Salmonella enterica Remodels the Host Cell Endosomal System for Efficient Intravacuolar Nutrition

Liss, Viktoria; Swart, A. Leoni; Kehl, Alexander; Hermanns, Natascha; Zhang, Yuying; Chikkaballi, Deepak; Böhles, Nathalie; Deiwick, Jörg; Hensel, Michael

doi:10.1016/j.chom.2017.02.005

Cited by 105 publications

(135 citation statements)

References 35 publications

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“…However, it is still unknown whether Salmonella-induced tubules play a role in pathogenesis. A recent study by Liss et al (2017) showed that Salmonella-induced tubules and SCVs form an extensive vacuolar continuum that allows rapid access of Salmonella to nutrients, thus promoting intracellular replication. These facts have raised doubt about the physiological role of tubules.…”

Section: Introductionmentioning

confidence: 99%

Contribution of bacterial effectors and host proteins to the composition and function ofSalmonella-induced tubules

Moest

Zhao

et al. 2018

Cellular Microbiology

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Cells infected with Salmonella are characterised by the appearance of membrane tubular structures that stretch from the bacterial vacuole. The formation of these tubules requires the translocation of Salmonella effector proteins within the infected cell. Different types of Salmonella-induced tubules with varying host protein compositions have been identified. This variability probably reflects the ability of these tubules to interact with different host compartments. Membrane tubules decorated with effector proteins but essentially devoid of host proteins and named LAMP1-negative (LNT) were observed. LNTs wrap around LAMP1-positive vesicles and may promote recruitment of lysosomal glycoproteins to bacterial vacuole and the formation of a replication niche. We conducted a biochemical and functional characterisation of LNTs. We show that the effector proteins SseF and SseG are necessary for their formation. The absence of these tubules is associated with decreased recruitment of LAMP1 to SCVs, decreased intracellular replication of Salmonella, and decreased virulence in mice. We found that the process leading to the recruitment of lysosomal glycoproteins to tubules involves the C-terminal domain of the effector protein SifA and the GTPase Arl8b. Overall, these data suggest that Salmonella-induced tubules promote the establishment of the replication niche by promoting recruitment of host proteins to the bacterial vacuole.

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Section: Introductionmentioning

confidence: 99%

Contribution of bacterial effectors and host proteins to the composition and function ofSalmonella-induced tubules

Moest

Zhao

et al. 2018

Cellular Microbiology

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“…Thus, the precise activation of SPI-2 genes within macrophages is essential for S. Typhimurium virulence. In addition to contributing to the SCV formation, SPI-2 also plays an important role in acquisition of nutrition and bacterial replication within macrophages (Figueira, Watson, Holden, & Helaine, 2013;Liss et al, 2017). In addition to contributing to the SCV formation, SPI-2 also plays an important role in acquisition of nutrition and bacterial replication within macrophages (Figueira, Watson, Holden, & Helaine, 2013;Liss et al, 2017).…”

mentioning

confidence: 99%

PagR mediates the precise regulation of Salmonella pathogenicity island 2 gene expression in response to magnesium and phosphate signals in Salmonella Typhimurium

Jiang

Wang

et al. 2019

Cellular Microbiology

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To establish systemic infections, Salmonella enterica serovar Typhimurium (S. Typhimurium) requires Salmonella pathogenicity island 2 (SPI-2) to survive and replicate within macrophages. High expression of many SPI-2 genes during the entire intracellular growth period within macrophages is essential, as it contributes to the formation of Salmonella-containing vacuole and bacterial replication. However, the regulatory mechanisms underlying the sustained induction of SPI-2 within macrophages are not fully understood. Here, we revealed a time-dependent regulation of SPI-2 expression mediated by a novel regulator PagR (STM2345) in response to the low Mg 2+ and low phosphate (P i ) signals, which ensured the high induction of SPI-2 during the entire intramacrophage growth period. Deletion of pagR results in reduced bacterial replication in macrophages and attenuation of systemic virulence in mice. The effects of pagR on virulence are dependent on upregulating the expression of slyA, a regulator of SPI-2.At the early (0-4 hr) and later (after 4 hr) stage post-infection of macrophages, pagR is induced by the low P i via PhoB/R two-component systems and low Mg 2+ via PhoP/Q systems, respectively. Collectively, our findings revealed that the PagR-mediated regulatory mechanism contributes to the precise and sustained activation of SPI-2 genes within macrophages, which is essential for S. Typhimurium systemic virulence.

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“…Typhimurium rapid access to endocytosed materials. Liss et al (2017) also demonstrated that intravacuolar S . Typhimurium connected to the SIF network are significantly more metabolically active than S .…”

Section: Sifs Link Salmonella To the Endocytic And Exocytic Pathwaysmentioning

confidence: 91%

“…Typhimurium can gain access to endocytosed nutrients (Popp et al, 2015). It was recently reported that membrane components and luminal content of the SIF network are both connected to, and interchanging with, the SCV in a SPI2-T3SS-dependent manner (Krieger et al, 2014; Liss et al, 2017), allowing S . Typhimurium rapid access to endocytosed materials.…”

Section: Sifs Link Salmonella To the Endocytic And Exocytic Pathwaysmentioning

confidence: 99%

What the SIF Is Happening—The Role of Intracellular Salmonella-Induced Filaments

Knuff

Finlay

2017

Front. Cell. Infect. Microbiol.

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A common strategy among intracellular bacterial pathogens is to enter into a vacuolar environment upon host cell invasion. One such pathogen, Salmonella enterica, resides within the Salmonella-containing vacuole (SCV) inside epithelial cells and macrophages. Salmonella hijacks the host endosomal system to establish this unique intracellular replicative niche, forming a highly complex and dynamic network of Salmonella-induced filaments (SIFs). SIFs radiate outwards from the SCV upon onset of bacterial replication. SIF biogenesis is dependent on the activity of bacterial effector proteins secreted by the Salmonella-pathogenicity island-2 (SPI-2) encoded type III secretion system. While the presence of SIFs has been known for almost 25 years, their precise role during infection remains elusive. This review summarizes our current knowledge of SCV maturation and SIF biogenesis, and recent advances in our understanding of the role of SIFs inside cells.

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Salmonella enterica Remodels the Host Cell Endosomal System for Efficient Intravacuolar Nutrition

Cited by 105 publications

References 35 publications

Contribution of bacterial effectors and host proteins to the composition and function ofSalmonella-induced tubules

Contribution of bacterial effectors and host proteins to the composition and function ofSalmonella-induced tubules

PagR mediates the precise regulation of Salmonella pathogenicity island 2 gene expression in response to magnesium and phosphate signals in Salmonella Typhimurium

What the SIF Is Happening—The Role of Intracellular Salmonella-Induced Filaments

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