<i>Salmonella enterica</i>
            Serovar Enteritidis Pathogenicity Island 1 Is Not Essential for but Facilitates Rapid Systemic Spread in Chickens

Desin, Taseen S.; Lam, Po-King S.; Koch, Birgit; Mickael, Claudia; Berberov, Emil M.; Wisner, Amanda L. S.; Townsend, H. G. G.; Potter, Andrew; Köster, Wolfgang

doi:10.1128/iai.00039-09

Cited by 49 publications

(65 citation statements)

References 57 publications

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“…Previous studies have also revealed that genes encoded by SPI-1 TTSS are involved in intestinal invasion whereas genes encoded on SPI-2 are required for systemic infection and survival within macrophages (Desin et al, 2009;Dieye et al, 2009;Jones et al, 2007;Li et al, 2009;Rychlík et al, 2009;Wisner et al, 2010). Mutations in the genes encoding secretory effector proteins or genes that regulate their expression lead to virulence attenuation in S. Enteritidis (Amy et al, 2004;Fardini et al, 2007;Parker & GuardPetter, 2001).…”

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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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%

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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“…For example, a Salmonella Senftenberg strain lacking T3SS-1 was isolated from a human clinical case and shown to be able to induce enterocolitis in a mouse model (Hu et al, 2008). Moreover, Salmonella Typhimurium T3SS-1-independent enteropathogenesis has also been demonstrated in murine and bovine infection models, and in chicken caecal and small-intestine explants (Coombes et al, 2005;Desin et al, 2009;Hapfelmeier et al, 2005). All these results indicate that in vivo T3SS-1-independent invasion mechanisms play an important role in Salmonella infection.…”

Section: Introductionmentioning

confidence: 99%

Heterogeneity of type III secretion system (T3SS)-1-independent entry mechanisms used by Salmonella Enteritidis to invade different cell types

et al. 2011

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Salmonella causes a wide range of diseases from acute gastroenteritis to systemic typhoid fever, depending on the host. To invade non-phagocytic cells, Salmonella has developed different mechanisms. The main invasion system requires a type III secretion system (T3SS) known as T3SS-1, which promotes a Trigger entry mechanism. However, other invasion factors have recently been described in Salmonella, including Rck and PagN, which were not expressed under our bacterial culture conditions. Based on these observations, we used adhesion and invasion assays to analyse the respective roles of Salmonella Enteritidis T3SS-1-dependent and -independent invasion processes at different times of infection. Diverse cell lines and cell types were tested, including endothelial, epithelial and fibroblast cells. We demonstrated that cell susceptibility to the T3SS-1-independent entry differs by a factor of nine between the most and the least permissive cell lines tested. In addition, using scanning electron and confocal microscopy, we showed that T3SS-1-independent entry into cells was characterized by a Trigger-like alteration, as for the T3SS-1-dependent entry, and also by Zipper-like cellular alteration. Our results demonstrate for what is believed to be the first time that Salmonella can induce Trigger-like entry independently of T3SS-1 and can induce Zipper-like entry independently of Rck. Overall, these data open new avenues for discovering new invasion mechanisms in Salmonella.

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“…Samples from the liver, spleen and caecum of each bird were enriched in selenite broth, as described above. Results pertaining to the group that received the total SPI-1 mutant (Sal18 DSPI-1 : : cat) have been reported previously by our group (Desin et al, 2009).…”

Section: Methodsmentioning

confidence: 69%

“…The SseB protein was produced and purified as an N-terminal His-tag fusion protein by using standard protocols, as described previously by our group (Desin et al, 2009).…”

Section: Methodsmentioning

confidence: 99%

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Salmonella enterica subspecies enterica serovar Enteritidis Salmonella pathogenicity island 2 type III secretion system: role in intestinal colonization of chickens and systemic spread

et al. 2010

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Salmonella enterica subspecies enterica serovar Enteritidis (S. Enteritidis) has been identified as a significant cause of salmonellosis in humans. Salmonella pathogenicity islands 1 and 2 (SPI-1 and SPI-2) each encode a specialized type III secretion system (T3SS) that enables Salmonella to manipulate host cells at various stages of the invasion/infection process. For the purposes of our studies we used a chicken isolate of S. Enteritidis (Sal18). In one study, we orally co-challenged 35-day-old specific pathogen-free (SPF) chickens with two bacterial strains per group. The control group received two versions of the wild-type strain Sal18: Sal18 attTn7 : : tet and Sal18 attTn7 : : cat, while the other two groups received the wild-type strain (Sal18 attTn7 : : tet) and one of two mutant strains. From this study, we concluded that S. Enteritidis strains deficient in the SPI-1 and SPI-2 systems were outcompeted by the wild-type strain. In a second study, groups of SPF chickens were challenged at 1 week of age with four different strains: the wild-type strain, and three other strains lacking either one or both of the SPI-1 and SPI-2 regions. On days 1 and 2 post-challenge, we observed a reduced systemic spread of the SPI-2 mutants, but by day 3, the systemic distribution levels of the mutants matched that of the wild-type strain. Based on these two studies, we conclude that the S. Enteritidis SPI-2 T3SS facilitates invasion and systemic spread in chickens, although alternative mechanisms for these processes appear to exist.

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Salmonella enterica Serovar Enteritidis Pathogenicity Island 1 Is Not Essential for but Facilitates Rapid Systemic Spread in Chickens

Cited by 49 publications

References 57 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

Heterogeneity of type III secretion system (T3SS)-1-independent entry mechanisms used by Salmonella Enteritidis to invade different cell types

Salmonella enterica subspecies enterica serovar Enteritidis Salmonella pathogenicity island 2 type III secretion system: role in intestinal colonization of chickens and systemic spread

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