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Published on: May 17, 2024
Epigenetic transgenerational effects of PM2.5 collected from southern Taiwan on sperm functions and DNA methylation
Chia-Wei Lee1, Kuan-Ling Chen1, Chung-Shin Yuan2
1Department of Safety, Health and Environmental Engineering, National Kaohsiung University of Science and Technology, Kaohsiung 81157, Taiwan.
Abstract:
During respiration, particulate matter with a diameter of 2.5 µm or less (PM2.5) suspended in the atmosphere enters the terminal alveoli and blood. PM2.5 particles can attach to toxic substances, resulting in health problems. Limited information is available regarding the effects of prenatal exposure to water-soluble PM2.5 (WS-PM2.5) and water-insoluble PM2.5 (WI-PM2.5) on male reproduction. In addition, whether exposure to these particles has transgenerational effects remains unknown. We investigated whether prenatal exposure to WS-PM2.5 and WI-PM2.5 disrupts sperm function in generations F1, F2, and F3 of male mice. Pregnant BALB/c mice were treated using intratracheal instillation on gestation days 7, 11, and 15 with 10 mg of a water extract or insoluble PM2.5. On postnatal day 105, epididymal sperm count, motility, morphology, mitochondrial membrane potential (MMP), reactive oxygen species (ROS) production, the sperm chromatin DNA fragmentation index (DFI), and testicular DNA methyltransferase (Dnmt) levels were evaluated in all generations. Whole-genome bisulfite sequencing was used to analyze the DNA methylation status of generation F3. According to the results, exposure to WS-PM2.5 affected sperm morphology, ROS production, and mean DFI in generation F1; ROS production and mean DFI in generation F2; and sperm morphology and MMP in generation F3. Similarly, exposure to WI-PM2.5 affected sperm morphology, ROS production, mean DFI, %DFI, and Dnmt1 expression in generation F1; sperm morphology, MMP, and ROS production in generation F2; and sperm morphology, ROS, and %DFI in generation F3. Two hypermethylated genes, PRR16 and TJP2, were observed in the WS-PM2.5 and WI-PM2.5 groups, two hypomethylated genes, NFATC1 and APOA5, were observed in the WS-PM2.5 group, and two hypomethylated genes, ZFP945 and GSE1, were observed in the WI-PM2.5 group. Hence, prenatal exposure to PM2.5 resulted in transgenerational epigenetic effects, which may explain certain phenotypic changes in male reproduction.
Insights
Prenatal exposure to water-soluble and water-insoluble PM2.5 (particulate matter 2.5) affects male mouse sperm function across three generations. This exposure also leads to transgenerational epigenetic changes, impacting reproductive health.
Area of Science:
- Environmental Health
- Reproductive Toxicology
- Epigenetics
Background:
- Particulate matter 2.5 (PM2.5) poses health risks upon inhalation.
- Limited data exists on prenatal exposure to water-soluble PM2.5 (WS-PM2.5) and water-insoluble PM2.5 (WI-PM2.5) and their effects on male reproduction.
- Transgenerational effects of PM2.5 exposure are largely unknown.
Purpose of the Study:
- To investigate the impact of prenatal WS-PM2.5 and WI-PM2.5 exposure on sperm function in male mice across F1, F2, and F3 generations.
- To determine if PM2.5 exposure induces transgenerational epigenetic alterations.
Main Methods:
- Pregnant mice received intratracheal instillation of WS-PM2.5 or WI-PM2.5.
- Sperm parameters (count, motility, morphology, mitochondrial membrane potential, ROS, DNA fragmentation index) and testicular DNA methyltransferase levels were assessed in offspring.
- Whole-genome bisulfite sequencing analyzed DNA methylation in the F3 generation.
Main Results:
- Both WS-PM2.5 and WI-PM2.5 exposure negatively impacted sperm morphology, ROS production, and DNA fragmentation across generations.
- Specific effects included altered mitochondrial membrane potential and DNA methyltransferase levels.
- Epigenetic analysis revealed hyper- and hypomethylated genes in exposed F3 offspring.
Conclusions:
- Prenatal exposure to PM2.5, both water-soluble and water-insoluble, disrupts male reproductive function transgenerationally.
- These reproductive effects are associated with epigenetic modifications, suggesting a mechanism for transgenerational inheritance of altered phenotypes.
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