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Developmental effects of maternal smoking during pregnancy on the human frontal cortex transcriptome

Stephen A. Semick, Leonardo Collado-Torres, Christina A. Markunas, Joo Heon Shin, Amy Deep-Soboslay, Ran Tao, Laura J. Bierut, Brion S. Maher, Eric O. Johnson, Thomas M. Hyde, Daniel R. Weinberger, Dana B. Hancock, Joel E. Kleinman, Andrew E. Jaffe
doi: https://doi.org/10.1101/236968
Stephen A. Semick
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
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Leonardo Collado-Torres
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
2Center for Computational Biology, Johns Hopkins University, Baltimore, MD, 21205, USA
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Christina A. Markunas
3Behavioral and Urban Health Program, Behavioral Health and Criminal Justice Division, RTI International, Research Triangle Park, NC, 27709, USA
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Joo Heon Shin
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
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Amy Deep-Soboslay
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
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Ran Tao
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
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Laura J. Bierut
4Department of Psychiatry, Washington University School of Medicine, St Louis, MO 63110, USA
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Brion S. Maher
5Department of Mental Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USA
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Eric O. Johnson
6Fellow Program and Behavioral Health and Criminal Justice Division, RTI International, Research Triangle Park, NC, 27709, USA
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Thomas M. Hyde
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
7Department of Psychiatry and Behavioral Sciences, Johns Hopkins School of Medicine, Baltimore, MD 21205, USA
8Department of Neurology, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA
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Daniel R. Weinberger
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
7Department of Psychiatry and Behavioral Sciences, Johns Hopkins School of Medicine, Baltimore, MD 21205, USA
8Department of Neurology, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA
9Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, MD, 21205, USA
10McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins School of Medicine, Baltimore, MD 21205, USA
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Dana B. Hancock
3Behavioral and Urban Health Program, Behavioral Health and Criminal Justice Division, RTI International, Research Triangle Park, NC, 27709, USA
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Joel E. Kleinman
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
7Department of Psychiatry and Behavioral Sciences, Johns Hopkins School of Medicine, Baltimore, MD 21205, USA
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Andrew E. Jaffe
1Lieber Institute for Brain Development, Johns Hopkins Medical Campus, Baltimore, MD, 21205, USA
2Center for Computational Biology, Johns Hopkins University, Baltimore, MD, 21205, USA
5Department of Mental Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USA
10McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins School of Medicine, Baltimore, MD 21205, USA
11Department of Biostatistics, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, 21205, USA
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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 post-mortem 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 2 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 post-mortem cortical regions. These results underscore the enhanced sensitivity to the biological effect of smoking exposure in the developing brain and offer novel insight into the effects of maternal smoking during pregnancy on the prenatal human brain. They also begin to address the relationship between in utero exposure to smoking and the heightened risks for the subsequent development of neuropsychiatric disorders.

One Sentence Summary Maternal smoking during pregnancy alters the expression of genes within the developing human cortex and these changes are enriched for genes implicated in neuropsychiatric disorders.

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Posted December 20, 2017.
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Developmental effects of maternal smoking during pregnancy on the human frontal cortex transcriptome
Stephen A. Semick, Leonardo Collado-Torres, Christina A. Markunas, Joo Heon Shin, Amy Deep-Soboslay, Ran Tao, Laura J. Bierut, Brion S. Maher, Eric O. Johnson, Thomas M. Hyde, Daniel R. Weinberger, Dana B. Hancock, Joel E. Kleinman, Andrew E. Jaffe
bioRxiv 236968; doi: https://doi.org/10.1101/236968
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Developmental effects of maternal smoking during pregnancy on the human frontal cortex transcriptome
Stephen A. Semick, Leonardo Collado-Torres, Christina A. Markunas, Joo Heon Shin, Amy Deep-Soboslay, Ran Tao, Laura J. Bierut, Brion S. Maher, Eric O. Johnson, Thomas M. Hyde, Daniel R. Weinberger, Dana B. Hancock, Joel E. Kleinman, Andrew E. Jaffe
bioRxiv 236968; doi: https://doi.org/10.1101/236968

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