Impacts of Salmonella enterica Serovar Typhimurium and Its speG Gene on the Transcriptomes of In Vitro M Cells and Caco-2 Cells

Wang, Ke Chuan; Huang, Chih Hung; Huang, Ching Jou; Fang, Shiuh-Bin

doi:10.1371/journal.pone.0153444

Cited by 11 publications

(11 citation statements)

References 59 publications

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“…the putative effector protein STY2875 and the putative type 1 secretion apparatus encoded by STY2876, STY2877 and STY2878) contribute to adherence. When we tested the adherence in Caco-2 cells, other epithelial cell lines also worked with S. enterica (Wang et al, 2016), and we observed that S. Typhi DSTY2875 also presented attachment defects when previously cultured in LB pH 7.0 400 mM NaCl (Fig. 4c), supporting our conclusions.…”

Section: Spi-9 Contributes To Adherence To Epithelial Cell Linessupporting

confidence: 85%

SPI-9 of Salmonella enterica serovar Typhi is constituted by an operon positively regulated by RpoS and contributes to adherence to epithelial cells in culture

et al. 2016

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The genomic island 9 (SPI-9) from Salmonella enterica serovar Typhi (S. Typhi) carries three ORFs (STY2876, STY2877, STY2878) presenting 98 % identity with a type 1 secretory apparatus (T1SS), and a single ORF (STY2875) similar to a large RTX-like protein exhibiting repeated Ig domains. BapA, the Salmonella enterica serovar Enteritidis orthologous to S. Typhi STY2875, has been associated with biofilm formation, and is described as a virulence factor in mice. Preliminary in silico analyses revealed that S. Typhi STY2875 ORF has a 600 bp deletion compared with S. Enteritidis bapA, suggesting that S. Typhi STY2875 might be non-functional. At present, SPI-9 has not been studied in S. Typhi. We found that the genes constituting SPI-9 are arranged in an operon whose promoter was up-regulated in high osmolarity and low pH in a RpoS-dependent manner. All the proteins encoded by S. Typhi SPI-9 were located at the membrane fraction, consistent with their putative role as T1SS. Furthermore, SPI-9 contributed to adherence of S. Typhi to epithelial cells when bacteria were grown under high osmolarity or low pH. Under the test conditions, S. Typhi SPI-9 did not participate in biofilm formation. SPI-9 is functional in S. Typhi and encodes an adhesin induced under conditions normally found in the intestine, such as high osmolarity. Hence, this is an example of a locus that might be designated a pseudogene by computational approaches but not by direct biological assays.

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Section: Spi-9 Contributes To Adherence To Epithelial Cell Linessupporting

confidence: 85%

SPI-9 of Salmonella enterica serovar Typhi is constituted by an operon positively regulated by RpoS and contributes to adherence to epithelial cells in culture

et al. 2016

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“…The mutants Δ fliC and Δ spaS were used as controls. Δ speG and Δ fliC were constructed using the lambda red recombinase-mediated integration of linear polymerase chain reaction (PCR) amplicons to replace the target gene with a kanamycin resistance gene cassette, as previously reported (Gust et al, 2003 ; Wang et al, 2016a , b ). For generating the speG -complemented S .…”

Section: Methodsmentioning

confidence: 99%

“…The speG mutant of S . Typhimurium is a non-replicating strain in human cells and is thus a candidate vaccine vector for interacting with intestinal epithelial cells (Wang et al, 2016b ). We used RNA microarrays to determine whether S .…”

Section: Introductionmentioning

confidence: 99%

“…We used RNA microarrays to determine whether S . Typhimurium and speG affect the transcriptomes of two human intestinal epithelial cells and identified speG -regulated genes, including KYL4, SCTR, IL6, TNF , and CELF4 in Caco-2 cells and JUN, KLF6 , and KCTD11 in in vitro M cells, which are specialized intestinal epithelial cells conferring host immunity (Wang et al, 2016b ). However, it is unclear whether speG regulates the expression of other genes in Salmonella before and after bacterial invasion in human intestinal epithelium.…”

Section: Introductionmentioning

confidence: 99%

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speG Is Required for Intracellular Replication of Salmonella in Various Human Cells and Affects Its Polyamine Metabolism and Global Transcriptomes

Fang

Huang

et al. 2017

Front. Microbiol.

