Type 1 fimbriae are important factors limiting the dissemination and colonization of mice by Salmonella Enteritidis and contribute to the induction of intestinal inflammation during Salmonella invasion

Abstract

We have recently shown that Salmonella Gallinarum type 1 fimbriae with endogenous mannose-resistant (MR) variant of the FimH protein increase systemic dissemination of S. Gallinarum and colonization of internal organs in comparison to the S. Gallinarum fimH knockout strain or the mutant expressing mannose-sensitive (MS) FimH variant from S. Enteritidis. Elaborating from these studies, we proposed that MS variants of FimH are advantageous in gastrointestinal infections, in contrast to MR FimH variants which decrease intestinal colonization and promote their systemic spreading. To support our hypothesis, we carried out in vivo studies using mice infected with wild-type S. Enteritidis and its fimH knockout strain (S. Enteritidis), which was characterized by significantly lower adhesion and invasiveness of murine ICE-1 intestinal cells. Using bioluminescence imaging, we observed that the loss of MS FimH adhesin correlates well with the highly increased colonization of mice by these bacteria. The appearance of the mutant strain was observed much earlier than wild-type Salmonella, and mice infected with 104–107 S. Enteritidis fimH::kan CFUs had significantly (P < 0.05) shorter infection-free time than animals inoculated with wild-type S. Enteritidis. Infections caused by non-typhoid Salmonella, such as S. Enteritidis, are associated with massive inflammation of the lamina propria and lymph nodes in the intestinal tract. Therefore, we evaluated the role of MS type 1 fimbriae in the induction of cytokine expression and secretion, using murine ICE-1 intestinal cells. We showed that the expression, as well as secretion, of Il-1b, Il-6, Il-10, and Il-12b was significantly higher in cells infected with wild-type S. Enteritidis compared to cells infected with the mutant strain. Based on our results, we propose that type 1 fimbriae may play an important role in the pathogenicity of S. Enteritidis and may contribute to an intestinal inflammatory response.

Cinnamaldehyde, Carvacrol and Organic Acids Affect Gene Expression of Selected Oxidative Stress and Inflammation Markers in IPEC‐J2 Cells Exposed to Salmonella typhimurium

“…This applies in particular to combinations of the phytocompounds with certain acids, particularly cinnamaldehyde with cinnamic acid and carvacrol with either cinnamic or propionic acid. The increase in the secretion of fimbrial proteins is correlated with increased inflammation of the affected cells (Kuźmińska‐Bajor et al ., ). Ibarra et al .…”

“…This applies in particular to combinations of the phytocompounds with certain acids, particularly cinnamaldehyde with cinnamic acid and carvacrol with either cinnamic or propionic acid. The increase in the secretion of fimbrial proteins is correlated with increased inflammation of the affected cells (Kuźmińska-Bajor et al, 2015). Ibarra et al (2010) also showed that type 1 fimbriae production is increased as a bacterial stress response, and this production does not result in increased invasion, but it is a result of impaired ability to invade host-cells.…”

SalmonellaFimbrial Protein FimH Is Involved in Expression of Proinflammatory Cytokines in a Toll-Like Receptor 4-Dependent Manner

“…FimH is responsible for binding to target receptors and exhibits specificity for glycoproteins containing terminal mannose residues (15)(16)(17). This adhesive protein has been reported to play an important role in bacterial adhesion during the process of colonization and invasion of host tissue (18)(19)(20)(21)(22)(23). Moreover, the interactions between type 1 fimbriae and host cell receptors play a critical role in the initiation and modulation of innate and adaptive immune responses (24)(25)(26).…”

Pre-Growth Culture Conditions Affect Type 1 Fimbriae-Dependent Adhesion of Salmonella

“…Salmonella enterica uses various factors for successful infection by the fecal-oral route. The SPI-1 T3SS is crucial for Salmonella infection, but other systems, including flagella and fimbrial operons, contribute to Salmonella pathogenesis [ 18 , 19 , 20 , 21 , 22 , 23 ].…”