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. 2023 Oct 17;12(20):3800.
doi: 10.3390/foods12203800.

Inhibition of IEC-6 Cell Proliferation and the Mechanism of Ulcerative Colitis in C57BL/6 Mice by Dandelion Root Polysaccharides

Shengkun Yan  1   2 , Lijun Yin  1 , Rong Dong  2
Affiliations

Inhibition of IEC-6 Cell Proliferation and the Mechanism of Ulcerative Colitis in C57BL/6 Mice by Dandelion Root Polysaccharides

Shengkun Yan et al. Foods. .

Abstract

An exploration was conducted on the potential therapeutic properties of dandelion polysaccharide (DP) in addressing 3% dextran sodium sulfate (DSS)-induced ulcerative colitis (UC) in murine models. Subsequent assessments focused on DP's influence on inflammation, oxidative stress, and ferroptosis in IEC-6 cells damaged by H2O2. Results highlighted the efficacy of DP in mitigating weight loss, improving disease activity index scores, normalizing colon length, and alleviating histological abnormalities in the affected mice. DP repaired colonic mitochondrial damage by enhancing iron transport and inhibited iron death in colonic cells. Moreover, DP played a pivotal role in enhancing the antioxidant potential. This was evident from the increased expression levels of Nrf2, HO-1, NQO-1, and GSH, coupled with a decrease in MDA and 4-HNE markers in the UC-afflicted mice. Concurrently, DP manifested inhibitory effects on MPO activation and transcription levels of inflammatory mediators such as IL-1β, IL-6, TNF-α, and iNOS. An upsurge in the expression of occludin and ZO-1 was also observed. Restoration of intestinal tightness resulted in decreased serum LPS and LDH levels. Thereafter, administration of DP by gavage increased fecal flora diversity and relative abundance of probiotics in UC mice. Analysis of metabolites indicated that DP counteracted metabolic disturbances and augmented the levels of short-chain fatty acids in ulcerative colitis-affected mice. In vitro studies underscored the role of DP in triggering Nrf2 activation, which in turn exhibited anti-inflammatory, antioxidant, and anti-ferroptotic properties. Summarily, DP's capacity to activate Nrf2 contributes to the suppression of ferroptotic processes in intestinal epithelial cells of UC-affected mice, enhancing the intestinal barrier's integrity. Beyond that, DP possesses the ability to modulate the gut microbiome, rectify metabolic imbalances, rejuvenate short-chain fatty acid levels, and bolster the intestinal barrier as a therapeutic approach to UC.

Keywords: Nrf2; dandelion root polysaccharides; ferroptosis; gut flora; metabolites; ulcerative colitis.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Assessment of enteritis manifestations in murine models. Panel (A) displays a graphical representation of the study layout. Panels (B,C) depict the colon lengths observed in mice. Panel (D) showcases the calculated Disease Activity Index (DAI) scores across experimental cohorts. Panel (E) presents the impact of dandelion root polysaccharide (DP) on murine body mass trends. Panel (F) reveals microscopic visuals of colon specimens post-hematoxylin-eosin (H&E) staining procedure. The computation for DAI was anchored on criteria like body mass fluctuations, fecal consistency, and observable blood in feces. Symbols * p < 0.05, ** p < 0.01, and *** p < 0.001 signify statistical deviations from the control set. Markers # p < 0.05, ## p < 0.01 indicate significant variations from the model set.
Figure 2
Figure 2
Inhibitory effect of DP on iron death in colonic epithelial cells of UC mice. (A): Scanning electron microscope to observe the state of Colonic tissue. (B,C): Images of colon tissue following TUNEL staining. (D): Determination of iron content in colonic tissue. (E,F): The relative protein levels of GPX4, SLC7A11, and TFR1. * p ˂ 0.05, ** p < 0.01 and *** p ˂ 0.001, compared with control group. # p ˂ 0.05, ## p ˂ 0.01, and ### p ˂ 0.001, compared with the model group.
Figure 3
Figure 3
Modulation of Nrf2 anti-lipid peroxidation signaling activation by DP in the colon of UC mice. (A,B): Immunohistochemistry for MPO. (C–E): Elisa’s detection of 4-HNE, MDA, and GSH. (F,G): The relative protein levels of Nrf2, HO-1, and NQO-1. * p ˂ 0.05, ** p < 0.01 and *** p ˂ 0.001, compared with the control group. # p ˂ 0.05, ## p ˂ 0.01, compared with the model group.
Figure 4
Figure 4
Effect of DP on the intestinal barrier as well as inflammation in UC mice. (A,B): ELISA detection of LPS and LDH content. (C,D): Immunofluorescence detection of occludin and ZO-1. (E): Relative mRNA of TNF-α, iNOS, IL-6 and IL-1β. * p ˂ 0.05 and ** p ˂ 0.001, compared with control group. # p ˂ 0.05, compared with the model group.
Figure 5
Figure 5
DP regulates intestinal flora regulating UC. (A): Beta diversity analysis sample for PCoA analysis of phylum (A) and genus (B). (C): The abundance of intestinal flora at the phylum level. (D): The abundance of intestinal flora at the genus level. (E): Abundance of Helicobacteraceae, Romboutsia, Lactobacillus, Odoribacter, Bacteroides, and Lachnoclostridium in each group at the genus level. * p ˂ 0.05, compared with control group. # p ˂ 0.05, ## p < 0.01, compared with the model group.
Figure 6
Figure 6
Effects of DP on short-chain fatty acids. (A): Metabolites 2D PCA. (B): Metabolites 3D PCA. (C): The effects of DP on short-chain fatty acids: hydroxypropionic acid, pseudolaric acid, butonate, 3-hydroxyisobutyric acid, 3-hydroxybutyrate, and valproic acid. * p ˂ 0.05, compared with control group. # p ˂ 0.05, compared with the model group.
Figure 7
Figure 7
Anti-inflammatory and antioxidant effects of DP on H2O2-induced inflammation model of IEC-6 cells. (A): CCK-8 detects the proliferation activity of IEC-6. (B,C): Effect of DP on IEC-6 apoptosis. (D–F): Elisa’s detection of 4-HNE, MDA, and GSH. (G): Relative mRNA of IL-1β, IL-6, TNF-α, and iNOS. (H,I): The relative protein levels of Nrf2, HO-1, and NQO-1. * p ˂ 0.05, ** p ˂ 0.01, and *** p ˂ 0.0001, compared with the control group. # p ˂ 0.05, ## p ˂ 0.01, and ### p ˂ 0.0001, compared with the model group.
Figure 8
Figure 8
The death mechanism of IEC-6 cells induced by DP on H2O2. (A): Scanning electron microscope to observe the state of IEC-6 cells. (B): Determination of iron content in IEC-6 cells. (C,D): The relative protein levels of GPX4, SLC7A11, and TFR1. ** p < 0.01 and *** p ˂ 0.001, compared with control group. # p ˂ 0.05, ## p ˂ 0.01, compared with model group.
Figure 9
Figure 9
Anion exchange chromatogram of the crude DP on a DEAE sepharose fast-flow ion exchange column.
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