Integrated mRNA- and miRNA-sequencing analyses unveil the underlying mechanism of tobacco pollutant-induced developmental toxicity in zebrafish embryos

Abstract Tobacco pollutants are prevalent in the environment, leading to inadvertent exposure of pregnant females. Studies of these pollutants' toxic effects on embryonic development have not fully elucidated the potential underlying mechanisms. Therefore, in this study, we aimed to investigate...

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Main Authors: Jiasheng Chen, Yuxin Lin, Deyi Gen, Wanxian Chen, Rui Han, Hao Li, Shijie Tang, Shukai Zheng, Xiaoping Zhong
Format: Article
Language:English
Published: BMC 2024-03-01
Series:Journal of Translational Medicine
Subjects:
Online Access:https://doi.org/10.1186/s12967-024-05050-9
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author Jiasheng Chen
Yuxin Lin
Deyi Gen
Wanxian Chen
Rui Han
Hao Li
Shijie Tang
Shukai Zheng
Xiaoping Zhong
author_facet Jiasheng Chen
Yuxin Lin
Deyi Gen
Wanxian Chen
Rui Han
Hao Li
Shijie Tang
Shukai Zheng
Xiaoping Zhong
author_sort Jiasheng Chen
collection DOAJ
description Abstract Tobacco pollutants are prevalent in the environment, leading to inadvertent exposure of pregnant females. Studies of these pollutants' toxic effects on embryonic development have not fully elucidated the potential underlying mechanisms. Therefore, in this study, we aimed to investigate the developmental toxicity induced by cigarette smoke extract (CSE) at concentrations of 0.25, 1, and 2.5% using a zebrafish embryo toxicity test and integrated transcriptomic analysis of microRNA (miRNA) and messenger RNA (mRNA). The findings revealed that CSE caused developmental toxicity, including increased mortality and decreased incubation rate, in a dose-dependent manner. Moreover, CSE induced malformations and apoptosis, specifically in the head and heart of zebrafish larvae. We used mRNA and miRNA sequencing analyses to compare changes in the expression of genes and miRNAs in zebrafish larvae. The bioinformatics analysis indicates that the mechanism underlying CSE-induced developmental toxicity was associated with compromised genetic material damage repair, deregulated apoptosis, and disturbed lipid metabolism. The enrichment analysis and RT-qPCR show that the ctsba gene plays a crucial function in embryo developmental apoptosis, and the fads2 gene mainly regulates lipid metabolic toxicity. The results of this study improve the understanding of CSE-induced developmental toxicity in zebrafish embryos and contribute insights into the formulation of novel preventive strategies against tobacco pollutants during early embryonic development.
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spelling doaj.art-374895d36f0e4837a72de1e363c2ccc02024-03-10T12:20:58ZengBMCJournal of Translational Medicine1479-58762024-03-0122111510.1186/s12967-024-05050-9Integrated mRNA- and miRNA-sequencing analyses unveil the underlying mechanism of tobacco pollutant-induced developmental toxicity in zebrafish embryosJiasheng Chen0Yuxin Lin1Deyi Gen2Wanxian Chen3Rui Han4Hao Li5Shijie Tang6Shukai Zheng7Xiaoping Zhong8Department of Burns and Plastic Surgery, The Second Affiliated Hospital of Shantou University Medical CollegeDepartment of Burns and Plastic Surgery, The Second Affiliated Hospital of Shantou University Medical CollegeDepartment of Burns and Plastic Surgery, The Second Affiliated Hospital of Shantou University Medical CollegeDepartment of Burns and Plastic Surgery, The Second Affiliated Hospital of Shantou University Medical CollegeDepartment of Burns and Plastic Surgery, The Second Affiliated Hospital of Shantou University Medical CollegeDepartment of Burns and Plastic Surgery, The Second Affiliated Hospital of Shantou University Medical CollegeDepartment of Burns and Plastic Surgery, The Second Affiliated Hospital of Shantou University Medical CollegeDepartment of Burns and Plastic Surgery, The Second Affiliated Hospital of Shantou University Medical CollegeDepartment of Burns and Plastic Surgery, The Second Affiliated Hospital of Shantou University Medical CollegeAbstract Tobacco pollutants are prevalent in the environment, leading to inadvertent exposure of pregnant females. Studies of these pollutants' toxic effects on embryonic development have not fully elucidated the potential underlying mechanisms. Therefore, in this study, we aimed to investigate the developmental toxicity induced by cigarette smoke extract (CSE) at concentrations of 0.25, 1, and 2.5% using a zebrafish embryo toxicity test and integrated transcriptomic analysis of microRNA (miRNA) and messenger RNA (mRNA). The findings revealed that CSE caused developmental toxicity, including increased mortality and decreased incubation rate, in a dose-dependent manner. Moreover, CSE induced malformations and apoptosis, specifically in the head and heart of zebrafish larvae. We used mRNA and miRNA sequencing analyses to compare changes in the expression of genes and miRNAs in zebrafish larvae. The bioinformatics analysis indicates that the mechanism underlying CSE-induced developmental toxicity was associated with compromised genetic material damage repair, deregulated apoptosis, and disturbed lipid metabolism. The enrichment analysis and RT-qPCR show that the ctsba gene plays a crucial function in embryo developmental apoptosis, and the fads2 gene mainly regulates lipid metabolic toxicity. The results of this study improve the understanding of CSE-induced developmental toxicity in zebrafish embryos and contribute insights into the formulation of novel preventive strategies against tobacco pollutants during early embryonic development.https://doi.org/10.1186/s12967-024-05050-9Cigarette smoke extractRNA-seqApoptosis disorderLipid metabolism
spellingShingle Jiasheng Chen
Yuxin Lin
Deyi Gen
Wanxian Chen
Rui Han
Hao Li
Shijie Tang
Shukai Zheng
Xiaoping Zhong
Integrated mRNA- and miRNA-sequencing analyses unveil the underlying mechanism of tobacco pollutant-induced developmental toxicity in zebrafish embryos
Journal of Translational Medicine
Cigarette smoke extract
RNA-seq
Apoptosis disorder
Lipid metabolism
title Integrated mRNA- and miRNA-sequencing analyses unveil the underlying mechanism of tobacco pollutant-induced developmental toxicity in zebrafish embryos
title_full Integrated mRNA- and miRNA-sequencing analyses unveil the underlying mechanism of tobacco pollutant-induced developmental toxicity in zebrafish embryos
title_fullStr Integrated mRNA- and miRNA-sequencing analyses unveil the underlying mechanism of tobacco pollutant-induced developmental toxicity in zebrafish embryos
title_full_unstemmed Integrated mRNA- and miRNA-sequencing analyses unveil the underlying mechanism of tobacco pollutant-induced developmental toxicity in zebrafish embryos
title_short Integrated mRNA- and miRNA-sequencing analyses unveil the underlying mechanism of tobacco pollutant-induced developmental toxicity in zebrafish embryos
title_sort integrated mrna and mirna sequencing analyses unveil the underlying mechanism of tobacco pollutant induced developmental toxicity in zebrafish embryos
topic Cigarette smoke extract
RNA-seq
Apoptosis disorder
Lipid metabolism
url https://doi.org/10.1186/s12967-024-05050-9
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