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The speG gene has been reported to regulate polyamine metabolism in Escherichia coli and Shigella, but its role in Salmonella remains unknown. Our preliminary studies have revealed that speG widely affects the transcriptomes of infected in vitro M and Caco-2 cells and that it is required for the intracellular replication of Salmonella enterica serovar Typhimurium (S. Typhimurium) in HeLa cells. In this study, we demonstrated that speG plays a time-dependent and cell type-independent role in the intracellular replication of S. Typhimurium. Moreover, high-performance liquid chromatography (HPLC) of four major polyamines demonstrated putrescine, spermine, and cadaverine as the leading polyamines in S. Typhimurium. The deletion of speG significantly increased the levels of the three polyamines in intracellular S. Typhimurium, suggesting the inhibitory effect of speG on the biosynthesis of these polyamines. The deletion of speG was associated with elevated levels of these polyamines in the attenuated intracellular replication of S. Typhimurium in host cells. This result was subsequently validated by the dose-dependent suppression of intracellular proliferation after the addition of the polyamines. Furthermore, our RNA transcriptome analysis of S. Typhimurium SL1344 and its speG mutant outside and inside Caco-2 cells revealed that speG regulates the genes associated with flagellar biosynthesis, fimbrial expression, and functions of types III and I secretion systems. speG also affects the expression of genes that have been rarely reported to correlate with polyamine metabolism in Salmonella, including those associated with the periplasmic nitrate reductase system, glucarate metabolism, the phosphotransferase system, cytochromes, and the succinate reductase complex in S. Typhimurium in the mid-log growth phase, as well as those in the ilv–leu and histidine biosynthesis operons of intracellular S. Typhimurium after invasion in Caco-2 cells. In the present study, we characterized the phenotypes and transcriptome effects of speG in S. Typhimurium and reviewed the relevant literature to facilitate a more comprehensive understanding of the potential role of speG in the polyamine metabolism and virulence regulation of Salmonella.

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“…Paradoxically, Salmonella exploit M cells as a route for the host invasion. Both S. Typhi [160] and S. Typhimurium [161] selectively target and invade M cells through SPI-1.…”

Section: Escape Of Innate Immune Systemmentioning

confidence: 99%

Salmonella Virulence and Immune Escape

et al. 2020

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Salmonella genus represents the most common foodborne pathogens causing morbidity, mortality, and burden of disease in all regions of the world. The introduction of antimicrobial agents and Salmonella-specific phages has been considered as an effective intervention strategy to reduce Salmonella contamination. However, data from the United States, European countries, and low- and middle-income countries indicate that Salmonella cases are still a commonly encountered cause of bacterial foodborne diseases globally. The control programs have not been successful and even led to the emergence of some multidrug-resistant Salmonella strains. It is known that the host immune system is able to effectively prevent microbial invasion and eliminate microorganisms. However, Salmonella has evolved mechanisms of resisting host physical barriers and inhibiting subsequent activation of immune response through their virulence factors. There has been a high interest in understanding how Salmonella interacts with the host. Therefore, in the present review, we characterize the functions of Salmonella virulence genes and particularly focus on the mechanisms of immune escape in light of evidence from the emerging mainstream literature.

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Impacts of Salmonella enterica Serovar Typhimurium and Its speG Gene on the Transcriptomes of In Vitro M Cells and Caco-2 Cells

Cited by 11 publications

References 59 publications

SPI-9 of Salmonella enterica serovar Typhi is constituted by an operon positively regulated by RpoS and contributes to adherence to epithelial cells in culture

SPI-9 of Salmonella enterica serovar Typhi is constituted by an operon positively regulated by RpoS and contributes to adherence to epithelial cells in culture

speG Is Required for Intracellular Replication of Salmonella in Various Human Cells and Affects Its Polyamine Metabolism and Global Transcriptomes

Salmonella Virulence and Immune Escape

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