Zearalenone induces immuno-compromised status via TOR/NF/κB pathway and aggravates the spread of Aeromonas hydrophila to grass carp gut (Ctenopharyngodon idella)

The occurrence of immuno-compromised status in animals with zearalenone (ZEA) exposure may be a critical contributor to associated mucosal (gastrointestinal tract) diseases. However, it is difficult to assess the associated risks with limited reference data. This study comprehensively discussed the...

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Main Authors: Hong-Yun Zhang, Ya-Li Wang, Xiao-Qiu Zhou, Wei-Dan Jiang, Pei Wu, Yang Liu, Lu Zhang, Hai-Feng Mi, Jun Jiang, Sheng-Yao Kuang, Ling Tang, Lin Feng
Format: Article
Language:English
Published: Elsevier 2021-12-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651321008988
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author Hong-Yun Zhang
Ya-Li Wang
Xiao-Qiu Zhou
Wei-Dan Jiang
Pei Wu
Yang Liu
Lu Zhang
Hai-Feng Mi
Jun Jiang
Sheng-Yao Kuang
Ling Tang
Lin Feng
author_facet Hong-Yun Zhang
Ya-Li Wang
Xiao-Qiu Zhou
Wei-Dan Jiang
Pei Wu
Yang Liu
Lu Zhang
Hai-Feng Mi
Jun Jiang
Sheng-Yao Kuang
Ling Tang
Lin Feng
author_sort Hong-Yun Zhang
collection DOAJ
description The occurrence of immuno-compromised status in animals with zearalenone (ZEA) exposure may be a critical contributor to associated mucosal (gastrointestinal tract) diseases. However, it is difficult to assess the associated risks with limited reference data. This study comprehensively discussed the effects of ZEA on intestinal immune components, cytokines and molecular mechanism of juvenile grass carp infected with Aeromonas hydrophila. Specifically, the fish were fed six graded levels of dietary ZEA (0–2507 μg kg−1 diet) for 70 d. The results pointed out that the average residual amount of ZEA in the intestines increased with dose level after ZEA feeding. We further performed an infection assay using A. hydrophila. After 14 d, ZEA groups increased enteritis morbidity rate compared with controls. The acid phosphatase (ACP), lysozyme (LZ) activities and immunoglobulin M (IgM) content were significantly decreased in three intestinal segments. Furthermore, ZEA could reduce the transcription of β-defensin-1, Hepcidin, liver expressed antimicrobial peptide 2A/2B (LEAP-2A/2B) and Mucin-2. We next confirmed the loss of these immune components accompanied by the invasion of the intestinal barrier by bacteria, as indicated by activation of the nuclear factor κB (NF-κB) and the expression of downstream cytokines. Notably, the phosphorylated target of rapamycin (TOR) plays an important role in regulating these genes, thus indicating a possible target caused by ZEA. In summary, the extensive inhibition of immune components by ZEA promotes the spread of pathogens, which may increase the possibility of intestinal mucosa exposure and the risk of transforming disease.
