Lentinula edodes Cultured Extract and Rouxiella badensis subsp. acadiensis (Canan SV-53) Intake Alleviates Immune Deregulation and Inflammation by Modulating Signaling Pathways and Epigenetic Mechanisms

Roghayeh Shahbazi, Hamed Yasavoli‐Sharahi, Nawal Alsadi, Farzaneh Sharifzad, S. Fang, Cyrille Cuenin, Vincent Cahais, Felicia Fei‐Lei Chung, Zdenko Herceg, Chantal Matar
In: International Journal of Molecular Sciences · 2023 · vol. 24(19) , pp. 14610 · doi:10.3390/ijms241914610 · PMID:37834058 · W4387101807
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Abstract

Puberty is a critical developmental period of life characterized by marked physiological changes, including changes in the immune system and gut microbiota development. Exposure to inflammation induced by immune stressors during puberty has been found to stimulate central inflammation and lead to immune disturbance at distant sites from the gut; however, its enduring effects on gut immunity are not well explored. Therefore, in this study, we used a pubertal lipopolysaccharides (LPS)-induced inflammation mouse model to mimic pubertal exposure to inflammation and dysbiosis. We hypothesized that pubertal LPS-induced inflammation may cause long-term dysfunction in gut immunity by enduring dysregulation of inflammatory signaling and epigenetic changes, while prebiotic/probiotic intake may mitigate the gut immune system deregulation later in life. To this end, four-week-old female Balb/c mice were fed prebiotics/probiotics and exposed to LPS in the pubertal window. To better decipher the acute and enduring immunoprotective effects of biotic intake, we addressed the effect of treatment on interleukin (IL)-17 signaling related-cytokines and pathways. In addition, the effect of treatment on gut microbiota and epigenetic alterations, including changes in microRNA (miRNA) expression and DNA methylation, were studied. Our results revealed a significant dysregulation in selected cytokines, proteins, and miRNAs involved in key signaling pathways related to IL-17 production and function, including IL-17A and F, IL-6, IL-1β, transforming growth factor-β (TGF-β), signal transducer and activator of transcription-3 (STAT3), p-STAT3, forkhead box O1 (FOXO1), and miR-145 in the small intestine of adult mice challenged with LPS during puberty. In contrast, dietary interventions mitigated the lasting adverse effects of LPS on gut immune function, partly through epigenetic mechanisms. A DNA methylation analysis demonstrated that enduring changes in gut immunity in adult mice might be linked to differentially methylated genes, including Lpb, Rorc, Runx1, Il17ra, Rac1, Ccl5, and Il10, involved in Th17 cell differentiation and IL-17 production and signaling. In addition, prebiotic administration prevented LPS-induced changes in the gut microbiota in pubertal mice. Together, these results indicate that following a healthy diet rich in prebiotics and probiotics is an optimal strategy for programming immune system function in the critical developmental windows of life and controlling inflammation later in life.

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References (100)

SciLite annotations

treatment 175
lipopolysaccharide (LPS) Prebiotics LPS prebiotic LPS LPS LPS prebiotic compound probiotic bacterium Rouxiella badensis subsp conventional balanced diet LPS prebiotic AHCC (2 g/kg BW/day) LPS 1X sterile phosphate-buffered saline (PBS LPS control drinking water LPS water LPS prebiotic prebiotic + LPS LPS nutritional intervention LPS SV-53 (10 9 CFU/mL) control water control drinking water LPS water LPS probiotic + LPS LPS nutritional intervention LPS-prebiotic LPS-probiotic inhibitors LPS prebiotic/probiotic LPS AHCC + LPS LPS LPS LPS LPS AHCC + LPS LPS AHCC + LPS LPS LPS LPS prebiotic prebiotic LPS AHCC + LPS +115 more
host 91
mice Balb/c mice Balb/c mice mice Mice mice mice mice mice mice mice mice mice mice Mice Mice Mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice mice Mice mice mice mice mice Mice mice mice mice mice mice +31 more
sample-material 5
LPS LPS intestinal tissue tissue lysates pieces of ileum
state 49
lipopolysaccharide (LPS) interleukin (IL)-6 and IL-23 (miRNAs) LPS LPS prebiotic p-STAT prebiotic p-STAT3 p-STAT3 p-STAT3 p-STAT3 p-STAT3 LPS LPS p-STAT3 LPS LPS prebiotic LPS prebiotic LPS LPS prebiotic LPS prebiotic LPS-injected PI3K-Akt JAK-STAT LPS AHCC-fed Il17ra ) LPS LPS AHCC + LPS LPS LPS prebiotic p-STAT3 p-STAT3 LPS p-STAT3 p-STAT3 INF-γ LPS-exposed miR-145 knockdown LPS LPS p-STAT3
organisms 111
microbiota transgenic mice enterobacteriaceae bacterium c/sb65 microbiota mus sp. mus sp. mus sp. shiitake mushroom strain 323 bacteria stick insect bacteria stick insect intestinal metagenome segmented filamentous bacterium bacteria stick insect microbiota mus sp. enterobacteriaceae bacterium c/sb65 shiitake mushroom candidatus gribaldobacteria bacterium strain 323 enterobacteriaceae bacterium c/sb65 mus sp. mus sp. rodents rodents mus sp. mus sp. mus sp. escherichia coli o26:h11 mus sp. shiitake mushroom mus sp. mus sp. mus sp. transgenic mice horseradish transgenic mice mus sp. mus sp. mus sp. mus sp. mus sp. mus sp. mus sp. mus sp. mus sp. mus sp. mus sp. mus sp. mus sp. mus sp. mus sp. mus sp. microbiota tannerellaceae bacteroidaceae myroidaceae capsularis parabacteroides strain 341 +51 more
chemicals 14
glucosyllipopolysaccharide lipopolysaccharide long-chain carboxylate polyunsaturated fatty acid histone water water water amino oligosaccharide water bis-tris nitrogen polyphenol histone

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