Transcytosis of Gastrointestinal Epithelial Cells by Escherichia coli K1

Burns, Jane L.; Griffith, Adam; Barry, John J. A.; Jonas, Mechthild; Emil, Y.

doi:10.1203/00006450-200101000-00010

Cited by 32 publications

(30 citation statements)

References 29 publications

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“…We therefore tested Caco-2 cells for their state of cell differentiation and the effect of this state on invasion by S. Enteritidis. Alkaline phosphatase activity was significantly higher (P,0.01, Student's ttest) in 14-day-old cells compared with 5-day-old cells (Table 3) (Burns et al, 2001;Hara et al, 1993). In addition, 14-day-old cells showed well-developed apical brush borders, as visualized by TEM, indicating that 14-day-old cells were well differentiated (data not shown).…”

Section: S Enteritidis Isolates Differ In Their Invasiveness In Diffmentioning

confidence: 89%

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: S Enteritidis Isolates Differ In Their Invasiveness In Diffmentioning

confidence: 89%

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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“…One milliliter of fresh medium (with 10% FCS and no antibiotics) was added to the lower chamber, and about 8 ϫ 10 7 bacteria in 400 l of tissue culture medium were added to the upper chamber; this inoculum is consistent with that used by others (2,3,11) and with the density of intestinal enterococci in some settings. Transepithelial electrical resistance was monitored at the beginning and end of the experiment.…”

Section: Methodsmentioning

confidence: 99%

“…A similar assay has also been used by others to study gram-positive bacteria; for example, pneumococci were shown to translocate through the endothelial cell line EC 219, which is a rat brain microvessel-derived cell line, and group B streptococci were found to penetrate through a chorion cell line without disruption of intercellular junctions (15,24). A human colon carcinoma cell line, T84, has been widely used for in vitro models of transport studies (3,4,8,9). These cells have the ability to form a tall columnar epithelial monolayer and to develop tight or occluding intercellular junctions when grown on permeable supports, with the basolateral surface attached to the support and the apical surface exposed to the outside (4).…”

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confidence: 99%

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Translocation of Enterococcus faecalis Strains across a Monolayer of Polarized Human Enterocyte-Like T84 Cells

Zeng

Fang

Weinstock³

et al. 2004

J Clin Microbiol

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We used a two-chamber system to study transcytosis of Enterococcus faecalis across monolayers of human colon carcinoma-derived T84 cells, which show structural resemblance to the native intestine. Among 16 E. faecalis isolates from different sources, the well-characterized strain OG1RF and 8 other isolates (2 endocarditis isolates, 1 urine isolate, and all 5 fecal isolates) showed translocation in this assay, while 6 clinical isolates (3 endocarditis and 3 urine isolates), the recipient strain JH2-2, and the control, Escherichia coli DH5␣, had no detectable translocation. Of two OG1RF mutants involving the previously studied epa (enterococcal polysaccharide antigen) gene cluster, known to be needed for virulence and resistance to killing by polymorphonuclear leukocytes, one epa mutant (TX5179) was unable to translocate, while TX5180, with an epa disruption farther downstream, showed a moderate decrease in translocation relative to that of the wild-type strain OG1RF (P < 0.01), indicating that the epa gene cluster is important for translocation across a T84 monolayer. This observation was confirmed by complementation of the epa mutant (TX5179) with epa genes and restoration of its translocation ability. In conclusion, we have demonstrated translocation of at least some strains of E. faecalis across T84 monolayers, although strains differ considerably in this ability, and we have demonstrated that epa mutations can cause marked changes in successful translocation. These results suggest that this model may be a useful in vitro system for studying the process of translocation from the intestinal tract.Enterococci are part of the normal flora in human intestines and are also a leading cause of nosocomial infections (5, 12). These organisms seem to be able to migrate from the gastrointestinal tract into the bloodstream and cause systemic infections such as bacteremia and even endocarditis. The passage of bacteria from the gastrointestinal tract to extraintestinal sites is called translocation (1,22). Wells and colleagues have presented evidence that Enterococcus faecalis can translocate across the mouse intestinal tract (23). In their study, following E. faecalis overgrowth (elicited by metronidazole and streptomycin treatment after oral inoculation of E. faecalis resistant to these agents), coccal bacteria appeared in the intestinal lumen and were observed within vacuoles in the cytoplasm of epithelial cells (23). By immunofluorescent microscopy, E. faecalis cells were localized within columnar epithelial cells, lamina propria, submucosa, and muscularis externa. Thus, E. faecalis cells appear to be able to translocate across an intact intestinal tract, although the enterococcal traits involved in the process were not determined. Runkel et al. also reported that morphine, a known inhibitor of myoelectric activity in the intestines of rats that prolongs gut transit time, increases intestinal microflora levels and promotes bacterial translocation from the intestinal tract to extraintestinal sites (16).An in vitro transc...

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“…In vitro studies have shown that bacteria can transcytose across cultured cell monolayers, including Campylobacter jejuni (Grant et al, 1993;Russell and Blake, 1994;Bacon et al, 2001;Kopecko et al, 2001;Hu et al, 2008;Watson and Galán, 2008), Neisseria gonorrhoeae and Neisseria meningitidis (Makino et al, 1991;Merz and So, 2000;Kuespert et al, 2006;Wang et al, 2008;Sutherland et al, 2010), Streptococcus pneumoniae (Zhang et al, 2000;Kaetzel, 2001), and Escherichia coli (Burns et al, 2001;Xie et al, 2004). Yet, with the exception of bacterial sampling by M cells (see next paragraph), this is the first time to our knowledge that a bacterium has been shown to translocate across an epithelial layer by transcytosis in vivo, resulting in its systemic dissemination.…”

Section: Discussionmentioning

confidence: 99%

Transcytosis ofListeria monocytogenesacross the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin

Nikitas¹,

Deschamps²,

Disson³

et al. 2011

J Cell Biol

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Transcytosis of Gastrointestinal Epithelial Cells by Escherichia coli K1

Cited by 32 publications

References 29 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

Translocation of Enterococcus faecalis Strains across a Monolayer of Polarized Human Enterocyte-Like T84 Cells

Transcytosis ofListeria monocytogenesacross the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin

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