Effects of PM2.5 and high-fat diet on glucose and lipid metabolisms and role of MT-COX3 methylation in male rats

Chen Li; Shu Ni; Lei Zhao; Huishu Lin; Xueli Yang; Qiang Zhang; Liwen Zhang; Liqiong Guo; Shoufang Jiang; Naijun Tang

Environment International (Jun 2024)

Effects of PM2.5 and high-fat diet on glucose and lipid metabolisms and role of MT-COX3 methylation in male rats

Chen Li,
Shu Ni,
Lei Zhao,
Huishu Lin,
Xueli Yang,
Qiang Zhang,
Liwen Zhang,
Liqiong Guo,
Shoufang Jiang,
Naijun Tang

Affiliations

Chen Li: Department of Occupational and Environmental Health, School of Public Health, Tianjin Medical University, Tianjin 300070, China; Tianjin Key Laboratory of Environment, Nutrition and Public Health, Tianjin 300070, China; Center for International Collaborative Research on Environment, Nutrition and Public Health, Tianjin 300070, China
Shu Ni: Department of Occupational and Environmental Health, School of Public Health, Tianjin Medical University, Tianjin 300070, China; Tianjin Key Laboratory of Environment, Nutrition and Public Health, Tianjin 300070, China; Center for International Collaborative Research on Environment, Nutrition and Public Health, Tianjin 300070, China
Lei Zhao: Institute of Disaster and Emergency Medicine, Tianjin University, Tianjin 300072, China; Wenzhou Safety (Emergency) Institute, Tianjin University, Wenzhou 32500, China
Huishu Lin: Institute of Disaster and Emergency Medicine, Tianjin University, Tianjin 300072, China; Wenzhou Safety (Emergency) Institute, Tianjin University, Wenzhou 32500, China
Xueli Yang: Department of Occupational and Environmental Health, School of Public Health, Tianjin Medical University, Tianjin 300070, China; Tianjin Key Laboratory of Environment, Nutrition and Public Health, Tianjin 300070, China; Center for International Collaborative Research on Environment, Nutrition and Public Health, Tianjin 300070, China
Qiang Zhang: Department of Occupational and Environmental Health, School of Public Health, Tianjin Medical University, Tianjin 300070, China; Tianjin Key Laboratory of Environment, Nutrition and Public Health, Tianjin 300070, China; Center for International Collaborative Research on Environment, Nutrition and Public Health, Tianjin 300070, China
Liwen Zhang: Department of Occupational and Environmental Health, School of Public Health, Tianjin Medical University, Tianjin 300070, China; Tianjin Key Laboratory of Environment, Nutrition and Public Health, Tianjin 300070, China; Center for International Collaborative Research on Environment, Nutrition and Public Health, Tianjin 300070, China
Liqiong Guo: Institute of Disaster and Emergency Medicine, Tianjin University, Tianjin 300072, China; Wenzhou Safety (Emergency) Institute, Tianjin University, Wenzhou 32500, China; Corresponding author at: Institute of Disaster and Emergency Medicine, Tianjin University, Tianjin 300072, China.
Shoufang Jiang: Department of Occupational and Environmental Health, Hebei Province Key Laboratory of Occupational Health and Safety for Coal Industry, School of Public Health, North China University of Science and Technology, Tangshan, Hebei 063210, China; Corresponding author at: School of Public Health, North China University of Science and Technology, Tangshan, Hebei 063210, China
Naijun Tang: Department of Occupational and Environmental Health, School of Public Health, Tianjin Medical University, Tianjin 300070, China; Tianjin Key Laboratory of Environment, Nutrition and Public Health, Tianjin 300070, China; Center for International Collaborative Research on Environment, Nutrition and Public Health, Tianjin 300070, China; Corresponding author at: Department of Occupational and Environmental Health, School of Public Health, Tianjin Medical University, Tianjin 300070, China.

Journal volume & issue: Vol. 188
p. 108780

Abstract

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Both fine particulate matter (PM2.5) and high-fat diet (HFD) can cause changes in glucose and lipid metabolisms; however, the mechanism of their combined effects on glucose and lipid metabolisms is still unclear. This study aimed to investigate the effects of PM2.5 and HFD co-exposure on glucose and lipid metabolisms and mitochondrial DNA methylation in Wistar rats. PM2.5 and HFD co-treatment led to an increase in fasting blood glucose levels, an alteration in glucose tolerance, and a decrease in high density lipoprotein cholesterol (HDL-C) levels in Wistar rats. In the homeostasis model assessment (HOMA), HOMA-insulin resistance (HOMA-IR) increased and HOMA-insulin sensitivity (HOMA-IS) and HOMA-β cell function (HOMA-β) decreased in rats co-exposed to PM2.5 and HFD. Additionally, superoxide dismutase (SOD) and malondialdehyde (MDA) levels were increased, and interleukin-6 (IL-6) and interleukin-10 (IL-10) mRNA expressions were upregulated in the brown adipose tissue following PM2.5 and HFD co-exposure. Bisulfite pyrosequencing was used to detect the methylation levels of mitochondrially-encoded genes (MT-COX1, MT-COX2 and MT-COX3), and MT-COX3 was hypermethylated in the PM2.5 and HFD co-exposure group. Moreover, MT-COX3-Pos.2 mediated 36.41 % (95 % CI: −27.42, −0.75) of the total effect of PM2.5 and HFD exposure on HOMA-β. Our study suggests that PM2.5 and HFD co-exposure led to changes in glucose and lipid metabolisms in rats, which may be related to oxidative stress and inflammatory responses, followed by mitochondrial stress leading to MT-COX3 hypermethylation. Moreover, MT-COX3-Pos.2 was found for the first time as a mediator in the impact of co-exposure to PM2.5 and HFD on β-cell function. It could serve as a potential biomarker, offering fresh insights into the prevention and treatment of metabolic diseases.

Published in Environment International

ISSN: 0160-4120 (Print)
Publisher: Elsevier
Country of publisher: United Kingdom
LCC subjects: Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.journals.elsevier.com/environment-international

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