Participation of the Salmonella OmpD Porin in the Infection of RAW264.7 Macrophages and BALB/c Mice

Ipinza, Francisco; Collao, Bernardo; Monsalva, Debbie; Bustamante, Vı́ctor H.; Luraschi, Roberto; Alegría-Arcos, Melissa; Almonacid, Daniel E.; Aguayo, Daniel; Calderón, Iván L.; Gil, Fernando; Santiviago, Carlos A.; Morales, Eduardo; Calva, Edmundo; Saavedra, Claudia P.

doi:10.1371/journal.pone.0111062

Cited by 24 publications

(17 citation statements)

References 48 publications

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“…Hence, the downregulation of ompD could be another factor for the reduction of adhesion and invasion of Salmonella Typhimurium in mammalian cells. This is concurrent with the findings of Ipinza et al [38] who described the role of ompD in Salmonella invasion and intracellular survival in RAW264.7 cells and BALBc mice. The significance of ompD in adherence of Salmonella Typhimurium was also indicated in human monocytes and intestinal epithelial cells [39].…”

Section: Discussionsupporting

confidence: 91%

Inhibition of Salmonella Typhimurium adhesion, invasion, and intracellular survival via treatment with methyl gallate alone and in combination with marbofloxacin

Birhanu

Park

Lee

et al. 2018

Vet Res

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Salmonella enterica serovar Typhimurium infects intestinal epithelia and macrophages, which is prevented by inhibiting adhesion and cell invasion. This study aimed to investigate the role of methyl gallate (MG) in adhesion, invasion, and intracellular survival of Salmonella Typhimurium in Caco-2 and RAW 264.7 cells via a gentamicin protection assay, confocal microscopy, and quantitative reverse-transcription polymerase chain reaction. MG (30 µg/mL) inhibited adhesion and invasion of Salmonella Typhimurium by 54.01% and 60.5% in RAW 264.7 cells, respectively. The combination of MG with sub-minimum inhibitory concentration (MIC) of marbofloxacin (MRB) inhibited the adhesion, invasion, and intracellular survival by 70.49%, 67.36%, and 74%, respectively. Confocal microscopy further revealed reductions in bacterial count in Caco-2 cells treated with MG alone or with sub-MIC of MRB. Furthermore, MG alone or in combination with sub-MIC of MRB decreased the motility of Salmonella Typhimurium. Quorum sensing genes including sdiA , srgE , and rck were downregulated by 52.8%, 61.7%, and 22.2%, respectively. Moreover, rac - 1 was downregulated by 56.9% and 71.9% for MG alone and combined with sub-MIC of MRB, respectively, in mammalian cells. Furthermore, MG downregulated virulence genes of Salmonella Typhimurium including cheY, ompD , sipB , lexA , and ompF by 59.6%, 60.2%, 20.5%, 31.4%, and 16.2%, respectively. Together, the present results indicate that MG alone or in combination with a sub-MIC of MRB effectively inhibited the adhesion, invasion, and intracellular survival of Salmonella Typhimurium in vitro by downregulating quorum sensing and virulence genes. Electronic supplementary material The online version of this article (10.1186/s13567-018-0597-8) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 91%

Inhibition of Salmonella Typhimurium adhesion, invasion, and intracellular survival via treatment with methyl gallate alone and in combination with marbofloxacin

Birhanu

Park

Lee

et al. 2018

Vet Res

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“…Expression of nmpC was downregulated in S. Typhimurium exposed to H 2 O 2 (Calderón et al, 2011). Additionally, NmpC may be needed for adherence and recognition of S. Typhimurium to human macrophages and epithelial cells during the initial stages of infection (Hara-Kaonga and Pistole, 2004) and is also involved in host cell recognition in mammalian models (Ipinza et al, 2014;van der Heijden et al, 2016). In our study, we observed up-regulation of both nmpC and ROS detoxification gene ahpC on leaves.…”

Section: Discussionsupporting

confidence: 53%

Salmonella enterica Elicits and Is Restricted by Nitric Oxide and Reactive Oxygen Species on Tomato

et al. 2020

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The enteric pathogen Salmonella enterica can interact with parts of the plant immune system despite not being a phytopathogen. Previous transcriptomic profiling of S. enterica associating with tomato suggested that Salmonella was responding to oxidative and nitrosative stress in the plant niche. We aimed to investigate whether Salmonella was eliciting generation of reactive oxygen species (ROS) and nitric oxide (NO), two components of the microbe-associated molecular pattern (MAMP)-triggered immunity (MTI) of plants. We also sought to determine whether this interaction had any measurable effects on Salmonella colonization of plants. Biochemical, gene expression and on-plant challenge assays of tomato vegetative and fruit organs were conducted to assess the elicitation of ROS and NO in response to Salmonella Newport association. The counter bacterial response and the effect of NO and ROS on Salmonella colonization was also investigated. We detected H 2 O 2 in leaves and fruit following challenge with live S. Newport (p < 0.05). Conversely, NO was detected on leaves but not on fruit in response to S. Newport (p < 0.05). We found no evidence of plant defense attenuation by live S. Newport. Bacterial gene expression of S. Newport associating with leaves and fruit were indicative of adaptation to biotic stress in the plant niche. The nitrosative stress response genes hmpA and yoaG were significantly upregulated in S. Newport on leaves and fruit tissue compared to tissue scavenged of NO or ROS (p < 0.05). Chemical modulation of these molecules in the plant had a restrictive effect on bacterial populations. Significantly higher S. Newport titers were retrieved from H 2 O 2 scavenged leaves and fruit surfaces compared to controls (p < 0.05). Similarly, S. Newport counts recovered from NO-scavenged leaves, but not fruit, were higher compared to control (p < 0.05), and significantly lower on leaves pre-elicited to produce endogenous NO. We present evidence of Salmonella elicitation of ROS and NO in tomato, which appear to have a restricting effect on the pathogen. Moreover, bacterial recognition of ROS and NO stress was detected. This work shows that tomato has mechanisms to restrict Salmonella populations and ROS and NO detoxification may play an important role in Salmonella adaptation to the plant niche.

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“…In mice immunized with porins (containing mainly OmpD), IgM antibodies are produced by B1b cells and these antibodies reduce S. typhimurium bacteraemia, suggesting a protective role for OmpD . In RAW264.7, a mouse macrophage cell line, OmpD inhibits replication of S. typhimurium and reduces systemic dissemination by neutralizing reactive oxygen species .…”

Section: Discussionmentioning

confidence: 99%

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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Participation of the Salmonella OmpD Porin in the Infection of RAW264.7 Macrophages and BALB/c Mice

Cited by 24 publications

References 48 publications

Inhibition of Salmonella Typhimurium adhesion, invasion, and intracellular survival via treatment with methyl gallate alone and in combination with marbofloxacin

Inhibition of Salmonella Typhimurium adhesion, invasion, and intracellular survival via treatment with methyl gallate alone and in combination with marbofloxacin

Salmonella enterica Elicits and Is Restricted by Nitric Oxide and Reactive Oxygen Species on Tomato

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

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