Intestinal Inflammation Responds to Microbial Tissue Load Independent of Pathogen/Non-Pathogen Discrimination

Willer, Yvonne; Muller, B; Bumann, Dirk

doi:10.1371/journal.pone.0035992

Cited by 9 publications

(11 citation statements)

References 32 publications

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“…Thus, genes controlling these first few hours of response to pathogen invasion are likely gene candidates for resistance traits. However, if this does not result in elimination or destruction of the micro-organism, then the tissue load (Willer et al, 2012), and whether the micro-organism is alive or dead (Fontana and Vance, 2011), in other words sensing micro-organism growth in tissues, may become more important determinants of immunopathology. In this second phase, the host may detect micro-organism derived metabolic molecules such as mRNA or bacterial pyrophosphates.…”

Section: Identity Of Candidate Resistance and Tolerance Genesmentioning

confidence: 99%

The molecular pathways underlying host resistance and tolerance to pathogens

Glass¹

2012

Front. Gene.

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Breeding livestock that are better able to withstand the onslaught of endemic- and exotic pathogens is high on the wish list of breeders and farmers world-wide. However, the defense systems in both pathogens and their hosts are complex and the degree of genetic variation in resistance and tolerance will depend on the trade-offs that they impose on host fitness as well as their life-histories. The genes and pathways underpinning resistance and tolerance traits may be distinct or intertwined as the outcome of any infection is a result of a balance between collateral damage of host tissues and control of the invading pathogen. Genes and molecular pathways associated with resistance are mainly expressed in the mucosal tract and the innate immune system and control the very early events following pathogen invasion. Resistance genes encode receptors involved in uptake of pathogens, as well as pattern recognition receptors (PRR) such as the toll-like receptor family as well as molecules involved in strong and rapid inflammatory responses which lead to rapid pathogen clearance, yet do not lead to immunopathology. In contrast tolerance genes and pathways play a role in reducing immunopathology or enhancing the host's ability to protect against pathogen associated toxins. Candidate tolerance genes may include cytosolic PRRs and unidentified sensors of pathogen growth, perturbation of host metabolism and intrinsic danger or damage associated molecules. In addition, genes controlling regulatory pathways, tissue repair and resolution are also tolerance candidates. The identities of distinct genetic loci for resistance and tolerance to infectious pathogens in livestock species remain to be determined. A better understanding of the mechanisms involved and phenotypes associated with resistance and tolerance should ultimately help to improve livestock health and welfare.

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Section: Identity Of Candidate Resistance and Tolerance Genesmentioning

confidence: 99%

The molecular pathways underlying host resistance and tolerance to pathogens

Glass¹

2012

Front. Gene.

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“…Kim et al [ 5 ] and Huang et al [ 20 ] found that P. linteus organic extracts inhibited NF-κB, MMP-9 and MAPK activation in vivo and in vitro , leading to the conclusion that P. linteus may present a therapeutic approach for inflammation-associated disorders such as rheumatoid arthritis, psoriasis and other autoimmune afflictions. Shnyreva et al [ 21 ] found that treatment of K562 cells with P. linteus ethanol extract increased the expression of the anti-inflammatory cytokine IL-10.…”

Section: Introductionmentioning

confidence: 99%

Phellinus linteus polysaccharide extracts increase the mitochondrial membrane potential and cause apoptotic death of THP-1 monocytes

Griensven

Verhoeven

2013

Chin Med

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BackgroundThe differentiation resp. death of human monocytic THP-1 cells induced by polysaccharide extracts of the medicinal mushrooms Phellinus linteus, Agaricus bisporus and Agaricus brasiliensis have been studied. This study aims to identify leads for the causal effects of these mushroom components on cell differentiation and death.MethodsTHP-1 cells were treated with different polysaccharide extracts of mushrooms and controls. Morphological effects were observed by light microscopy. Flow cytometry was applied to follow the cell differentiation by cell cycle shifts after staining with propidium iodide, changes of mitochondrial membrane potential after incubation with JC-1, and occurrence of intracellular reactive oxygen species after incubation with hydroethidine. Principal component analysis of the data was performed to evaluate the cellular effects of the different treatments.ResultsP. linteus polysaccharide extracts induced dose-dependent apoptosis of THP-1 cells within 24 h, while A. bisporus and A. brasiliensis polysaccharide extracts caused differentiation into macrophages. A pure P. linteus polysaccharide had no effect. Apoptosis was inhibited by preincubating THP-1 cells with human serum. The principal component analysis revealed that P. linteus, A. bisporus and A. brasiliensis polysaccharide extracts increased reactive oxygen species production. Both A. bisporus and A. brasiliensis polysaccharide extracts decreased the mitochondrial membrane potential, while this was increased by P. linteus polysaccharide extracts.ConclusionsP. linteus polysaccharide extracts caused apoptosis of THP-1 monocytes while A. bisporus and A. brasiliensis polysaccharide extracts caused these cells to differentiate into macrophages. The protective effects of human serum suggested that P. linteus polysaccharide extract induced apoptosis by extrinsic pathway, i.e. by binding to the TRAIL receptor. The mitochondrial membrane potential together with reactive oxygen species seems to play an important role in cell differentiation and cell death.

