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Review
. 2024 Nov 10:950:175042.
doi: 10.1016/j.scitotenv.2024.175042. Epub 2024 Jul 29.

The dual effects of Benzo(a)pyrene/Benzo(a)pyrene-7,8-dihydrodiol-9,10-epoxide on DNA Methylation

Cheng Zhao  1 , Hui Jin  2 , Yu Lei  1 , Qilin Li  1 , Ying Zhang  3 , Qianjin Lu  4
Affiliations
Review

The dual effects of Benzo(a)pyrene/Benzo(a)pyrene-7,8-dihydrodiol-9,10-epoxide on DNA Methylation

Cheng Zhao et al. Sci Total Environ. .

Abstract

Benzo(a)pyrene (BaP) is one of the most thoroughly studied polycyclic aromatic hydrocarbons(PAHs) and a widespread organic pollutant in various areas of human life. Its teratogenic, immunotoxic and carcinogenic effects on organisms are well documented and widely recognized by researchers. In the body, BaP is enzymatically converted to form a more active benzo(a)pyrene-7,8-dihydrodiol-9,10-epoxide (BPDE). BaP/BPDE has the potential to trigger gene mutations, influence epigenetic modifications and cause damage to cellular structures, ultimately contributing to disease onset and progression. However, there are different points of view when studying epigenetics using BaP/BPDE. On the one hand, it is claimed in cancer research that BaP/BPDE contributes to gene hypermethylation and, in particular, induces the hypermethylation of tumor's suppressor gene promoters, leading to gene silencing and subsequent cancer development. Conversely, studies in human and animal populations suggest that exposure to BaP results in genome-wide DNA hypomethylation, potentially leading to adverse outcomes in inflammatory diseases. This apparent contradiction has not been summarized in research for almost four decades. This article presents a comprehensive review of the current literature on the influence of BaP/BPDE on DNA methylation regulation. It demonstrates that BaP/BPDE exerts a dual-phase regulatory effect on methylation, which is influenced by factors such as the concentration and duration of BaP/BPDE exposure, experimental models and detection methods used in various studies. Acute/high concentration exposure to BaP/BPDE often results in global demethylation of DNA, which is associated with inhibition of DNA methyltransferase 1 (DNMT1) after exposure. At certain specific gene loci (e.g., RAR-β), BPDE can form DNA adducts, recruiting DNMT3 and leading to hypermethylation at specific sites. By integrating these different mechanisms, our goal is to unravel the patterns and regulations of BaP/BPDE-induced DNA methylation changes and provide insights into future precision therapies targeting epigenetics.

Keywords: Autoimmune disease; Benzo(a)pyrene(BaP); Benzo(a)pyrene-7,8-dihydrodiol-9,10-epoxide(BPDE); Cancer; DNA methylation.

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Conflict of interest statement

Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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