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Developmental effects of maternal smoking during pregnancy on the human frontal cortex transcriptome
Stephen A Semick1, Leonardo Collado-Torres1,2, Christina A Markunas3
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA.
Insights
Maternal smoking during pregnancy significantly alters prenatal brain gene expression, impacting 14 genes. These changes are linked to addiction, synaptic function, and autism spectrum disorder (ASD) risks, highlighting the developing brain
Area of Science:
- Neuroscience
- Genomics
- Developmental Biology
Background:
- Maternal smoking during pregnancy is a significant public health issue with known effects on early child development.
- Limited understanding exists regarding prenatal maternal smoking's impact on human cortical biology.
- Prenatal brain development exhibits unique sensitivities to environmental exposures.
Purpose of the Study:
- To investigate the genome-wide differential gene expression in the human prenatal cortex due to maternal smoking.
- To compare the effects of prenatal smoke exposure with direct adult smoking on cortical gene expression.
- To explore the relationship between prenatal smoking, gene expression, and the risk of neuropsychiatric disorders.
Main Methods:
- Genome-wide differential gene expression analysis using RNA sequencing (RNA-seq).
- Analysis of postmortem human prefrontal cortices from prenatal (N=33) and adult (N=207) cohorts.
- Comparison of gene expression patterns between smoking-exposed and non-exposed individuals across different life stages.
Main Results:
- Prenatal smoke exposure was associated with differential expression in 14 genes, compared to only 2 in adults.
- Significant differences in gene expression effects were observed between prenatal and adult smoking exposures (1,315 genes).
- Prenatal smoking-associated genes were enriched in pathways related to addiction, synaptic function, and autism spectrum disorder (ASD).
Conclusions:
- The developing brain shows heightened sensitivity to the biological effects of smoking exposure.
- Maternal smoking during pregnancy profoundly impacts prenatal human cortical gene expression.
- Prenatal smoke exposure may contribute to the heightened risk of subsequent neuropsychiatric disorders, including ASD.
Abstract:
Cigarette smoking during pregnancy is a major public health concern. While there are well-described consequences in early child development, there is very little known about the effects of maternal smoking on human cortical biology during prenatal life. We therefore performed a genome-wide differential gene expression analysis using RNA sequencing (RNA-seq) on prenatal (N = 33; 16 smoking-exposed) as well as adult (N = 207; 57 active smokers) human postmortem prefrontal cortices. Smoking exposure during the prenatal period was directly associated with differential expression of 14 genes; in contrast, during adulthood, despite a much larger sample size, only two genes showed significant differential expression (FDR < 10%). Moreover, 1,315 genes showed significantly different exposure effects between maternal smoking during pregnancy and direct exposure in adulthood (FDR < 10%)-these differences were largely driven by prenatal differences that were enriched for pathways previously implicated in addiction and synaptic function. Furthermore, prenatal and age-dependent differentially expressed genes were enriched for genes implicated in non-syndromic autism spectrum disorder (ASD) and were differentially expressed as a set between patients with ASD and controls in postmortem cortical regions. These results underscore the enhanced sensitivity to the biological effect of smoking exposure in the developing brain and offer insight into how maternal smoking during pregnancy affects gene expression in the prenatal human cortex. They also begin to address the relationship between in utero exposure to smoking and the heightened risks for the subsequent development of neuropsychiatric disorders.
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