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. 2023 Feb;103(3):1273-1282.
doi: 10.1002/jsfa.12221. Epub 2022 Sep 26.

Emodin modulates gut microbial community and triggers intestinal immunity

Humphrey A Mabwi #  1   2   3   4 , Hee Ju Lee #  1 , Emmanuel Hitayezu  1 , Intan Rizki Mauliasari  1 , Cheol-Ho Pan  1   4 , Kilaza Samson Mwaikono  5 , Erick V G Komba  3 , Choong-Gu Lee  1   4 , Kwang Hyun Cha  1
Affiliations

Emodin modulates gut microbial community and triggers intestinal immunity

Humphrey A Mabwi et al. J Sci Food Agric. 2023 Feb.

Abstract

Background: The gut microbiota (GM) plays an important role in human health and is being investigated as a possible target for new therapies. Although there are many studies showing that emodin can improve host health, emodin-GM studies are scarce. Here, the effects of emodin on the GM were investigated in vitro and in vivo.

Results: In vitro single bacteria cultivation showed that emodin stimulated the growth of beneficial bacteria Akkermansia, Clostridium, Roseburia, and Ruminococcus but inhibited major gut enterotypes (Bacteroides and Prevotella). Microbial community analysis from a synthetic gut microbiome model through co-culture indicated the consistent GM change by emodin. Interestingly, emodin stimulated Clostridium and Ruminococcus (which are related to Roseburia and Faecalibacterium) in a mice experiment and induced anti-inflammatory immune cells, which may correlate with its impact on specific gut bacteria.

Conclusion: Emodin (i) showed similar GM changes in monoculture, co-culture, and in an in vivo mice experiment and (ii) simulated regulatory T-cell immune responses in vivo. This suggest that emodin may be used to modulate the GM and improve health. © 2022 The Authors. Journal of The Science of Food and Agriculture published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Keywords: MiSeq; T regulatory cell; emodin; gut microbiome.

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Conflict of interest statement

The authors declare no competing financial interest.

Figures

Figure 1
Figure 1
Effects of emodin on single‐bacteria cultures, as determined by heatmap analysis. (A) Emodin and other six anthraquinones chemicals were added to the culture of each bacterium at 100 μmol L−1, after which (B) growth was measured at OD600 nm. The text colors indicate bacteria in the same phyla, as follows: green (Actinobacteria), black (Proteobacteria), purple (Verrumicrobia), blue (Firmicutes), and red (Bacteroidetes).
Figure 2
Figure 2
Effects of emodin on synthetic gut‐microbial communities. The mucosal environment was simulated by adding solid mucin–agar gel to the bottom of culture tubes. (A) A β‐diversity non‐metric multidimensional scaling plot of microbial community where bacteria distinctively clustered based on mucosal environment simulation and emodin treatment. (B) Linear discriminant analysis (LDA) showing specific microbiota to efficiently colonize the mucosal solid part, whereas others dominated in the luminal liquid part.
Figure 3
Figure 3
Bar graphs showing the effects of emodin on relative bacterial abundance in the (A) mucosal and (B) luminal part through a synthetic gut microbial ecosystem. Emodin significantly increased the relative abundance of beneficial microbes (Faecalibacterium and Roseburia) and inhibited inflammation‐related microbes (Bacteroides and Prevotella) and opportunistic gut pathogen (Enterococcus). Statistical significance was determined using Student's t‐test (n = 4/group; P < 0.05).
Figure 4
Figure 4
(A) Mice cecum microbial‐community profiling. β‐diversity index; ordination method: NMDS; distance method: Bray–Curtis distance matrix; statistical method: permutational multivariate analysis of variance. Each dot represents a mouse, n ≥ 6/group. (B) SparCC network plot of bacterial interactions following emodin treatment. Nodes represent detected phylotypes (OTU clustered at 97% similarity) and shows fraction of increase/decrease where emodin increased Clostridium and Ruminococcus and decreased Bacteroides and Prevotella. Linear discriminant analysis (LDA) effect size analysis. (C) Bar chart indicating the log‐transformed LDA scores between groups and (D) cladogram indicating the phylogenetic relationships of bacteria taxa between emodin and control group (n ≥ 6/group).
Figure 5
Figure 5
Increased cellular expression of forkhead box P3 transcription factor (Foxp3), Helios, retinoic acid‐related orphan receptor (RORgt), and inducible co‐stimulatory molecule (ICOS) in mice treated with emodin. Colon lamina propria (cLP) lymphocytes were isolated and the expression levels of Foxp3, Helios, RORgt, and ICOS were analyzed after intracellular staining. (A, C, E, G) Representative dot‐plots of the percentages of cells expressing Foxp3, Helios, RORgt, and ICOS among the CD4 cell population in individual mice. (B, D, F, H) Fluorescence‐activated cell sorting plots of CD4, Foxp3, Helios, and ICOS expression in immune cells in the cLP. The numbers in the quadrants represent cell frequencies, and the circles in the graph plots represent individual mice corresponding to each parameter (n ≥ 6 mice).
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