Evaluating protective effects of botanicals under inflammation and oxidative stress in chicken apical-out enteroids

ABSTRACT: Botanicals (BOTs) are well known for their anti-inflammatory and antioxidant activities. They have been widely used as feed additives to reduce inflammation and improve intestinal functions in agricultural animals. However, the effects of BOTs on chicken intestinal epithelial functions are...

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Main Authors: Federico Ghiselli, Liang-en Yu, Andrea Piva, Ester Grilli, Yihang Li
Format: Article
Language:English
Published: Elsevier 2023-08-01
Series:Poultry Science
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0032579123003401
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author Federico Ghiselli
Liang-en Yu
Andrea Piva
Ester Grilli
Yihang Li
author_facet Federico Ghiselli
Liang-en Yu
Andrea Piva
Ester Grilli
Yihang Li
author_sort Federico Ghiselli
collection DOAJ
description ABSTRACT: Botanicals (BOTs) are well known for their anti-inflammatory and antioxidant activities. They have been widely used as feed additives to reduce inflammation and improve intestinal functions in agricultural animals. However, the effects of BOTs on chicken intestinal epithelial functions are not fully understood. The 3D apical-out chicken enteroids recapitulate the intestinal tissue, and allow convenient access to the luminal surface, thus serving as a suitable model for investigating gut functions. The aim of this study was to identify the roles of BOTs in protecting the intestinal epithelium in chicken enteroids under challenging conditions. Apical-out enteroids were isolated from the small intestines of 18 days-old chicken embryos. Lipopolysaccharide (LPS, 10 µg/mL) and menadione (400 µM) challenges were performed in the media with or without BOTs. Paracellular Fluorescein isothiocyanate–dextran 4kD (FD4) permeability, inflammatory cytokine gene expression, and reactive oxygen species (ROS) generation were analyzed post-BOTs and challenges treatments. Statistical analysis was performed using one-way ANOVA and post hoc multiple comparisons among treatments. The results showed that the LPS challenge for 24 h induced a 50% increase in FD4 permeability compared with nontreated control; thymol, thyme essential oil, and phenol-rich extract significantly (P < 0.02) reduced FD4 permeability by 25%, 41%, and 48% respectively, in comparison with LPS treatment. Moreover, the gene expression of inflammatory cytokines was upregulated, tight junction proteins and defensins were downregulated (P < 0.05) after 6 h of LPS treatment, while these BOTs treatments significantly restored the LPS-induced gene expression alterations (P < 0.05). Menadione oxidative challenge for 1 h significantly increased the ROS level compared with unchallenged control. Enteroids treated with thymol and thyme essential oils showed 30% reduced ROS levels, while the phenol-rich extract reduced them by 60%, in comparison with the challenged group (P < 0.0001). These data confirmed the role of BOTs in supporting the barrier function and reducing the disruptive effects of inflammation and oxidation in the chicken intestine.
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spelling doaj.art-ac4cadff2ac4473aa08e1c18bad18e492023-07-29T04:34:26ZengElsevierPoultry Science0032-57912023-08-011028102821Evaluating protective effects of botanicals under inflammation and oxidative stress in chicken apical-out enteroidsFederico Ghiselli0Liang-en Yu1Andrea Piva2Ester Grilli3Yihang Li4Department of Veterinary Medical Sciences, University of Bologna, Ozzano dell'Emilia, ItalyDepartment of Animal and Food Sciences, University of Delaware, Newark, DE 19711, USADepartment of Veterinary Medical Sciences, University of Bologna, Ozzano dell'Emilia, Italy; Vetagro S.p.A. - Via Ignazio Porro, Reggio Emilia (RE), ItalyDepartment of Veterinary Medical Sciences, University of Bologna, Ozzano dell'Emilia, Italy; Vetagro Inc., Chicago, IL 60603, USADepartment of Animal and Food Sciences, University of Delaware, Newark, DE 19711, USA; Corresponding author:ABSTRACT: Botanicals (BOTs) are well known for their anti-inflammatory and antioxidant activities. They have been widely used as feed additives to reduce inflammation and improve intestinal functions in agricultural animals. However, the effects of BOTs on chicken intestinal epithelial functions are not fully understood. The 3D apical-out chicken enteroids recapitulate the intestinal tissue, and allow convenient access to the luminal surface, thus serving as a suitable model for investigating gut functions. The aim of this study was to identify the roles of BOTs in protecting the intestinal epithelium in chicken enteroids under challenging conditions. Apical-out enteroids were isolated from the small intestines of 18 days-old chicken embryos. Lipopolysaccharide (LPS, 10 µg/mL) and menadione (400 µM) challenges were performed in the media with or without BOTs. Paracellular Fluorescein isothiocyanate–dextran 4kD (FD4) permeability, inflammatory cytokine gene expression, and reactive oxygen species (ROS) generation were analyzed post-BOTs and challenges treatments. Statistical analysis was performed using one-way ANOVA and post hoc multiple comparisons among treatments. The results showed that the LPS challenge for 24 h induced a 50% increase in FD4 permeability compared with nontreated control; thymol, thyme essential oil, and phenol-rich extract significantly (P < 0.02) reduced FD4 permeability by 25%, 41%, and 48% respectively, in comparison with LPS treatment. Moreover, the gene expression of inflammatory cytokines was upregulated, tight junction proteins and defensins were downregulated (P < 0.05) after 6 h of LPS treatment, while these BOTs treatments significantly restored the LPS-induced gene expression alterations (P < 0.05). Menadione oxidative challenge for 1 h significantly increased the ROS level compared with unchallenged control. Enteroids treated with thymol and thyme essential oils showed 30% reduced ROS levels, while the phenol-rich extract reduced them by 60%, in comparison with the challenged group (P < 0.0001). These data confirmed the role of BOTs in supporting the barrier function and reducing the disruptive effects of inflammation and oxidation in the chicken intestine.http://www.sciencedirect.com/science/article/pii/S0032579123003401chicken enteroidsgut barrierbotanicalsoxidative stressinflammation
spellingShingle Federico Ghiselli
Liang-en Yu
Andrea Piva
Ester Grilli
Yihang Li
Evaluating protective effects of botanicals under inflammation and oxidative stress in chicken apical-out enteroids
Poultry Science
chicken enteroids
gut barrier
botanicals
oxidative stress
inflammation
title Evaluating protective effects of botanicals under inflammation and oxidative stress in chicken apical-out enteroids
title_full Evaluating protective effects of botanicals under inflammation and oxidative stress in chicken apical-out enteroids
title_fullStr Evaluating protective effects of botanicals under inflammation and oxidative stress in chicken apical-out enteroids
title_full_unstemmed Evaluating protective effects of botanicals under inflammation and oxidative stress in chicken apical-out enteroids
title_short Evaluating protective effects of botanicals under inflammation and oxidative stress in chicken apical-out enteroids
title_sort evaluating protective effects of botanicals under inflammation and oxidative stress in chicken apical out enteroids
topic chicken enteroids
gut barrier
botanicals
oxidative stress
inflammation
url http://www.sciencedirect.com/science/article/pii/S0032579123003401
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AT estergrilli evaluatingprotectiveeffectsofbotanicalsunderinflammationandoxidativestressinchickenapicaloutenteroids
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