Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (22): 4771-4785.doi: 10.3864/j.issn.0578-1752.2025.22.016

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles     Next Articles

Study on the Antioxidant Function and Mechanism of 18β-glycyrrhetinic Acid Using Porcine Intestinal Organoid Model

LI RuiTong(), CHEN QingMei, XU JianFang, ZHANG JunMin, SI Wei(), ZHANG TieYing()   

  1. State Key Laboratory of Animal Nutrition and Feeding/Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193
  • Received:2025-03-28 Accepted:2025-06-27 Online:2025-11-16 Published:2025-11-21
  • Contact: SI Wei, ZHANG TieYing

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Abstract:

【Background】Oxidative stress is a key factor compromising intestinal health and impeding the growth and development of pigs. Consequently, the identification and development of natural and effective antioxidant compounds are of great significance for enhancing animal health and production efficiency. 18β-Glycyrrhetinic acid (GA), a pentacyclic triterpenoid extracted from Glycyrrhiza spp., has been recognized for its antioxidant activity. 【Objective】This study aimed to establish an oxidative stress injury model based on porcine intestinal organoids to assess the antioxidant efficacy of GA and to explore its potential underlying mechanisms. The findings were intended to provide a theoretical foundation for the application of GA as a functional antioxidant additive in livestock and poultry nutrition. 【Method】Intestinal crypts were isolated and collected from the jejunal tissues of piglets and used to construct porcine intestinal organoids via a three-dimensional culture system. The structural and functional integrity of the organoids was confirmed by immunofluorescence staining for intestinal epithelial stem cell and differentiation markers, including LGR5, β-catenin, Ki67, PCNA, c-Myc, CDX2, and lysozyme, indicating the presence of typical intestinal epithelial lineages. After 48 hours of passaging, organoids were treated with hydrogen peroxide (H2O2) at concentrations of 0, 100, 250, 500, 750, 1 000, 1 500, and 2 000 μmol·L-1 for three days to induce oxidative stress, respectively. The optimal H2O2 concentration for model establishment was determined through comprehensive evaluation of morphological parameters (budding rate, branching coefficient, and bud condition), cellular proliferation activity (EdU incorporation and Ki67 expression), intracellular reactive oxygen species (ROS) levels (detected by fluorescent probes), and expression of key genes in the Wnt/β-catenin signaling pathway (Lgr5, C-myc, Cyclin D1, β-catenin, PCNA, and AXIN2). Subsequently, GA at concentrations of 10, 50, and 100 μmol·L-1 was applied to the oxidative stress model to assess its protective effect. The antioxidant capacity and underlying mechanism of GA were investigated by analyzing organoid morphology, proliferation activity, intracellular ROS accumulation, and expression of representative proteins associated with the Wnt/β-catenin signaling pathway (β-catenin, PCNA, LGR5, and CDX2). 【Result】After 48 hours of passaging, treatment of porcine intestinal organoids with 1 mmol·L-1 H2O2 for three days successfully established a stable oxidative stress injury model. This was demonstrated by a significant decrease in the organoid budding rate and branching coefficient, accompanied by a marked reduction in the proportion of EdU-positive cells and Ki67 expression. Moreover, oxidative stress induced activation of the Wnt/β-catenin signaling pathway, as evidenced by significant upregulation of C-myc expression. Under normal culture conditions, GA at concentrations of 10, 50, and 100 μmol·L-1 exerted no adverse effects on organoid growth. However, under oxidative stress conditions, 100 μmol·L-1 GA exhibited the most pronounced protective effect, significantly enhancing the budding rate and branching coefficient, and promoting cell proliferation as indicated by increased EdU-positive cell proportion and elevated Ki67 expression. Additionally, GA treatment effectively reduced ROS accumulation and inhibited the activation of the Wnt/β-catenin pathway, demonstrated by the downregulation of β-catenin, PCNA, and LGR5 protein expression levels. 【Conclusion】In this study, a porcine intestinal organoid model of oxidative stress was successfully established. Based on this model, the protective role of GA against oxidative damage in organoids was confirmed, and its underlying mechanism was preliminarily elucidated. GA exerted notable antioxidant activity by improving organoid morphological development, promoting cellular proliferation, reducing intracellular ROS levels, and downregulating the Wnt/β-catenin signaling pathway. These findings laid a theoretical foundation for the functional development and practical application of GA in the nutritional regulation and health management of livestock and poultry.

