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Prenatal exposure to environmental air pollution and psychosocial stress jointly contribute to the epigenetic regulation of the serotonin transporter gene in newborns

Molecular Psychiatry volume 28, pages 3503–3511 (2023)Cite this article

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Abstract

Antenatal exposures to maternal stress and to particulate matter with an aerodynamic diameter of less than 2.5 μm (PM2.5) have been independently associated with developmental outcomes in early infancy and beyond. Knowledge about their joint impact, biological mechanisms of their effects and timing-effects, is still limited. Both PM2.5 and maternal stress exposure during pregnancy might result in altered patterns of DNA methylation in specific stress-related genes, such as the serotonin transporter gene (SLC6A4 DNAm), that might, in turn, influence infant development across several domains, including bio-behavioral, cognitive and socio-emotional domains. Here, we investigated the independent and interactive influence of variations in antenatal exposures to maternal pandemic-related stress (PRS) and PM2.5 on SLC6A4 DNAm levels in newborns. Mother–infant dyads (N = 307) were enrolled at delivery during the COVID-19 pandemic. Infants’ methylation status was assessed in 13 CpG sites within the SLC6A4 gene’s region (chr17:28562750–28562958) in buccal cells at birth and women retrospectively report on PRS. PM2.5 exposure throughout the entire gestation and at each gestational trimester was estimated using a spatiotemporal model based on residential address. Among several potentially confounding socio-demographic and health-related factors, infant’s sex was significantly associated with infants’ SLC6A4 DNAm levels, thus hierarchical regression models were adjusted for infant’s sex. Higher levels of SLC6A4 DNAm at 6 CpG sites were found in newborns born to mothers reporting higher levels of antenatal PRS and greater PM2.5 exposure across gestation, while adjusting for infant’s sex. These effects were especially evident when exposure to elevated PM2.5 occurred during the second trimester of pregnancy. Several important brain processes (e.g., synaptogenesis and myelination) occur during mid-pregnancy, potentially making the second trimester a sensitive time window for the effects of stress-related exposures. Understanding the interplay between environmental and individual-level stressors has important implications for the improvement of mother-infant health during and after the pandemic.

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Fig. 1: Distribution map of pollution and methylation data.
Fig. 2: Association between maternal PRS and infants’ SLC6A4 DNAm PC1 as a function of antenatal exposure to air pollution (β = 0.11, p = 0.04).
Fig. 3: Association between maternal PRS and infants’ SLC6A4 DNAm PC1 as a function of antenatal exposure to air pollution at each trimester of pregnancy.

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Funding

SN was supported by a co-funding of the European Union—European Social Fund REACT-EU, PON Ricerca e Innovazione 2014–2020. LP was supported by the Italian Health Ministry, Ricerca Corrente 2022–2023. Work supported by #NEXTGENERATIONEU (NGEU) and funded by the Ministry of University and Research (MUR), National Recovery and Resilience Plan (NRRP), project MNESYS (PE0000006) – A Multiscale integrated approach to the study of the nervous system in health and disease (DN. 1553 11.10.2022).

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Authors and Affiliations

  1. Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy

    Sarah Nazzari, Lucia Cagliero, Julia Maccarini & Livio Provenzi

  2. Developmental Psychobiology Lab, IRCCS Mondino Foundation, Pavia, Italy

    Lucia Cagliero, Serena Grumi, Julia Maccarini & Livio Provenzi

  3. European Commission, Joint Research Centre (JRC), Ispra, Italy

    Enrico Pisoni

  4. Multiple Sclerosis Center, Neurocenter of South of Switzerland, EOC, Lugano, Switzerland

    Giulia Mallucci

  5. Multiple Sclerosis Research Center, IRCCS Mondino Foundation, Pavia, Italy

    Roberto Bergamaschi

  6. Molecular Biology Lab, Scientific Institute IRCCS E. Medea, Bosisio Parini, Italy

    Roberto Giorda

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  1. Sarah Nazzari
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Contributions

SN contributed to data analysis and drafting the manuscript; LC contributed to data analysis and conceptualization; SG and JM contributed to study design and data management; EP contributed to data collection and pre-processing of pollution data; GM and RB supervised the methodology and contributed to the conceptualization; RB contributed to data analysis and preprocessing of epigenetic data; LP conceptualized the study, obtained funding, coordinated the project, contributed to data analysis and first manuscript draft. All authors contributed to the final manuscript draft and approved the submission.

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Correspondence to Livio Provenzi.

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Nazzari, S., Cagliero, L., Grumi, S. et al. Prenatal exposure to environmental air pollution and psychosocial stress jointly contribute to the epigenetic regulation of the serotonin transporter gene in newborns. Mol Psychiatry 28, 3503–3511 (2023). https://doi.org/10.1038/s41380-023-02206-9

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