Oxidative stress caused by 3-monochloro-1,2-propanediol provokes intestinal stem cell hyperproliferation and the protective role of quercetin

Recently, the contaminant 3-monochloropropane-1,2-diol (3-MCPD) found in food and the environment has garnered significant global attention due to its detrimental health effects on animals, including reproductive toxicity, neurotoxicity, and nephrotoxicity. However, the specific impacts and mechanis...

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Main Authors: Zongzhong Liu, Yanfei He, Yuhan Wang, Kefeng Ren, Pengpeng Xia, Binbin Xie, Tian Wei
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651325001873
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author Zongzhong Liu
Yanfei He
Yuhan Wang
Kefeng Ren
Pengpeng Xia
Binbin Xie
Tian Wei
author_facet Zongzhong Liu
Yanfei He
Yuhan Wang
Kefeng Ren
Pengpeng Xia
Binbin Xie
Tian Wei
author_sort Zongzhong Liu
collection DOAJ
description Recently, the contaminant 3-monochloropropane-1,2-diol (3-MCPD) found in food and the environment has garnered significant global attention due to its detrimental health effects on animals, including reproductive toxicity, neurotoxicity, and nephrotoxicity. However, the specific impacts and mechanisms of 3-MCPD on intestinal health remain elusive. Here, we employed the adult intestine of Drosophila melanogaster, a notable invertebrate model organism, to investigate the intestinal toxicity of 3-MCPD and its underlying mechanisms. Our findings revealed that exposure to 3-MCPD led to a decrease in the number of enterocyte cells and an elevation in apoptosis levels, ultimately disrupting the intestinal epithelial barrier and its function. This disruption subsequently triggered hyperproliferation and differentiation of intestinal stem cells (ISCs). Mechanistically, 3-MCPD induced oxidative stress in the Drosophila intestine, which was likely responsible for ISC hyperproliferation and intestinal damage. Intriguingly, quercetin, a natural antioxidant derived from dietary fruits and vegetables, alleviated 3-MCPD-induced intestinal toxicity by inhibiting the JNK pathway. Our findings uncover a mechanism whereby suppression of undesirable ISC hyperproliferation, caused by 3-MCPD-induced oxidative stress, maintains intestinal homeostasis, and provide a theoretical basis for exploiting quercetin, a natural antioxidant, as a dietary antidote against the intestinal hazards posed by environmental toxicants.
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publishDate 2025-02-01
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series Ecotoxicology and Environmental Safety
spelling doaj-art-a2de8ce93f9e47e7bc60de1f38400ea82025-02-07T04:46:37ZengElsevierEcotoxicology and Environmental Safety0147-65132025-02-01291117851Oxidative stress caused by 3-monochloro-1,2-propanediol provokes intestinal stem cell hyperproliferation and the protective role of quercetinZongzhong Liu0Yanfei He1Yuhan Wang2Kefeng Ren3Pengpeng Xia4Binbin Xie5Tian Wei6Department of Toxicology, School of Public Health, Anhui Medical University, Hefei, China; Key Laboratory of Environmental Toxicology of Anhui Higher Education Institutes, Hefei, ChinaDepartment of Toxicology, School of Public Health, Anhui Medical University, Hefei, China; Key Laboratory of Environmental Toxicology of Anhui Higher Education Institutes, Hefei, ChinaDepartment of Toxicology, School of Public Health, Anhui Medical University, Hefei, China; Key Laboratory of Environmental Toxicology of Anhui Higher Education Institutes, Hefei, ChinaDepartment of Toxicology, School of Public Health, Anhui Medical University, Hefei, China; Key Laboratory of Environmental Toxicology of Anhui Higher Education Institutes, Hefei, ChinaDepartment of Toxicology, School of Public Health, Anhui Medical University, Hefei, China; Key Laboratory of Environmental Toxicology of Anhui Higher Education Institutes, Hefei, ChinaDepartment of Toxicology, School of Public Health, Anhui Medical University, Hefei, China; Key Laboratory of Environmental Toxicology of Anhui Higher Education Institutes, Hefei, ChinaDepartment of Toxicology, School of Public Health, Anhui Medical University, Hefei, China; Key Laboratory of Environmental Toxicology of Anhui Higher Education Institutes, Hefei, China; Corresponding author at: Department of Toxicology, School of Public Health, Anhui Medical University, Hefei, China.Recently, the contaminant 3-monochloropropane-1,2-diol (3-MCPD) found in food and the environment has garnered significant global attention due to its detrimental health effects on animals, including reproductive toxicity, neurotoxicity, and nephrotoxicity. However, the specific impacts and mechanisms of 3-MCPD on intestinal health remain elusive. Here, we employed the adult intestine of Drosophila melanogaster, a notable invertebrate model organism, to investigate the intestinal toxicity of 3-MCPD and its underlying mechanisms. Our findings revealed that exposure to 3-MCPD led to a decrease in the number of enterocyte cells and an elevation in apoptosis levels, ultimately disrupting the intestinal epithelial barrier and its function. This disruption subsequently triggered hyperproliferation and differentiation of intestinal stem cells (ISCs). Mechanistically, 3-MCPD induced oxidative stress in the Drosophila intestine, which was likely responsible for ISC hyperproliferation and intestinal damage. Intriguingly, quercetin, a natural antioxidant derived from dietary fruits and vegetables, alleviated 3-MCPD-induced intestinal toxicity by inhibiting the JNK pathway. Our findings uncover a mechanism whereby suppression of undesirable ISC hyperproliferation, caused by 3-MCPD-induced oxidative stress, maintains intestinal homeostasis, and provide a theoretical basis for exploiting quercetin, a natural antioxidant, as a dietary antidote against the intestinal hazards posed by environmental toxicants.http://www.sciencedirect.com/science/article/pii/S01476513250018733-monochloro-1,2-propanediolOxidative stressIntestinal stem cellQuercetinJNK
spellingShingle Zongzhong Liu
Yanfei He
Yuhan Wang
Kefeng Ren
Pengpeng Xia
Binbin Xie
Tian Wei
Oxidative stress caused by 3-monochloro-1,2-propanediol provokes intestinal stem cell hyperproliferation and the protective role of quercetin
Ecotoxicology and Environmental Safety
3-monochloro-1,2-propanediol
Oxidative stress
Intestinal stem cell
Quercetin
JNK
title Oxidative stress caused by 3-monochloro-1,2-propanediol provokes intestinal stem cell hyperproliferation and the protective role of quercetin
title_full Oxidative stress caused by 3-monochloro-1,2-propanediol provokes intestinal stem cell hyperproliferation and the protective role of quercetin
title_fullStr Oxidative stress caused by 3-monochloro-1,2-propanediol provokes intestinal stem cell hyperproliferation and the protective role of quercetin
title_full_unstemmed Oxidative stress caused by 3-monochloro-1,2-propanediol provokes intestinal stem cell hyperproliferation and the protective role of quercetin
title_short Oxidative stress caused by 3-monochloro-1,2-propanediol provokes intestinal stem cell hyperproliferation and the protective role of quercetin
title_sort oxidative stress caused by 3 monochloro 1 2 propanediol provokes intestinal stem cell hyperproliferation and the protective role of quercetin
topic 3-monochloro-1,2-propanediol
Oxidative stress
Intestinal stem cell
Quercetin
JNK
url http://www.sciencedirect.com/science/article/pii/S0147651325001873
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