Salmonella enterica Induces Joint Inflammation and Expression of Interleukin-17 in Draining Lymph Nodes Early after Onset of Enterocolitis in Mice

Llana, Mariángeles Noto; Sarnacki, Sebastián H.; Vázquez, Melina; Gärtner, A.; Giacomodonato, Mónica N.; Cerquetti, M C

doi:10.1128/iai.00324-12

Cited by 19 publications

(27 citation statements)

References 57 publications

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“…Increased levels of IL‐23 and IL‐6 in response to rOmpA‐sal may lead to the induction of IL‐17‐producing cells. Mice infected with Salmonella enterica express IL‐17 in draining lymph nodes and develop arthritis early after onset of enterocolitis . We and others have shown that patients with ReA/uSpA have increased IL‐17 and IL‐6 in the synovial fluid compared to patients with rheumatoid arthritis , but IL‐23 was not detected in our previous study .…”

Section: Discussioncontrasting

confidence: 66%

RecombinantSalmonella typhimuriumouter membrane protein A is recognized by synovial fluid CD8 cells and stimulates synovial fluid mononuclear cells to produce interleukin (IL)-17/IL-23 in patients with reactive arthritis and undifferentiated spondyloarthropathy

Chaurasia

Shasany

Aggarwal

et al. 2016

Clinical and Experimental Immunology

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SummaryIn developing countries, one-third of patients with reactive arthritis (ReA) and undifferentiated spondyloarthropathy (uSpA) are triggered by Salmonella typhimurium. Synovial fluid mononuclear cells (SFMCs) of patients with ReA and uSpA proliferate to low molecular weight fractions (lmwf) of outer membrane proteins (Omp) of S. typhimurium. To characterize further the immunity of Omp of Salmonella, cellular immune response to two recombinant proteins of lmwf, OmpA and OmpD of S. typhimurium (rOmpA/D-sal) was assessed in 30 patients with ReA/uSpA. Using flow cytometry, 17 of 30 patients' SF CD81 T cells showed significant intracellular interferon (IFN)-g to Omp crude lysate of S. typhimurium. Of these 17, 11 showed significantly more CD8rOmpA-sal, whereas only four showed reactivity to rOmpD-sal. The mean stimulation index was significantly greater in rOmpA-sal than rOmpD-sal [3Á0 (1Á5-6Á5) versus 1Á5 (1Á0-2Á75), P < 0Á005]. Similarly, using enzymelinked immunospot (ELISPOT) in these 17 patients, the mean spots of IFN-g-producing SFMCs were significantly greater in rOmpA-sal than rOmpD-sal [44Á9 (3Á5-130Á7) versus 19Á25 (6-41), P < 0Á05]. SFMCs stimulated by rOmpA-sal produced significantly more proinflammatory cytokines than rOmpD-sal: IFN-g [1Á44 (0Á39-20Á42) versus 0Á72 (0Á048-9Á15) ng/ml, P < 0Á05], interleukin (IL)217 [28Á60 (6Á15-510Á86) versus 11Á84 (6Á83-252Á62) pg/ml, P < 0Á05], IL-23 [70Á19 (15-1161Á16) versus 28Á25 (> 15-241Á52) pg/ml, P < 0Á05] and IL-6 [59Á78 (2Á03-273Á36) versus 10Á17 (0Á004-190Á19) ng/ml, P < 0Á05]. The rOmpA-sal-specific CD8 1 T cell response correlated with duration of current synovitis (r 5 0Á53, P < 0Á05). Thus, OmpA of S. typhimurium is a target of SF CD8 1 T cells and drives SFMC to produce increased cytokines of the IL-17/IL-23 axis which contribute to the pathogenesis of Salmonella-triggered ReA.

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Section: Discussioncontrasting

confidence: 66%

RecombinantSalmonella typhimuriumouter membrane protein A is recognized by synovial fluid CD8 cells and stimulates synovial fluid mononuclear cells to produce interleukin (IL)-17/IL-23 in patients with reactive arthritis and undifferentiated spondyloarthropathy

Chaurasia

Shasany

Aggarwal

et al. 2016

Clinical and Experimental Immunology

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“…Furthermore, intestinal infection with Δ invG mutant of Salmonella , bearing a defective TTSS-1, triggers neither intestinal inflammatory IL-17 nor joint inflammation [16,49]. In the present work we show that consumption of LCFM prevents IL-17 intestinal response to Salmonella and at the same time blocks the induction of joint inflammation.…”