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“…Johansson et al ., ), making it unlikely that the E. cyathigerum genotypes present at a given waterbody would never have encountered E. coli in other waterbodies. Furthermore, an immune response to familiar non‐pathogenic bacteria has been observed before and interpreted as immune priming of the host (Freitak et al ., , ) or the inability to distinguish between pathogenic and non‐pathogenic bacterial challenges (Willer et al ., ).…”

Section: Discussionmentioning

confidence: 99%

“…Interactions with non‐pathogenic bacteria have been ignored in the context of trade‐offs underlying the maintenance of variation in immune function (Sheldon & Verhulst, ; Schmid‐Hempel, ). Yet, it has recently been documented that exposure to non‐pathogenic bacteria can activate the immune system (Freitak et al ., ; Freitak, Heckel & Vogel, ; Willer, Müller & Bumann, ). We therefore hypothesise that non‐pathogenic bacteria may also increase vulnerability to predation, hence may play a role in the maintenance of variation in immune defence.…”

Section: Introductionmentioning

confidence: 99%

Non‐pathogenic aquatic bacteria activate the immune system and increase predation risk in damselfly larvae

Janssens

Stoks

2013

Freshwater Biology

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Summary Pathogens can increase vulnerability to predation through their harmful effects on hosts. Recently, it was shown that the mere activation of the immune system by pathogens may increase the host's risk of predation. Here, we test whether exposure to non‐pathogenic bacteria also activates the immune system and thereby increases vulnerability to predation. We exposed Enallagma cyathigerum damselfly larvae to a non‐pathogenic strain of the bacterium Escherichia coli and measured immune defence, anti‐predator behaviour and survival times in the presence of larval dragonfly predators. To evaluate whether non‐pathogenic bacteria also generated energy‐based trade‐offs leading to other fitness costs, we also quantified growth rate and survival in the absence of predators. Exposure to the non‐pathogenic bacterium did not affect survival in the absence of the predator but increased growth rate, possibly a response to reduce exposure time to the bacterium. Larvae exposed to the bacterium activated their immune response as shown by an increase in the activity of phenoloxidase and the number of haemocytes. The bacterium affected anti‐predator traits involved in avoiding detection by predators as well as traits involved in escape after detection. Pre‐exposed larvae showed higher activity levels and further increased the number of feeding strikes in the presence of predation risk, possibly driven by energetic constraints. Pre‐exposed larvae swam less often when attacked, but faster. This impaired anti‐predator response came at the ecological cost of increased vulnerability to predation. Our study demonstrated that exposure to non‐pathogenic bacteria increases vulnerability to predation, which is a novel type of antagonistic interaction. This highlights the unexplored possibility that non‐pathogens may play a role in maintaining variation in immune defence through insidious effects on predator–prey interactions. Since non‐pathogenic bacteria can be very abundant, this unexplored ecological cost of immune system activation in terms of increased predation may have major consequences in natural systems and may provide an unexplored new force underlying variation in immune defence.

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Intestinal Inflammation Responds to Microbial Tissue Load Independent of Pathogen/Non-Pathogen Discrimination

Cited by 9 publications

References 32 publications

The molecular pathways underlying host resistance and tolerance to pathogens

The molecular pathways underlying host resistance and tolerance to pathogens

Phellinus linteus polysaccharide extracts increase the mitochondrial membrane potential and cause apoptotic death of THP-1 monocytes

Non‐pathogenic aquatic bacteria activate the immune system and increase predation risk in damselfly larvae

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