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Escherichia coli mediated resistance of Entamoeba histolytica to oxidative stress is triggered by oxaloacetate.

ABSTRACT: Amebiasis, a global intestinal parasitic disease, is due to Entamoeba histolytica. This parasite, which feeds on bacteria in the large intestine of its human host, can trigger a strong inflammatory response upon invasion of the colonic mucosa. Whereas information about the mechanisms which are used by the parasite to cope with oxidative and nitrosative stresses during infection is available, knowledge about the contribution of bacteria to these mechanisms is lacking. In a recent study, we demonstrated that enteropathogenic Escherichia coli O55 protects E. histolytica against oxidative stress. Resin-assisted capture (RAC) of oxidized (OX) proteins coupled to mass spectrometry (OX-RAC) was used to investigate the oxidation status of cysteine residues in proteins present in E. histolytica trophozoites incubated with live or heat-killed E. coli O55 and then exposed to H2O2-mediated oxidative stress. We found that the redox proteome of E. histolytica exposed to heat-killed E. coli O55 is enriched with proteins involved in redox homeostasis, lipid metabolism, small molecule metabolism, carbohydrate derivative metabolism, and organonitrogen compound biosynthesis. In contrast, we found that proteins associated with redox homeostasis were the only OX-proteins that were enriched in E. histolytica trophozoites which were incubated with live E. coli O55. These data indicate that E. coli has a profound impact on the redox proteome of E. histolytica. Unexpectedly, some E. coli proteins were also co-identified with E. histolytica proteins by OX-RAC. We demonstrated that one of these proteins, E. coli malate dehydrogenase (EcMDH) and its product, oxaloacetate, are key elements of E. coli-mediated resistance of E. histolytica to oxidative stress and that oxaloacetate helps the parasite survive in the large intestine. We also provide evidence that the protective effect of oxaloacetate against oxidative stress extends to Caenorhabditis elegans.

SUBMITTER: Shaulov Y

PROVIDER: S-EPMC6181410 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Escherichia coli mediated resistance of Entamoeba histolytica to oxidative stress is triggered by oxaloacetate.

Shaulov Yana Y Shimokawa Chikako C Trebicz-Geffen Meirav M Nagaraja Shruti S Methling Karen K Lalk Michael M Weiss-Cerem Lea L Lamm Ayelet T AT Hisaeda Hajime H Ankri Serge S

PLoS pathogens 20181011 10

Amebiasis, a global intestinal parasitic disease, is due to Entamoeba histolytica. This parasite, which feeds on bacteria in the large intestine of its human host, can trigger a strong inflammatory response upon invasion of the colonic mucosa. Whereas information about the mechanisms which are used by the parasite to cope with oxidative and nitrosative stresses during infection is available, knowledge about the contribution of bacteria to these mechanisms is lacking. In a recent study, we demons ...[more]

PMID: 30308066

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Project description:Characterization of the human microbiota is providing new insightsinto the complexity of host–parasite–bacterium relationships. Amoebiasis (an intestinal infection affecting a large proportion of the population in many countries worldwide) is caused by the amoebic parasite Entamoeba histolytica. During amoebiasis, the parasite encounters several types of stress as a result of the host’s response to infection. Given that E. histolytica phagocytises bacteria in the intestinal lumen, we hypothesized that enteric bacteria can influence the course of an amoebic infection. Hence, we used live Escherichia coli O55 as a pertinent model of the bacterial community’s contribution to amoebic responses during host- induced stress. By measuring amoebic survival, we found that live E. coli protected E. histolytica against oxidative stress (OS) but not against nitrosative stress. E. coli– associated protection is correlated with massive transcriptionalchanges in amoebic genes acquired through lateral transfer from the bacterial kingdom, including genes coding for proteinscontaining leucine-rich repeat (LRR) motifs. The transcriptome profile triggered by OS and E. coli was also observed with other enteric bacteria, including pathogens and non-pathogens. In contrast, exposure to a probiotic resulted in a different transcriptome profile. The present study shows that OS and live bacteria together modulate 84 of E. histolytica’s 137 LRR protein genes. The LRR proteins are involvedin protein-ligand and protein-protein interactions – especially in proteins that interact with bacteria as part of the innate immune response in mammals and plants, such as Toll-like receptors. The structural and functional homology of LRRs and TLRs identified here suggest that despite its old age in evolutionary terms, the protozoan E. histolytica displays key characteristics of higher eukaryotes’ innate immune systems. We conclude that components of innate immunity existed in the common ancestor of plants and animals

Dataset Information

Escherichia coli mediated resistance of Entamoeba histolytica to oxidative stress is triggered by oxaloacetate.

Publications

Escherichia coli mediated resistance of Entamoeba histolytica to oxidative stress is triggered by oxaloacetate.

Similar Datasets

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