Chronic exposure to zearalenone induces intestinal inflammation and oxidative injury in adult Drosophila melanogaster midgut

In the past decade, mycotoxin zearalenone (ZEN)-induced gastrointestinal adverse effects have been increasingly attracting worldwide attention. This study aimed to determine the gastrointestinal adverse effects of ZEN in Drosophila melanogaster (D. melanogaster) and reveal possible mechanisms of act...

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Main Authors: Zhi Chen, Fen Wang, Wen Zhang, Shuangshuang Zhou, Di Wen, Ren Mu
Format: Article
Language:English
Published: Elsevier 2023-02-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651323000593
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author Zhi Chen
Fen Wang
Wen Zhang
Shuangshuang Zhou
Di Wen
Ren Mu
author_facet Zhi Chen
Fen Wang
Wen Zhang
Shuangshuang Zhou
Di Wen
Ren Mu
author_sort Zhi Chen
collection DOAJ
description In the past decade, mycotoxin zearalenone (ZEN)-induced gastrointestinal adverse effects have been increasingly attracting worldwide attention. This study aimed to determine the gastrointestinal adverse effects of ZEN in Drosophila melanogaster (D. melanogaster) and reveal possible mechanisms of action of ZEN in insects. Here, chronic exposure of D. melanogaster to ZEN killed flies in a dose-dependent manner (2–20 µM). ZEN (20 µM) decreased the survival rates and climbing ability of flies, and activated immune deficiency-mediated intestinal immunity in midgut, leading to the production of antimicrobial peptides. Meanwhile, ZEN exposure induced morphological alteration of adult midgut. Further study suggested that high levels of oxidative stress was observed in ZEN-treated midgut due to the imbalance between the production of reactive oxygen species and the expression and activities of cellular antioxidant enzyme, including superoxide dismutase and catalase. ZEN-induced oxidative stress then caused cell death, impaired gut barrier function and increased gut permeability, leading to oxidative injury in midgut. Subsequently, ZEN-induce midgut injury further disrupted intestinal stem cell (ISC) homeostasis, stimulating ISC proliferation and tissue regeneration, but did not alter cell fate specification of ISC. Additionally, activation of Jun N-terminal kinase pathway was involved in ZEN-induced oxidative injury and tissue regeneration in midgut. Antioxidant vitamin E alleviated ZEN-induced oxidative injury to midgut epithelium. Collectively, this study provided additional evidences for ZEN-induced gastrointestinal adverse effects from an invertebrate model, extended our understanding of the mechanisms mediating mycotoxin toxicity in organisms.
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spelling doaj.art-1f52962f5085470b9fe4a904adbd20d22023-02-02T04:47:06ZengElsevierEcotoxicology and Environmental Safety0147-65132023-02-01251114555Chronic exposure to zearalenone induces intestinal inflammation and oxidative injury in adult Drosophila melanogaster midgutZhi Chen0Fen Wang1Wen Zhang2Shuangshuang Zhou3Di Wen4Ren Mu5Corresponding authors.; College of Biological Science and Agriculture, Qiannan Normal University for Nationalities, Duyun 558000, ChinaCollege of Biological Science and Agriculture, Qiannan Normal University for Nationalities, Duyun 558000, ChinaCollege of Biological Science and Agriculture, Qiannan Normal University for Nationalities, Duyun 558000, ChinaCollege of Biological Science and Agriculture, Qiannan Normal University for Nationalities, Duyun 558000, ChinaCorresponding authors.; College of Biological Science and Agriculture, Qiannan Normal University for Nationalities, Duyun 558000, ChinaCorresponding authors.; College of Biological Science and Agriculture, Qiannan Normal University for Nationalities, Duyun 558000, ChinaIn the past decade, mycotoxin zearalenone (ZEN)-induced gastrointestinal adverse effects have been increasingly attracting worldwide attention. This study aimed to determine the gastrointestinal adverse effects of ZEN in Drosophila melanogaster (D. melanogaster) and reveal possible mechanisms of action of ZEN in insects. Here, chronic exposure of D. melanogaster to ZEN killed flies in a dose-dependent manner (2–20 µM). ZEN (20 µM) decreased the survival rates and climbing ability of flies, and activated immune deficiency-mediated intestinal immunity in midgut, leading to the production of antimicrobial peptides. Meanwhile, ZEN exposure induced morphological alteration of adult midgut. Further study suggested that high levels of oxidative stress was observed in ZEN-treated midgut due to the imbalance between the production of reactive oxygen species and the expression and activities of cellular antioxidant enzyme, including superoxide dismutase and catalase. ZEN-induced oxidative stress then caused cell death, impaired gut barrier function and increased gut permeability, leading to oxidative injury in midgut. Subsequently, ZEN-induce midgut injury further disrupted intestinal stem cell (ISC) homeostasis, stimulating ISC proliferation and tissue regeneration, but did not alter cell fate specification of ISC. Additionally, activation of Jun N-terminal kinase pathway was involved in ZEN-induced oxidative injury and tissue regeneration in midgut. Antioxidant vitamin E alleviated ZEN-induced oxidative injury to midgut epithelium. Collectively, this study provided additional evidences for ZEN-induced gastrointestinal adverse effects from an invertebrate model, extended our understanding of the mechanisms mediating mycotoxin toxicity in organisms.http://www.sciencedirect.com/science/article/pii/S0147651323000593ZearalenoneDrosophila midgutIntestinal immunityOxidative stressCell deathTissue regeneration
spellingShingle Zhi Chen
Fen Wang
Wen Zhang
Shuangshuang Zhou
Di Wen
Ren Mu
Chronic exposure to zearalenone induces intestinal inflammation and oxidative injury in adult Drosophila melanogaster midgut
Ecotoxicology and Environmental Safety
Zearalenone
Drosophila midgut
Intestinal immunity
Oxidative stress
Cell death
Tissue regeneration
title Chronic exposure to zearalenone induces intestinal inflammation and oxidative injury in adult Drosophila melanogaster midgut
title_full Chronic exposure to zearalenone induces intestinal inflammation and oxidative injury in adult Drosophila melanogaster midgut
title_fullStr Chronic exposure to zearalenone induces intestinal inflammation and oxidative injury in adult Drosophila melanogaster midgut
title_full_unstemmed Chronic exposure to zearalenone induces intestinal inflammation and oxidative injury in adult Drosophila melanogaster midgut
title_short Chronic exposure to zearalenone induces intestinal inflammation and oxidative injury in adult Drosophila melanogaster midgut
title_sort chronic exposure to zearalenone induces intestinal inflammation and oxidative injury in adult drosophila melanogaster midgut
topic Zearalenone
Drosophila midgut
Intestinal immunity
Oxidative stress
Cell death
Tissue regeneration
url http://www.sciencedirect.com/science/article/pii/S0147651323000593
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