Placental DNA methylation signatures of maternal smoking during pregnancy and potential impacts on fetal growth

Todd M. Everson; Marta Vives-Usano; Emie Seyve; Andres Cardenas; Marina Lacasaña; Jeffrey M. Craig; Corina Lesseur; Emily R. Baker; Nora Fernandez-Jimenez; Barbara Heude; Patrice Perron; Beatriz Gónzalez-Alzaga; Jane Halliday; Maya A. Deyssenroth; Margaret R. Karagas; Carmen Íñiguez; Luigi Bouchard; Pedro Carmona-Sáez; Yuk J. Loke; Ke Hao; Thalia Belmonte; Marie A. Charles; Jordi Martorell-Marugán; Evelyne Muggli; Jia Chen; Mariana F. Fernández; Jorg Tost; Antonio Gómez-Martín; Stephanie J. London; Jordi Sunyer; Carmen J. Marsit; Johanna Lepeule; Marie France Hivert; Mariona Bustamante

doi:10.1038/s41467-021-24558-y

Placental DNA methylation signatures of maternal smoking during pregnancy and potential impacts on fetal growth

Todd M. Everson^*
, Marta Vives-Usano
, Emie Seyve
, Andres Cardenas
, Marina Lacasaña
, Jeffrey M. Craig
, Corina Lesseur
, Emily R. Baker
, Nora Fernandez-Jimenez
, Barbara Heude
, Patrice Perron
, Beatriz Gónzalez-Alzaga
, Jane Halliday
, Maya A. Deyssenroth
, Margaret R. Karagas
, Carmen Íñiguez
, Luigi Bouchard
, Pedro Carmona-Sáez
, Yuk J. Loke
, Ke Hao

Thalia Belmonte, Marie A. Charles, Jordi Martorell-Marugán, Evelyne Muggli, Jia Chen, Mariana F. Fernández, Jorg Tost, Antonio Gómez-Martín, Stephanie J. London, Jordi Sunyer, Carmen J. Marsit, Johanna Lepeule, Marie France Hivert, Mariona Bustamante^*

^*Autor correspondiente de este trabajo

Emory University
Barcelona Institute of Science and Technology (BIST)
Université Grenoble Alpes
Harvard University
University of California at Berkeley
Escuela Andaluza de Salud Publica
Instituto de Investigación Biosantaria (ibs.GRANADA)
Murdoch Children's Research Institute
Department of Paediatrics
Deakin University
Icahn School of Medicine at Mount Sinai
Dartmouth College
Biocruces Health Research Institute
Public Health Division of Gipuzkoa
Institut national de la santé et de la recherche médicale
Université de Sherbrooke
University of Valencia
Jaume I University
University of Granada
University of Oviedo
Atrys Health
Centre National de Recherche en Génomique Humaine
National Institutes of Health
Massachusetts General Hospital

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67 Citas (Scopus)

Resumen

Maternal smoking during pregnancy (MSDP) contributes to poor birth outcomes, in part through disrupted placental functions, which may be reflected in the placental epigenome. Here we present a meta-analysis of the associations between MSDP and placental DNA methylation (DNAm) and between DNAm and birth outcomes within the Pregnancy And Childhood Epigenetics (PACE) consortium (N = 1700, 344 with MSDP). We identify 443 CpGs that are associated with MSDP, of which 142 associated with birth outcomes, 40 associated with gene expression, and 13 CpGs are associated with all three. Only two CpGs have consistent associations from a prior meta-analysis of cord blood DNAm, demonstrating substantial tissue-specific responses to MSDP. The placental MSDP-associated CpGs are enriched for environmental response genes, growth-factor signaling, and inflammation, which play important roles in placental function. We demonstrate links between placental DNAm, MSDP and poor birth outcomes, which may better inform the mechanisms through which MSDP impacts placental function and fetal growth.

Idioma original	Inglés
Número de artículo	5095
Publicación	Nature Communications
Volumen	12
N.º	1
DOI	https://doi.org/10.1038/s41467-021-24558-y
Estado	Publicada - 1 dic 2021
Publicado de forma externa	Sí

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Everson, T. M., Vives-Usano, M., Seyve, E., Cardenas, A., Lacasaña, M., Craig, J. M., Lesseur, C., Baker, E. R., Fernandez-Jimenez, N., Heude, B., Perron, P., Gónzalez-Alzaga, B., Halliday, J., Deyssenroth, M. A., Karagas, M. R., Íñiguez, C., Bouchard, L., Carmona-Sáez, P., Loke, Y. J., ... Bustamante, M. (2021). Placental DNA methylation signatures of maternal smoking during pregnancy and potential impacts on fetal growth. Nature Communications, 12(1), Artículo 5095. https://doi.org/10.1038/s41467-021-24558-y

