The key to 2,6-dichloro-1,4-benzoquinone reproductive toxicity and green tea detoxification: Covalent binding and competitive binding

Halobenzoquinones (HBQs) are ubiquitous disinfection by-products (DBPs) in chlorinated drinking water with various health risks including reproductive toxicity, while the potential mechanisms are still unclear. Although green tea exhibits common detoxifying properties, its ability to mitigate the to...

Full description

Saved in:
Bibliographic Details
Main Authors: Meixian Liu, Zhiyuan Ning, Yong Cheng, Zhiyuan Zheng, Xiaoxue Yang, Ting Zheng, Na Li, Jian-Lin Wu
Format: Article
Language:English
Published: Elsevier 2024-11-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324013150
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850177388409782272
author Meixian Liu
Zhiyuan Ning
Yong Cheng
Zhiyuan Zheng
Xiaoxue Yang
Ting Zheng
Na Li
Jian-Lin Wu
author_facet Meixian Liu
Zhiyuan Ning
Yong Cheng
Zhiyuan Zheng
Xiaoxue Yang
Ting Zheng
Na Li
Jian-Lin Wu
author_sort Meixian Liu
collection DOAJ
description Halobenzoquinones (HBQs) are ubiquitous disinfection by-products (DBPs) in chlorinated drinking water with various health risks including reproductive toxicity, while the potential mechanisms are still unclear. Although green tea exhibits common detoxifying properties, its ability to mitigate the toxicity of HBQs still needs to be further deepened and explored. This study attempted to investigate the possible mechanism of the most common HBQ, 2,6-dichloro-1,4-benzoquinone (2,6-DCBQ) induced reproductive toxicity and elucidate the protective effect of green tea using a series of liquid chromatography-tandem mass spectrometry (LC-MS) approaches. Firstly, in vivo experiments showed that 2,6-DCBQ could induce testicular damage in male rats via significantly decreasing sperm-associated Leydig cells and seminiferous tubules. Then, in vitro incubation of 2,6-DCBQ with amino acids suggested that 2,6-DCBQ could bind to proteins via residues of cysteine or lysine and provided five additional modification patterns. Following, proteomics analysis revealed that at least 42 proteins were modified by 2,6-DCBQ, which were mainly enriched in the reproductive system. These results highlighted the significance of covalent protein modification in 2,6-DCBQ reproductive toxicity. Fortunately, we found that catechins (a class of major components of green tea) could competitively bind to 2,6-DCBQ in vivo and in vitro, reducing the amount and type of 2,6-DCBQ-protein adducts, thereby attenuating the reproductive system damage caused by 2,6-DCBQ. This study provides new insights into 2,6-DCBQ-induced reproductive system damage and reveals a new mechanism of green tea detoxification. Moreover, these findings offer potential strategies for alleviating the harmful impacts of environmental toxicants on human health.
format Article
id doaj-art-bca2cc6e60e24522ac1fda0b3821db29
institution OA Journals
issn 0147-6513
language English
publishDate 2024-11-01
publisher Elsevier
record_format Article
series Ecotoxicology and Environmental Safety
spelling doaj-art-bca2cc6e60e24522ac1fda0b3821db292025-08-20T02:18:58ZengElsevierEcotoxicology and Environmental Safety0147-65132024-11-0128611723910.1016/j.ecoenv.2024.117239The key to 2,6-dichloro-1,4-benzoquinone reproductive toxicity and green tea detoxification: Covalent binding and competitive bindingMeixian Liu0Zhiyuan Ning1Yong Cheng2Zhiyuan Zheng3Xiaoxue Yang4Ting Zheng5Na Li6Jian-Lin Wu7State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, Avenida Wai Long, Taipa, 999078, Macao, China; BayRay Innovation Center, Shenzhen Bay Laboratory, Shenzhen 518132, ChinaState Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, Avenida Wai Long, Taipa, 999078, Macao, ChinaZhejiang Skyherb Biotechnology Inc., Huzhou 313300, ChinaFaculty of Pharmaceutical Sciences, Shenzhen University of Advanced Technology, Shenzhen 518107, China; Center for Cancer Immunology, Institute of Biomedicine and Biotechnology, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, ChinaState Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, Avenida Wai Long, Taipa, 999078, Macao, ChinaMulti-omics Mass Spectrometry Core, Biomedical Research Core Facilities, Shenzhen Bay Laboratory, Shenzhen 518132, China.State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, Avenida Wai Long, Taipa, 999078, Macao, China; Corresponding authors.State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology, Avenida Wai Long, Taipa, 999078, Macao, China; Corresponding