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spelling doaj.art-146d71edc37744dcae841c5ea443971f2022-12-21T22:08:41ZengElsevierEcotoxicology and Environmental Safety0147-65132021-12-01225112786Zearalenone induces immuno-compromised status via TOR/NF/κB pathway and aggravates the spread of Aeromonas hydrophila to grass carp gut (Ctenopharyngodon idella)Hong-Yun Zhang0Ya-Li Wang1Xiao-Qiu Zhou2Wei-Dan Jiang3Pei Wu4Yang Liu5Lu Zhang6Hai-Feng Mi7Jun Jiang8Sheng-Yao Kuang9Ling Tang10Lin Feng11Animal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China; Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; Key Laboratory for Animal Disease-Resistance Nutrition, Chengdu 611130, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China; Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; Key laboratory of Animal Disease-resistant Nutrition, Ministry of Education, Chengdu 611130, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China; Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; Key laboratory of Animal Disease-resistant Nutrition, Ministry of Education, Chengdu 611130, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China; Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; Key laboratory of Animal Disease-resistant Nutrition, Ministry of Education, Chengdu 611130, China; Key laboratory of Animal Disease-resistant Nutrition and Feed, Ministry of Agriculture and Rural Affairs, Chengdu 611130, ChinaTongwei Research Institute, Chengdu 600438, ChinaTongwei Research Institute, Chengdu 600438, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, ChinaAnimal Nutrition Institute, Sichuan Academy of Animal Science, Chengdu 610066, ChinaAnimal Nutrition Institute, Sichuan Academy of Animal Science, Chengdu 610066, ChinaAnimal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, China; Fish Nutrition and Safety Production University Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; Key Laboratory for Animal Disease-Resistance Nutrition, Chengdu 611130, China; Correspondence to: Animal Nutrition Institute, Sichuan Agricultural University, Chengdu 611130, Sichuan, China.The occurrence of immuno-compromised status in animals with zearalenone (ZEA) exposure may be a critical contributor to associated mucosal (gastrointestinal tract) diseases. However, it is difficult to assess the associated risks with limited reference data. This study comprehensively discussed the effects of ZEA on intestinal immune components, cytokines and molecular mechanism of juvenile grass carp infected with Aeromonas hydrophila. Specifically, the fish were fed six graded levels of dietary ZEA (0–2507 μg kg−1 diet) for 70 d. The results pointed out that the average residual amount of ZEA in the intestines increased with dose level after ZEA feeding. We further performed an infection assay using A. hydrophila. After 14 d, ZEA groups increased enteritis morbidity rate compared with controls. The acid phosphatase (ACP), lysozyme (LZ) activities and immunoglobulin M (IgM) content were significantly decreased in three intestinal segments. Furthermore, ZEA could reduce the transcription of β-defensin-1, Hepcidin, liver expressed antimicrobial peptide 2A/2B (LEAP-2A/2B) and Mucin-2. We next confirmed the loss of these immune components accompanied by the invasion of the intestinal barrier by bacteria, as indicated by activation of the nuclear factor κB (NF-κB) and the expression of downstream cytokines. Notably, the phosphorylated target of rapamycin (TOR) plays an important role in regulating these genes, thus indicating a possible target caused by ZEA. In summary, the extensive inhibition of immune components by ZEA promotes the spread of pathogens, which may increase the possibility of intestinal mucosa exposure and the risk of transforming disease.http://www.sciencedirect.com/science/article/pii/S0147651321008988ZearalenoneImmunePathogen infectionMucus layerGrass carp
spellingShingle Hong-Yun Zhang
Ya-Li Wang
Xiao-Qiu Zhou
Wei-Dan Jiang
Pei Wu
Yang Liu
Lu Zhang
Hai-Feng Mi
Jun Jiang
Sheng-Yao Kuang
Ling Tang
Lin Feng
Zearalenone induces immuno-compromised status via TOR/NF/κB pathway and aggravates the spread of Aeromonas hydrophila to grass carp gut (Ctenopharyngodon idella)
Ecotoxicology and Environmental Safety
Zearalenone
Immune
Pathogen infection
Mucus layer
Grass carp
title Zearalenone induces immuno-compromised status via TOR/NF/κB pathway and aggravates the spread of Aeromonas hydrophila to grass carp gut (Ctenopharyngodon idella)
title_full Zearalenone induces immuno-compromised status via TOR/NF/κB pathway and aggravates the spread of Aeromonas hydrophila to grass carp gut (Ctenopharyngodon idella)
title_fullStr Zearalenone induces immuno-compromised status via TOR/NF/κB pathway and aggravates the spread of Aeromonas hydrophila to grass carp gut (Ctenopharyngodon idella)
title_full_unstemmed Zearalenone induces immuno-compromised status via TOR/NF/κB pathway and aggravates the spread of Aeromonas hydrophila to grass carp gut (Ctenopharyngodon idella)
title_short Zearalenone induces immuno-compromised status via TOR/NF/κB pathway and aggravates the spread of Aeromonas hydrophila to grass carp gut (Ctenopharyngodon idella)
title_sort zearalenone induces immuno compromised status via tor nf κb pathway and aggravates the spread of aeromonas hydrophila to grass carp gut ctenopharyngodon idella
topic Zearalenone
Immune
Pathogen infection
Mucus layer
Grass carp
url http://www.sciencedirect.com/science/article/pii/S0147651321008988
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