8). Recent years have seen an increase in the number of M. tuberculosis strains that are resistant to one or more antituberculosis drugs, and this has highlighted the need for the development of a new generation of antimicrobial agents. One hallmark of the M. tuberculosis life cycle is that it exists in two metabolically distinct growth states: an active replicative state and a nonproliferative persistent state where the bacterium survives without any increase in the bacterial burden on the host. Physiological studies carried out by Wayne and colleagues indicate that M. tuberculosis cells in the hypoxiainduced nonreplicative persistent state are blocked at the cell division stage after completing DNA replication and undergo a round of cell division prior to initiation of a new round of DNA replication (40,41). This latter process is also referred to as reactivation. Development of antimycobacterial agents targeting the cell division process could potentially prevent the multiplication and subsequent proliferation of the pathogen in active, as well as reactivation, growth states.FtsZ, a bacterial homolog of tubulin, is a key player in cell division and is essential for initiation of this process (22, 32). FtsZ protein catalyzes the formation of distinct structures, referred to as FtsZ rings (Z rings), at the midcell site and sets up a scaffold for ordered assembly of other cell division proteins. The combined action of multiple cell division proteins results in septation (22,32)....

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“…For example, filamentous bacteria are commonly observed in freshwater environments and are resistant to grazing by protist predators (3,10,26). Uropathogenic E. coli filaments formed during a urinary tract infection are protected from phagocytosis by polymorphonuclear leukocytes (18), while survival of Mycobacterium tuberculosis and S. enterica serovar Typhimurium in macrophages has been associated with filamentous phenotypes (2,11,29). Even with a diversity of examples, it is unknown if filament formation is a programmed response or a consequence of unfavorable environmental conditions.…”

Section: Discussionmentioning

confidence: 99%

“…Whether this increased RecA expression is a consequence or cause of E40 filamentation or is associated with an SOS response is unknown. Henry et al (11) found filament formation by S. Typhimurium within human melanoma cells to be sulA independent and occurred after FtsZ ring assembly. It resulted from a hisG mutation and required the activity of HisFH, a heterodimeric enzyme in the histidine biosynthetic pathway.…”

Section: Discussionmentioning

confidence: 99%

Survival and Virulence of Salmonella enterica Serovar Enteritidis Filaments Induced by Reduced Water Activity

Stackhouse

Faith

Kaspar

et al. 2012

Appl Environ Microbiol

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ABSTRACTSalmonella entericaserovar Enteritidis strain E40 filaments were developed under conditions of a reduced water activity (aw) of 0.95 in tryptic soy broth (TSB) or tryptic soy agar (TSA) supplemented with 8% or 7% NaCl, respectively. Filament formation was accompanied by an increase of biomass without an increase in CFU and was affected by incubation temperature and the physical milieu. The greatest amount of filaments was recovered from TSA with 7% NaCl and incubation at 30°C. Within 2 h of transfer to fresh TSB, filaments started to septate into normal-sized cells, resulting in a rapid increase in CFU.S. Enteritidis E40 filaments were not more tolerant of low- or high-temperature stresses than nonfilamented control cells. However, there was greater survival of filaments in 10% bile salts after 24 to 48 h of incubation, during pH 2.0 acid challenge for 10 min, and under desiccation on stainless steel surfaces at 25°C and 75.5% relative humidity for 7 days.S. Enteritidis E40 filaments invaded and multiplied within Caco-2 human intestinal epithelial cells to a similar degree as control cells when a comparable CFU of filaments and control cells was used.S. Enteritidis E40 filaments established a successful infection in mice via intragastric inoculation. The filaments colonized the gastrointestinal tract and disseminated to the spleen and liver at levels comparable to those attained by control cells, even when animals were inoculated with 10- to 100-fold fewer CFU. To our knowledge this is the first demonstration of virulence of stress-inducedSalmonellafilamentsin vitroandin vivo. Formation of filaments bySalmonellain food products and food processing environments is significant to food safety, because detection and quantitation of the pathogen may be compromised. The finding that these filaments are virulent further enhances their potential public health impact.

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Identification of Salmonella functions critical for bacterial cell division within eukaryotic cells

Cited by 41 publications

References 76 publications

Replication of Salmonella enterica Serovar Typhimurium in Human Monocyte-Derived Macrophages

Replication of Salmonella enterica Serovar Typhimurium in Human Monocyte-Derived Macrophages

Mycobacterium tuberculosis Cells Growing in Macrophages Are Filamentous and Deficient in FtsZ Rings

Survival and Virulence of Salmonella enterica Serovar Enteritidis Filaments Induced by Reduced Water Activity

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