Transcriptomic and metabolomic profile changes in the liver of Sprague Dawley rat offspring after maternal PFOS exposure during gestation and lactation

Epidemiological and experimental research has indicated an association between perfluorooctane sulfonate (PFOS) exposure and liver disease. However, the potential hepatotoxic effects and mechanisms of low-level prenatal PFOS exposure in offspring remain ambiguous. The objective of this research was...

Full description

Bibliographic Details
Main Authors: Ruiyuan Zhang, Guoqi Yu, Tingyu Luo, Xiaojing Zeng, Yan Sun, Bo Huang, Yongjie Liu, Jun Zhang
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651323013660
_version_ 1827377900426362880
author Ruiyuan Zhang
Guoqi Yu
Tingyu Luo
Xiaojing Zeng
Yan Sun
Bo Huang
Yongjie Liu
Jun Zhang
author_facet Ruiyuan Zhang
Guoqi Yu
Tingyu Luo
Xiaojing Zeng
Yan Sun
Bo Huang
Yongjie Liu
Jun Zhang
author_sort Ruiyuan Zhang
collection DOAJ
description Epidemiological and experimental research has indicated an association between perfluorooctane sulfonate (PFOS) exposure and liver disease. However, the potential hepatotoxic effects and mechanisms of low-level prenatal PFOS exposure in offspring remain ambiguous. The objective of this research was to examine the alterations in liver transcriptomic and metabolomic profiles in offspring rats at postnatal day (PND) 30 following gestational and lactational exposure to PFOS (from gestational day 1 to 20 and PND 1 to 21). Pregnant Sprague-Dawley rats were separated into a control group (3% starch gel solution, oral gavage) and a PFOS exposure group (0.03 mg/kg body weight per day, oral gavage). Histopathological changes in liver sections were observed by hematoxylin and eosin staining. Biochemical analysis was conducted to evaluate changes in glucose and lipid metabolism. Transcriptomic and metabolomic analyses were utilized to identify significant genes and metabolites associated with alterations of liver glucose and lipid metabolism through an integrated multi-omics analysis. No significant differences were found in the measured biochemical parameters. In total, 167 significant differentially expressed genes (DEGs) related to processes such as steroid biosynthesis, PPAR signaling pathway, and fat digestion and absorption were identified in offspring rats in the PFOS exposure group. Ninety-five altered metabolites were exhibited in the PFOS exposure group, such as heptaethylene glycol, lysoPE (0:0/18:0), lucidenic acid K, and p-Cresol sulfate. DEGs associated with steroid biosynthesis, PPAR signaling pathway, fat digestion and absorption were significantly upregulated in the PFOS exposure group (P < 0.05). The analysis of correlations indicated that there was a significant inverse correlation between all identified differential metabolites and the levels of fasting blood glucose, high-density lipoprotein, and triglycerides in the PFOS exposure group (P < 0.05). Our findings demystify that early-life PFOS exposure can lead to alterations in transcriptomic and metabolomic profiles in the offspring’s liver, which provided mechanistic insights into the potential hepatotoxicity and developmental toxicity associated with environmentally relevant levels of PFOS exposure.
first_indexed 2024-03-08T12:48:03Z
format Article
id doaj.art-2471aaf41c954bb2866afacb4e653d6b
institution Directory Open Access Journal
issn 0147-6513
language English
last_indexed 2024-03-08T12:48:03Z
publishDate 2024-01-01
publisher Elsevier
record_format Article
series Ecotoxicology and Environmental Safety
spelling doaj.art-2471aaf41c954bb2866afacb4e653d6b2024-01-21T05:05:04ZengElsevierEcotoxicology and Environmental Safety0147-65132024-01-01270115862Transcriptomic and metabolomic profile changes in the liver of Sprague Dawley rat offspring after maternal PFOS exposure during gestation and lactationRuiyuan Zhang0Guoqi Yu1Tingyu Luo2Xiaojing Zeng3Yan Sun4Bo Huang5Yongjie Liu6Jun Zhang7Ministry of Education-Shanghai Key Laboratory of Children's Environmental Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, 200092 Shanghai, China; School of Public Health, Shanghai Jiao Tong University School of Medicine, 200025, Shanghai, ChinaMinistry of Education-Shanghai Key Laboratory of Children's Environmental Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, 200092 Shanghai, China; Global Center for Asian Women’s Health, Yong Loo Lin School of Medicine, National University of Singapore, 117597 Singapore, SingaporeSchool of Public Health, Guilin Medical University, 541001 Guilin, Guangxi, ChinaMinistry of Education-Shanghai Key Laboratory of Children's Environmental Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, 200092 Shanghai, ChinaSchool of Public Health, Guilin Medical University, 541001 Guilin, Guangxi, ChinaSchool of Public Health, Guilin Medical University, 541001 Guilin, Guangxi, ChinaMinistry of Education-Shanghai Key Laboratory of Children's Environmental Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, 200092 Shanghai, China; State Environmental Protection Key Laboratory of Environmental Health Impact Assessment of Emerging Contaminants, Shanghai Academy of Environment Sciences, 200233, Shanghai, China; Correspondence to: Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200092, China.Ministry of Education-Shanghai Key Laboratory of Children's Environmental