Section: Discussionmentioning

confidence: 48%

“…Enteritidis in order to induce enterocolitis [16]. Mice received 20 mg of streptomycin 24 h before intragastric infection with 3 to 4 x 10 3 CFU of the pathogen (EC group).…”

Section: Resultsmentioning

confidence: 99%

Consumption of Lactobacillus casei Fermented Milk Prevents Salmonella Reactive Arthritis by Modulating IL-23/IL-17 Expression

et al. 2013

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Reactive arthritis is the development of sterile joint inflammation as a sequel to a remote infection, often in the gut. We have previously shown that a low dose of S. enteritidis inoculated to streptomycin-pretreated mice generates a self-limiting enterocolitis suitable for studying reactive arthritis. Here we show that consumption of Lactobacillus casei prior to infection abolishes intestinal and joint inflammation triggered by Salmonella. BALB/c mice were sacrificed after infection; intestinal and joint samples were analyzed for histological changes and expression of cytokines. TNF-α was measured by ELISA and the expression of IL-1β, IL-6, IL-10, IL-17, IL-23 and TGF-β was assessed by qPCR. L. casei consumption prevented Salmonella-induced synovitis, the increment of TNF-α in knees and the increase of IL-17 expression in popliteal and inguinal lymph nodes. At intestinal level consumption of L. casei drastically diminished S. enteritidis invasiveness and shortened splenic persistence of the pathogen. Bacterial loads recovered at days 2 and 5 from Peyer’s patches were 10-fold lower in mice fed with L. casei. In accordance, we found that the augment in gut permeability induced during enterocolitis was decreased in those animals. Consumption of L. casei prior to infection failed to increase anti- inflammatory molecules such as IL-10 and TGF-β in the intestine. On the other hand, consumption of L. casei abrogated the expression of TNF-α, IL-17, IL-23, IL-1β and IL-6 in cecum and mesenteric lymph nodes. These cytokines are needed for differentiation of immune cells involved in the development of reactive arthritis such as Th17 and γδ T cells. Trafficking of these inflammatory cells from the gut to the joints has been proposed as a mechanism of generation of reactive arthritis. Our results suggest that L. casei consumption prevents Salmonella-induced synovitis by altering the intestinal milieu necessary for differentiation of cells involved in the generation of joint inflammation.

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“…IL-17 is a central cytokine implicated in inflammation and antimicrobial defense [ 12 ]. In the murine models of S. Enteritidis infection, the onset of enterocolitis is associated with a dramatic increase in the expression of IL-17 [ 4 , 13 ]. Previous studies revealed an important role played by the Th17-mediated mucosal immunity in the early control of infections caused by a variety of pathogens [ 12 , 14 , 15 ].…”

Section: Discussionmentioning

confidence: 99%

Inflammatory Responses to Salmonella Infections Are Serotype-Specific

Ktsoyan

Ghazaryan

Manukyan

et al. 2013

International Journal of Bacteriology

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The main purpose of this study was to investigate the profile of inflammatory response in patients with acute salmonellosis caused by two serotypes of Salmonella enterica, S. Enteritidis and S. Typhimurium, as well as in convalescent patients with previous acute disease caused by S. Enteritidis. Patients with acute disease showed significantly elevated levels of IL-1β, IL-17, IL-10, and calprotectin compared to healthy control subjects. In convalescent patients, these markers were also significantly elevated, with the exception of IL-1β. Multivariate statistical analyses with the use of these variables produced models with a good predictive accuracy resulting in excellent separation of the diseased and healthy cohorts studied. Overall, the results suggest that the profile of inflammatory response in this disease is determined, to a significant degree, by the serotype of Salmonella, and the profile of certain cytokines and calprotectin remains abnormal for a number of months following the acute disease stage.

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Salmonella enterica Induces Joint Inflammation and Expression of Interleukin-17 in Draining Lymph Nodes Early after Onset of Enterocolitis in Mice

Cited by 19 publications

References 57 publications

RecombinantSalmonella typhimuriumouter membrane protein A is recognized by synovial fluid CD8 cells and stimulates synovial fluid mononuclear cells to produce interleukin (IL)-17/IL-23 in patients with reactive arthritis and undifferentiated spondyloarthropathy

RecombinantSalmonella typhimuriumouter membrane protein A is recognized by synovial fluid CD8 cells and stimulates synovial fluid mononuclear cells to produce interleukin (IL)-17/IL-23 in patients with reactive arthritis and undifferentiated spondyloarthropathy

Consumption of Lactobacillus casei Fermented Milk Prevents Salmonella Reactive Arthritis by Modulating IL-23/IL-17 Expression

Inflammatory Responses to Salmonella Infections Are Serotype-Specific

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