Flagella-mediated bacterial motility accelerates but is not required for Salmonella serotype Enteritidis invasion of differentiated Caco-2 cells

Asten, Fons J. A. M. van; Hendriks, Henno; Koninkx, J. F. J. G.; Dijk, J. E. van

doi:10.1016/j.ijmm.2004.07.012

Cited by 48 publications

(39 citation statements)

References 12 publications

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“…Invasion in cultured epithelial cells is routinely used as a measure of pathogenicity of Salmonella isolates (DibbFuller et al, 1999;van Asten et al, 2000van Asten et al, , 2004. Fewer studies have been conducted to determine differences in invasiveness of field isolates of S. Enteritidis (Pan et al, 2009;Pang et al, 2006;Solano et al, 1998).…”

Section: Discussionmentioning

confidence: 99%

“…These data support our hypothesis that not all isolates of S. Enteritidis recovered from poultry are equally pathogenic. Although the molecular mechanisms underlying the differences in the virulence of S. Enteritidis remain poorly understood, both flagella and TTSS proteins encoded by virulence-associated genes located on SPI-1 and SPI-2 are known to play a major role in the pathogenesis of S. Enteritidis infection in cultured epithelial cells and in chicken and mouse challenge models (Allen-Vercoe & Cogan et al, 2004;Dibb-Fuller et al, 1999;Methner & Barrow, 1997;van Asten et al, 2000van Asten et al, , 2004Yim et al, 2010). We observed that isolates with low invasiveness also had impaired secretion of SPI-1-encoded TTSS proteins (SipA and SipD) or motility-associated proteins (FlgK, FljB and FlgL) encoded by flagellar TTSS (Fig.…”

Section: Discussionmentioning

confidence: 99%

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Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system

et al. 2011

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Salmonella enterica serovar Enteritidis (S. Enteritidis) is a major cause of food-borne gastroenteritis in humans worldwide. Poultry and poultry products are considered the major vehicles of transmission to humans. Using cell invasiveness as a surrogate marker for pathogenicity, we tested the invasiveness of 53 poultry-associated isolates of S. Enteritidis in a well-differentiated intestinal epithelial cell model (Caco-2). The method allowed classification of the isolates into low (n57), medium (n518) and high (n530) invasiveness categories. Cell invasiveness of the isolates did not correlate with the presence of the virulence-associated gene spvB or the ability of the isolates to form biofilms. Testing of representative isolates with high and low invasiveness in a mouse model revealed that the former were more invasive in vivo and caused more and earlier mortalities, whereas the latter were significantly less invasive in vivo, causing few or no mortalities. Further characterization of representative isolates with low and high invasiveness showed that most of the isolates with low invasiveness had impaired motility and impaired secretion of either flagella-associated proteins (FlgK, FljB and FlgL) or type III secretion system (TTSS)-secreted proteins (SipA and SipD) encoded on Salmonella pathogenicity island-1. In addition, isolates with low invasiveness had impaired ability to invade and/or survive within chicken macrophages. These data suggest that not all isolates of S. Enteritidis recovered from poultry may be equally pathogenic, and that the pathogenicity of S. Enteritidis isolates is associated, in part, with both motility and secretion of TTSS effector proteins. INTRODUCTIONSalmonella enterica serovar Enteritidis (S. Enteritidis) is the leading cause of food-borne salmonellosis (WHO, 2008). S. Enteritidis-induced salmonellosis in humans is characterized by diarrhoea, fever, headache, abdominal pain, nausea and vomiting (CDC, 2007). S. Enteritidis is also increasingly reported from cases of invasive and extra-intestinal infections such as septicaemia, arthritis, endocarditis, meningitis and urinary tract infections (Ghosh & Vogt, 2006; Gordon et al., 2008;Katsenos et al., 2008; Kobayashi et al., 2009;Morpeth et al., 2009;Mutlu et al., 2009;Tena et al., 2007). Between 1990 and 2001, the US state and territorial health departments reported 677 S. Enteritidis outbreaks, which accounted for 23 366 illnesses, 1988 hospitalizations and 33 deaths (CDC, 2003). In 2006, countries within the European Union reported 1729 outbreaks caused by S. Enteritidis leading to 13 853 illnesses, 2714 hospitalizations and 14 deaths (EFSA, 2007). The Health Protection Agency of the UK reported 4194 cases of foodborne S. Enteritidis infection in (HPA, 2008. Poultry is considered the single largest reservoir of S. Enteritidis and most risk attribution studies have identified poultry and poultry products as the major source of human infection. S. Enteritidis is passed to humans mainly via handling and consumption of contaminated po...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system

et al. 2011

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“…T3SS-2 plays an important role in intracellular survival, and replication of Salmonella in the vacuole of the host cells, and is therefore essential for systemic dissemination of the bacteria (Abrahams & Hensel, 2006). The flagella share a similar structural design with T3SS (Macnab, 2004), and confer motility to Salmonella, and thus contribute to bacterial interaction with the intestinal epithelium (van Asten et al, 2004). Salmonellae are not the only bacteria in which a role for BamB in virulence has been demonstrated; a defect in invasion ability has been observed in a bamB mutant of the adherent invasive E. coli LF82 strain (Rolhion et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Investigation of the role of the BAM complex and SurA chaperone in outer-membrane protein biogenesis and type III secretion system expression in Salmonella