Health, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, 200092 Shanghai, China; School of Public Health, Shanghai Jiao Tong University School of Medicine, 200025, Shanghai, China; Correspondence to: Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200092, China.Epidemiological and experimental research has indicated an association between perfluorooctane sulfonate (PFOS) exposure and liver disease. However, the potential hepatotoxic effects and mechanisms of low-level prenatal PFOS exposure in offspring remain ambiguous. The objective of this research was to examine the alterations in liver transcriptomic and metabolomic profiles in offspring rats at postnatal day (PND) 30 following gestational and lactational exposure to PFOS (from gestational day 1 to 20 and PND 1 to 21). Pregnant Sprague-Dawley rats were separated into a control group (3% starch gel solution, oral gavage) and a PFOS exposure group (0.03 mg/kg body weight per day, oral gavage). Histopathological changes in liver sections were observed by hematoxylin and eosin staining. Biochemical analysis was conducted to evaluate changes in glucose and lipid metabolism. Transcriptomic and metabolomic analyses were utilized to identify significant genes and metabolites associated with alterations of liver glucose and lipid metabolism through an integrated multi-omics analysis. No significant differences were found in the measured biochemical parameters. In total, 167 significant differentially expressed genes (DEGs) related to processes such as steroid biosynthesis, PPAR signaling pathway, and fat digestion and absorption were identified in offspring rats in the PFOS exposure group. Ninety-five altered metabolites were exhibited in the PFOS exposure group, such as heptaethylene glycol, lysoPE (0:0/18:0), lucidenic acid K, and p-Cresol sulfate. DEGs associated with steroid biosynthesis, PPAR signaling pathway, fat digestion and absorption were significantly upregulated in the PFOS exposure group (P < 0.05). The analysis of correlations indicated that there was a significant inverse correlation between all identified differential metabolites and the levels of fasting blood glucose, high-density lipoprotein, and triglycerides in the PFOS exposure group (P < 0.05). Our findings demystify that early-life PFOS exposure can lead to alterations in transcriptomic and metabolomic profiles in the offspring’s liver, which provided mechanistic insights into the potential hepatotoxicity and developmental toxicity associated with environmentally relevant levels of PFOS exposure.http://www.sciencedirect.com/science/article/pii/S0147651323013660Perfluorooctane sulfonateMetabolomicsTranscriptomicsOffspringLiver
spellingShingle Ruiyuan Zhang
Guoqi Yu
Tingyu Luo
Xiaojing Zeng
Yan Sun
Bo Huang
Yongjie Liu
Jun Zhang
Transcriptomic and metabolomic profile changes in the liver of Sprague Dawley rat offspring after maternal PFOS exposure during gestation and lactation
Ecotoxicology and Environmental Safety
Perfluorooctane sulfonate
Metabolomics
Transcriptomics
Offspring
Liver
title Transcriptomic and metabolomic profile changes in the liver of Sprague Dawley rat offspring after maternal PFOS exposure during gestation and lactation
title_full Transcriptomic and metabolomic profile changes in the liver of Sprague Dawley rat offspring after maternal PFOS exposure during gestation and lactation
title_fullStr Transcriptomic and metabolomic profile changes in the liver of Sprague Dawley rat offspring after maternal PFOS exposure during gestation and lactation
title_full_unstemmed Transcriptomic and metabolomic profile changes in the liver of Sprague Dawley rat offspring after maternal PFOS exposure during gestation and lactation
title_short Transcriptomic and metabolomic profile changes in the liver of Sprague Dawley rat offspring after maternal PFOS exposure during gestation and lactation
title_sort transcriptomic and metabolomic profile changes in the liver of sprague dawley rat offspring after maternal pfos exposure during gestation and lactation
topic Perfluorooctane sulfonate
Metabolomics
Transcriptomics
Offspring
Liver
url http://www.sciencedirect.com/science/article/pii/S0147651323013660
work_keys_str_mv AT ruiyuanzhang transcriptomicandmetabolomicprofilechangesintheliverofspraguedawleyratoffspringaftermaternalpfosexposureduringgestationandlactation
AT guoqiyu transcriptomicandmetabolomicprofilechangesintheliverofspraguedawleyratoffspringaftermaternalpfosexposureduringgestationandlactation
AT tingyuluo transcriptomicandmetabolomicprofilechangesintheliverofspraguedawleyratoffspringaftermaternalpfosexposureduringgestationandlactation
AT xiaojingzeng transcriptomicandmetabolomicprofilechangesintheliverofspraguedawleyratoffspringaftermaternalpfosexposureduringgestationandlactation
AT yansun transcriptomicandmetabolomicprofilechangesintheliverofspraguedawleyratoffspringaftermaternalpfosexposureduringgestationandlactation
AT bohuang transcriptomicandmetabolomicprofilechangesintheliverofspraguedawleyratoffspringaftermaternalpfosexposureduringgestationandlactation
AT yongjieliu transcriptomicandmetabolomicprofilechangesintheliverofspraguedawleyratoffspringaftermaternalpfosexposureduringgestationandlactation
AT junzhang transcriptomicandmetabolomicprofilechangesintheliverofspraguedawleyratoffspringaftermaternalpfosexposureduringgestationandlactation