Repression of flagella is a common trait in field isolates of Salmonella enterica serovar Dublin and is associated with invasive human infections

The nontyphoidal Salmonella enterica serovar Dublin is adapted to cattle but infrequently infects humans, very often resulting in invasive infections with high levels of morbidity and mortality. A Salmonella-induced intestinal acute inflammatory response is postulated as a mechanism to prevent bacte...

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Bibliographic Details
Published in:Infection and immunity 2014-04, Vol.82 (4), p.1465-1476
Main Authors: Yim, Lucía, Sasías, Sebastián, Martínez, Arací, Betancor, Laura, Estevez, Verónica, Scavone, Paola, Bielli, Alejandro, Sirok, Alfredo, Chabalgoity, José Alejandro
Format: Article
Language:English
Subjects:
Analysis of Variance
Animals
Caco-2 Cells
Cecum
Chemokine CCL20 - metabolism
Female
Flagella - physiology
Flagellin - genetics
Flagellin - metabolism
Host Response and Inflammation
Humans
Interleukin-8 - metabolism
Mice
Mice, Inbred C57BL
Promoter Regions, Genetic
Salmonella enterica
Salmonella enterica - pathogenicity
Salmonella enterica - physiology
Salmonella Infections - microbiology
Salmonella Infections - pathology
Species Specificity
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Summary:The nontyphoidal Salmonella enterica serovar Dublin is adapted to cattle but infrequently infects humans, very often resulting in invasive infections with high levels of morbidity and mortality. A Salmonella-induced intestinal acute inflammatory response is postulated as a mechanism to prevent bacterial dissemination to systemic sites. In S. enterica serovar Typhimurium, flagella contribute to this response by providing motility and FliC-mediated activation of pattern recognition receptors. In this study, we found 4 Salmonella enterica isolates, with the antigenic formula 9,12:-:-, that, based on fliC sequence and multilocus sequence type (MLST) analyses, are aflagellate S. Dublin isolates. Interestingly, all were obtained from human bloodstream infections. Thus, we investigated the potential role of flagella in the unusual invasiveness exhibited by S. Dublin in humans by analyzing flagellation and proinflammatory properties of a collection of 10 S. Dublin human clinical isolates. We found that 4 of 7 blood isolates were aflagellate due to significantly reduced levels of fliC expression, whereas all 3 isolates from other sources were flagellated. Lack of flagella correlated with a reduced ability of triggering interleukin-8 (IL-8) and CCL20 chemokine expression in human intestinal Caco-2 cells and with reduced early inflammation in the ceca of streptomycin-pretreated C57/BL6 mice. These results indicate that flagella contribute to the host intestinal inflammatory response to Salmonella serovar Dublin and suggest that their absence may contribute to its systemic dissemination through dampening of the gut immune response. Analysis of FliC production in a collection of cattle isolates indicated that the aflagellate phenotype is widely distributed in field isolates of S. Dublin.
ISSN:0019-9567
1098-5522
DOI:10.1128/IAI.01336-13