et al. 2009

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In Escherichia coli, the assembly of outer-membrane proteins (OMP) requires the BAM complex and periplasmic chaperones, such as SurA or DegP. Previous work has suggested a potential link between OMP assembly and expression of the genes encoding type-III secretion systems. In order to test this hypothesis, we studied the role of the different lipoproteins of the BAM complex (i.e. BamB, BamC, BamD and BamE), and the periplasmic chaperones SurA and DegP, in these two phenotypes in Salmonella. Analysis of the corresponding deletion mutants showed that, as previously described with the DbamB mutant, BamD, SurA and, to a lesser extent, BamE play a role in outer-membrane biogenesis in Salmonella Enteritidis, while the membrane was not notably disturbed in DbamC and DdegP mutants. Interestingly, we found that BamD is not essential in Salmonella, unlike its homologues in Escherichia coli and Neisseria gonorrhoeae. In contrast, BamD was the only protein required for full expression of T3SS-1 and flagella, as demonstrated by transcriptional analysis of the genes involved in the biosynthesis of these T3SSs. In line with this finding, bamD mutants showed a reduced secretion of effector proteins by these T3SSs, and a reduced ability to invade HT-29 cells. As DsurA and DbamE mutants had lower levels of OMPs in their outer membrane, but showed no alteration in T3SS-1 and flagella expression, these results demonstrate the absence of a systematic link between an OMP assembly defect and the downregulation of T3SSs in Salmonella; therefore, this link appears to be related to a more specific mechanism that involves at least BamB and BamD.

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“…Mutation of the fliC gene together with motA mutation in S. Enteritidis impaired bacterial invasion severely but not adhesion (11). A comparison of several naturally occurring motA mutants of S. Enteritidis with nonflagellated mutant strains (fliC mutants) determined that they exhibit less invasiveness to Caco-2 cells (24).…”

Section: Figmentioning

confidence: 99%

“…Similarly, a nonflagellated mutant of S. Enteritidis was 50-fold less invasive to Caco-2 cell lines, even if the adhesion rate was similar to that of a flagellated strain (10). However, comparison of flagellar motor mutants and nonflagellated mutants of S. Enteritidis to the wild-type strain suggested that flagellin-mediated motility accelerates the invasion process rather than being essential (11).…”

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confidence: 98%

Salmonella enterica Serovar Kentucky Flagella Are Required for Broiler Skin Adhesion and Caco-2 Cell Invasion

Salehi

Howe

Lawrence

et al. 2017

Appl Environ Microbiol

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Nontyphoidal Salmonella strains are the main source of pathogenic bacterial contamination in the poultry industry. Recently, Salmonella enterica serovar Kentucky has been recognized as the most prominent serovar on carcasses in poultry-processing plants. Previous studies showed that flagella are one of the main factors that contribute to bacterial attachment to broiler skin. However, the precise role of flagella and the mechanism of attachment are unknown. There are two different flagellar subunits (fliC and fljB) expressed alternatively in Salmonella enterica serovars using phase variation. Here, by making deletions in genes encoding flagellar structural subunits (flgK, fliC, and fljB), and flagellar motor (motA), we were able to differentiate the role of flagella and their rotary motion in the colonization of broiler skin and cellular attachment. Utilizing a broiler skin assay, we demonstrated that the presence of FliC is necessary for attachment to broiler skin. Expression of the alternative flagellar subunit FljB enables Salmonella motility, but this subunit is unable to mediate tight attachment. Deletion of the flgK gene prevents proper flagellar assembly, making Salmonella significantly less adherent to broiler skin than the wild type. S. Kentucky with deletions in all three structural genes, fliC, fljB, and flgK, as well as a flagellar motor mutant (motA), exhibited less adhesion and invasion of Caco-2 cells, while an fljB mutant was as adherent and invasive as the wild-type strain.IMPORTANCE In this work, we answered clearly the role of flagella in S. Kentucky attachment to the chicken skin and Caco-2 cells. We demonstrated that the presence of FliC is necessary for attachment to broiler skin. Expression of the alternative flagellar subunit FljB enables Salmonella motility, but this subunit is unable to mediate strong attachment. Deletion of the flgK gene prevents proper flagellar assembly, making Salmonella significantly less adherent to broiler skin than the wild type. S. Kentucky with deletions in all three structural genes, fliC, fljB, and flgK, as well as a flagellar motor mutant (motA), exhibited less adhesion and invasion of Caco-2 cells, while an fljB mutant was as adherent and invasive as the wild-type strain. We expect these results will contribute to the understanding of the mechanisms of Salmonella attachment to food products.

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Flagella-mediated bacterial motility accelerates but is not required for Salmonella serotype Enteritidis invasion of differentiated Caco-2 cells

Cited by 48 publications

References 12 publications

Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system

Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system

Investigation of the role of the BAM complex and SurA chaperone in outer-membrane protein biogenesis and type III secretion system expression in Salmonella

Salmonella enterica Serovar Kentucky Flagella Are Required for Broiler Skin Adhesion and Caco-2 Cell Invasion

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