authors.Halobenzoquinones (HBQs) are ubiquitous disinfection by-products (DBPs) in chlorinated drinking water with various health risks including reproductive toxicity, while the potential mechanisms are still unclear. Although green tea exhibits common detoxifying properties, its ability to mitigate the toxicity of HBQs still needs to be further deepened and explored. This study attempted to investigate the possible mechanism of the most common HBQ, 2,6-dichloro-1,4-benzoquinone (2,6-DCBQ) induced reproductive toxicity and elucidate the protective effect of green tea using a series of liquid chromatography-tandem mass spectrometry (LC-MS) approaches. Firstly, in vivo experiments showed that 2,6-DCBQ could induce testicular damage in male rats via significantly decreasing sperm-associated Leydig cells and seminiferous tubules. Then, in vitro incubation of 2,6-DCBQ with amino acids suggested that 2,6-DCBQ could bind to proteins via residues of cysteine or lysine and provided five additional modification patterns. Following, proteomics analysis revealed that at least 42 proteins were modified by 2,6-DCBQ, which were mainly enriched in the reproductive system. These results highlighted the significance of covalent protein modification in 2,6-DCBQ reproductive toxicity. Fortunately, we found that catechins (a class of major components of green tea) could competitively bind to 2,6-DCBQ in vivo and in vitro, reducing the amount and type of 2,6-DCBQ-protein adducts, thereby attenuating the reproductive system damage caused by 2,6-DCBQ. This study provides new insights into 2,6-DCBQ-induced reproductive system damage and reveals a new mechanism of green tea detoxification. Moreover, these findings offer potential strategies for alleviating the harmful impacts of environmental toxicants on human health.http://www.sciencedirect.com/science/article/pii/S0147651324013150Catechin2,6-DCBQCovalent protein modificationRatReproductive toxicity
spellingShingle Meixian Liu
Zhiyuan Ning
Yong Cheng
Zhiyuan Zheng
Xiaoxue Yang
Ting Zheng
Na Li
Jian-Lin Wu
The key to 2,6-dichloro-1,4-benzoquinone reproductive toxicity and green tea detoxification: Covalent binding and competitive binding
Ecotoxicology and Environmental Safety
Catechin
2,6-DCBQ
Covalent protein modification
Rat
Reproductive toxicity
title The key to 2,6-dichloro-1,4-benzoquinone reproductive toxicity and green tea detoxification: Covalent binding and competitive binding
title_full The key to 2,6-dichloro-1,4-benzoquinone reproductive toxicity and green tea detoxification: Covalent binding and competitive binding
title_fullStr The key to 2,6-dichloro-1,4-benzoquinone reproductive toxicity and green tea detoxification: Covalent binding and competitive binding
title_full_unstemmed The key to 2,6-dichloro-1,4-benzoquinone reproductive toxicity and green tea detoxification: Covalent binding and competitive binding
title_short The key to 2,6-dichloro-1,4-benzoquinone reproductive toxicity and green tea detoxification: Covalent binding and competitive binding
title_sort key to 2 6 dichloro 1 4 benzoquinone reproductive toxicity and green tea detoxification covalent binding and competitive binding
topic Catechin
2,6-DCBQ
Covalent protein modification
Rat
Reproductive toxicity
url http://www.sciencedirect.com/science/article/pii/S0147651324013150
work_keys_str_mv AT meixianliu thekeyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT zhiyuanning thekeyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT yongcheng thekeyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT zhiyuanzheng thekeyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT xiaoxueyang thekeyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT tingzheng thekeyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT nali thekeyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT jianlinwu thekeyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT meixianliu keyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT zhiyuanning keyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT yongcheng keyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT zhiyuanzheng keyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT xiaoxueyang keyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT tingzheng keyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT nali keyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding
AT jianlinwu keyto26dichloro14benzoquinonereproductivetoxicityandgreenteadetoxificationcovalentbindingandcompetitivebinding