Key words: 18β-glycyrrhetinic acid, porcine intestinal organoid, oxidative stress

Table 1

Antibodies used in this study"

抗体 Antibody 货号 Art. No. 公司 Company
anti-β-catenin 8480S Cell Signaling Technology
anti-CDX2 12306S Cell Signaling Technology
anti-Ki67 9449S Cell Signaling Technology
anti-C-MyC 5605S Cell Signaling Technology
anti-PCNA 13110S Cell Signaling Technology
anti-LGR5 PA5-87974 Invitrogen
anti-Lysozyme MA5-32154 Invitrogen
anti-β-actin ab8226 Abcam
Goat Anti-Mouse IgG H&L (Alexa Fluor® 594) ab150116 Abcam
Multi-rAb CoraLite® Plus 594-Goat Anti-Rabbit RGAR004 Proteintech
HRP-Goat Anti-Rabbit IgG (H+L) HX2031 Huaxingbochuang
HRP-Goat Anti-Mouse IgG(H+L) HX2032 Huaxingbochuang

Table 2

Primer sequences for RT-qPCR analysis"

基因 Gene 序列号 Accession number 引物序列 Primer sequence (5' to 3')
β-actin XM_021086047.1 F: CAGGTCATCACCATCGGCAACG
R: GACAGCACCGTGTTGGCGTAGAGGT
Lgr5 NM_001315762.1 F: GCTGGCTGCCGTGGATGC
R: AGCAGGGCGCAGAGGACAAG
C-myc NM_001005154.1 F: CGGACACGGAGGAGAATGAC
R: GCTGCGTTTCAGCTCGTTTC
Cyclin D1 XM_021082686.1 F: GCAGAAGTGCGAGGAGGAGGTCTT
R: CGGATGGAGTTGTCGGTGTAGATGC
β-catenin NM_214367.1 F: AAGCCGAGTACTGAAGGTGC
R: AAAGCTTGCATTCCACCAGC
PCNA NM_001291925.1 F: GCAGAGCATGGACTCGTCTC
R: TTGGACATGCTGGTGAGGTT
AXIN2 XM_021066739.1 F: CTACTCCAAGTGCAAGAGCCA
R: GTGCTTTGGGCACCAAACTG

Fig. 1

The process of organoid formation from a single crypt unit (scale bar: 200 μm)"

Fig. 2

Immunofluorescence staining of various intestinal epithelial cell markers in porcine intestinal organoids A: Intestinal stem cell and Wnt/β-catenin pathway markers, including LGR5 (red), β-catenin (green), and DAPI (blue); B: Proliferation markers, including Ki67 (red), PCNA (red), C-Myc (red), and DAPI (blue); C: Differentiation and maturation markers, including CDX2 (red), Lysozyme (red), and DAPI (blue)"

Fig. 3

Effects of hydrogen peroxide on the growth status of porcine intestinal organoids A: Morphological changes of porcine intestinal organoids (scale bar: 400 μm); B: Budding efficiency of porcine intestinal organoids; C: Budding coefficient of porcine intestinal organoids; D: Bud distribution of porcine intestinal organoids. Data are presented as mean ± SD. Different lowercase letters indicate significant differences at P<0.05. No letter indicates no difference between groups. The same as below"

Fig. 4

Oxidative damage of porcine intestinal organoids induced by hydrogen peroxide A: Immunofluorescence staining of porcine intestinal organoids (EdU and Ki67 in red fluorescence, ROS in green fluorescence, DAPI in blue fluorescence; scale bar: 200 μm); B: Gene expression level of Lgr5; C: Gene expression level of C-myC; D: Gene expression level of Cyclin D1; E: Gene expression level of β-catenin; F: Gene expression level of PCNA; G: Gene expression level of AXIN2"

Fig. 5

Effects of 18β-glycyrrhetinic acid on the growth status of porcine intestinal organoids A: Morphological changes of porcine intestinal organoids; B: Budding efficiency of porcine intestinal organoids; C: Budding coefficient of porcine intestinal organoids; D: Bud condition of porcine intestinal organoids"

Fig. 6

Effect of 18β-glycyrrhetinic acid on the growth state of porcine intestinal organoids under oxidative stress A: Morphological changes of porcine intestinal organoids (scale bar: 400 μm); B: Budding efficiency of porcine intestinal organoids; C: Budding coefficient of porcine intestinal organoids; D: Budding condition of porcine intestinal organoids; E: Bud distribution of porcine intestinal organoids."

Fig. 7

Effects of 18β-glycyrrhetinic acid on alleviating oxidative stress injury in porcine intestinal organoids A: Immunofluorescence staining of porcine intestinal organoids (EdU and Ki67 in red fluorescence, ROS in green fluorescence, DAPI in blue fluorescence; scale bar: 200 μm); B: Western blot analysis of key proteins in the Wnt/β-catenin signaling pathway; C: Expression level of β-catenin protein; D: Expression level of PCNA protein; E: Expression level of LGR5 protein; F: Expression level of CDX2 protein"

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