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. 2023 Nov 19;13(22):3574.
doi: 10.3390/ani13223574.

Artificial Pasture Grazing System Attenuates Lipopolysaccharide-Induced Gut Barrier Dysfunction, Liver Inflammation, and Metabolic Syndrome by Activating ALP-Dependent Keap1-Nrf2 Pathway

Qasim Ali  1 , Sen Ma  1   2   3 , Boshuai Liu  1 , Ahsan Mustafa  4 , Zhichang Wang  1   2   3 , Hao Sun  1   2   3 , Yalei Cui  1   2   3 , Defeng Li  1   2   3 , Yinghua Shi  1   2   3
Affiliations

Artificial Pasture Grazing System Attenuates Lipopolysaccharide-Induced Gut Barrier Dysfunction, Liver Inflammation, and Metabolic Syndrome by Activating ALP-Dependent Keap1-Nrf2 Pathway

Qasim Ali et al. Animals (Basel). .

Abstract

Geese can naturally obtain dietary fiber from pasture, which has anti-inflammatory and antioxidant properties. This study aimed to investigate the inhibitory impacts of pasture on ameliorating LPS-ROS-induced gut barrier dysfunction and liver inflammation in geese. Materials and methods. The lipopolysaccharides (LPS), alkaline phosphatase (ALP), reactive oxygen species (ROS), tight junction proteins, antioxidant enzymes, immunoglobulins, and metabolic syndrome were determined using ELISA kits. The Kelch-like-ECH-associated protein 1-Nuclear factor erythroid 2-related factor 2 (Keap1-Nrf2) and inflammatory cytokines were determined using the quantitative reverse transcription PCR (RT-qPCR) method. The intestinal morphology was examined using the Hematoxylin and Eosin (H&E) staining method in ileal tissues. Results. Pasture significantly influences nutrient absorption (p < 0.001) by ameliorating LPS and ROS-facilitated ileal permeability (p < 0.05) and systemic inflammation (p < 0.01). Herein, the gut permeability was paralleled by liver inflammation, which was significantly mimicked by ALP-dependent Nrf2 (p < 0.0001) and antioxidant enzyme activation (p < 0.05). Indeed, the correlation analysis of host markers signifies the importance of pasture in augmenting geese's health and production by averting gut and liver inflammation. Conclusions. Our results provide new insight into the mechanism of the pasture-induced ALP-dependent Nrf2 signaling pathway in limiting systemic inflammation in geese.

Keywords: Keap1-Nrf2; geese; intestinal alkaline phosphatase; lipopolysaccharides; pasture grazing; systemic inflammation.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
A commercial diet-dependent decline in ALP activity caused gut permeability and systemic inflammation. Protein levels of (A) ileal ALP, (B) ileal LPS, and (C) ileal ROS; Ileal tight junction proteins (D) ZO-1, (E) occludin, and (F) claudin measured by ELISA kits; mRNA levels of (G) ileal COX2, (H) ileal iNOS, (I) ileal IL-6, (J) ileal IL-1β, and (K) ileal TNF-α. IHF: in-house feeding system; AGF: artificial pasture grazing system. Data were presented as mean ± SD (n = 6). Data with * p < 0.05, ** p < 0.01, *** p < 0.001, **** p < 0.0001 were significant; ns: not significant (Student’s t-test, p < 0.05).
Figure 2
Figure 2
Commercial diet caused deterioration of nutrient absorption. VH: villus height; VW: villus width; DBV: distance between two villi; CD: crypt depth; IHF: in-house feeding system; AGF: artificial pasture grazing system.
Figure 3
Figure 3
Commercial diet caused deterioration of nutrient absorption by affecting the thickness of ileal muscular tonic and muscularis mucosa (50 µm). (A) Light micrograph of the wall of ileum tissues (hematoxylin and eosin). 1: outer layer of muscular tonic; 2: inner layer of muscular tonic; 3: outer layer of lamina muscularis mucosa; 4: ganglion of submucosal nerve plexus; 5: inner layer of lamina muscularis mucosa; 6: crypts; and 7: pillars of unstriated muscle cells (between crypts). (B) Comparison of the cecal membrane thickness of geese with different feeding systems (50 µm).
Figure 4
Figure 4
Commercial diet-dependent gut permeability is paralleled by liver inflammation. mRNA levels of (A) liver COX2, (B) liver iNOS, (C) liver IL-6, (D) liver IL-1β, and (E) liver TNF-α between the two feeding groups. Data were presented as mean ± SD (n = 6). Data with **** p < 0.0001 were significant (Student’s t-test, p < 0.05).
Figure 5
Figure 5
Long-term pasture intake caused redox signaling pathway activation. mRNA levels of (A) liver Keap1 and (B) liver Nrf2. (C–L) Protein levels of (C) liver HO-1, (D) liver GSH-Px, (E) liver GSR, (F) liver CAT, (G) liver T-SOD, (H) liver T-AOC, (I) liver MDA, (J) liver IgA, (K) liver IgG, and (L) liver IgM between the two feeding groups. Data were presented as mean ± SD (n = 6). Data with * p < 0.05, ** p < 0.01, *** p < 0.001, **** p < 0.0001 were significant; ns: not significant (Student’s t-test, p < 0.05).
Figure 6
Figure 6
Long-term high dietary fiber diet caused improved growth performance of geese. (A) ADFI and ADG measurement on 45 d, 60 d, and 90 d, and (B) ABW and FCR measurement on 45 d, 60 d, and 90 d from the two feeding groups. Data were presented as mean ± SD (n = 6). Data with *** p < 0.001, **** p < 0.0001 were significant (Student’s t-test, p < 0.05).
Figure 7
Figure 7
Long-term high dietary fiber diet caused improved metabolic profile of geese. Protein levels of (A) liver HDL-C, (B) liver LDL-C, (C) liver TG, (D) liver T-CHO, and (E) liver BUN between the two feeding groups. Data were presented as mean ± SD (n = 6). Data with * p < 0.05, ** p < 0.01, *** p < 0.001, **** p < 0.0001 were significant; ns: not significant (Student’s t-test, p < 0.05).
Figure 8
Figure 8
Pearson correlation analysis of ALP-dependent Keap1-Nrf2 signaling pathway-induced antioxidants with LPS/ROS-induced gut barrier dysfunctions, systemic inflammation, growth performance, and metabolic syndrome at 45 d (A), 60 d (B), and (C) 90 d. In the correlation heatmaps, the significant correlations were represented as (r > 0.52 or r < −0.52, p < 0.01). The size of the circle and its color intensity are proportional to the correlation values.
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