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title = "Placental DNA methylation signatures of maternal smoking during pregnancy and potential impacts on fetal growth",

abstract = "Maternal smoking during pregnancy (MSDP) contributes to poor birth outcomes, in part through disrupted placental functions, which may be reflected in the placental epigenome. Here we present a meta-analysis of the associations between MSDP and placental DNA methylation (DNAm) and between DNAm and birth outcomes within the Pregnancy And Childhood Epigenetics (PACE) consortium (N = 1700, 344 with MSDP). We identify 443 CpGs that are associated with MSDP, of which 142 associated with birth outcomes, 40 associated with gene expression, and 13 CpGs are associated with all three. Only two CpGs have consistent associations from a prior meta-analysis of cord blood DNAm, demonstrating substantial tissue-specific responses to MSDP. The placental MSDP-associated CpGs are enriched for environmental response genes, growth-factor signaling, and inflammation, which play important roles in placental function. We demonstrate links between placental DNAm, MSDP and poor birth outcomes, which may better inform the mechanisms through which MSDP impacts placental function and fetal growth.",

author = "Everson, \{Todd M.\} and Marta Vives-Usano and Emie Seyve and Andres Cardenas and Marina Lacasa{\~n}a and Craig, \{Jeffrey M.\} and Corina Lesseur and Baker, \{Emily R.\} and Nora Fernandez-Jimenez and Barbara Heude and Patrice Perron and Beatriz G{\'o}nzalez-Alzaga and Jane Halliday and Deyssenroth, \{Maya A.\} and Karagas, \{Margaret R.\} and Carmen {\'I}{\~n}iguez and Luigi Bouchard and Pedro Carmona-S{\'a}ez and Loke, \{Yuk J.\} and Ke Hao and Thalia Belmonte and Charles, \{Marie A.\} and Jordi Martorell-Marug{\'a}n and Evelyne Muggli and Jia Chen and Fern{\'a}ndez, \{Mariana F.\} and Jorg Tost and Antonio G{\'o}mez-Mart{\'i}n and London, \{Stephanie J.\} and Jordi Sunyer and Marsit, \{Carmen J.\} and Johanna Lepeule and Hivert, \{Marie France\} and Mariona Bustamante",

note = "Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = dec,

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doi = "10.1038/s41467-021-24558-y",

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Everson, TM, Vives-Usano, M, Seyve, E, Cardenas, A, Lacasaña, M, Craig, JM, Lesseur, C, Baker, ER, Fernandez-Jimenez, N, Heude, B, Perron, P, Gónzalez-Alzaga, B, Halliday, J, Deyssenroth, MA, Karagas, MR, Íñiguez, C, Bouchard, L, Carmona-Sáez, P, Loke, YJ, Hao, K, Belmonte, T, Charles, MA, Martorell-Marugán, J, Muggli, E, Chen, J, Fernández, MF, Tost, J, Gómez-Martín, A, London, SJ, Sunyer, J, Marsit, CJ, Lepeule, J, Hivert, MF & Bustamante, M 2021, 'Placental DNA methylation signatures of maternal smoking during pregnancy and potential impacts on fetal growth', Nature Communications, vol. 12, n.º 1, 5095. https://doi.org/10.1038/s41467-021-24558-y

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AU - Everson, Todd M.

AU - Vives-Usano, Marta

AU - Seyve, Emie

AU - Cardenas, Andres

AU - Lacasaña, Marina

AU - Craig, Jeffrey M.

AU - Lesseur, Corina

AU - Baker, Emily R.

AU - Fernandez-Jimenez, Nora

AU - Heude, Barbara

AU - Perron, Patrice

AU - Gónzalez-Alzaga, Beatriz

AU - Halliday, Jane

AU - Deyssenroth, Maya A.

AU - Karagas, Margaret R.

AU - Íñiguez, Carmen

AU - Bouchard, Luigi

AU - Carmona-Sáez, Pedro

AU - Loke, Yuk J.

AU - Hao, Ke

AU - Belmonte, Thalia

AU - Charles, Marie A.

AU - Martorell-Marugán, Jordi

AU - Muggli, Evelyne

AU - Chen, Jia

AU - Fernández, Mariana F.

AU - Tost, Jorg

AU - Gómez-Martín, Antonio

AU - London, Stephanie J.

AU - Sunyer, Jordi

AU - Marsit, Carmen J.

AU - Lepeule, Johanna

AU - Hivert, Marie France

AU - Bustamante, Mariona

PY - 2021/12/1

Y1 - 2021/12/1

N2 - Maternal smoking during pregnancy (MSDP) contributes to poor birth outcomes, in part through disrupted placental functions, which may be reflected in the placental epigenome. Here we present a meta-analysis of the associations between MSDP and placental DNA methylation (DNAm) and between DNAm and birth outcomes within the Pregnancy And Childhood Epigenetics (PACE) consortium (N = 1700, 344 with MSDP). We identify 443 CpGs that are associated with MSDP, of which 142 associated with birth outcomes, 40 associated with gene expression, and 13 CpGs are associated with all three. Only two CpGs have consistent associations from a prior meta-analysis of cord blood DNAm, demonstrating substantial tissue-specific responses to MSDP. The placental MSDP-associated CpGs are enriched for environmental response genes, growth-factor signaling, and inflammation, which play important roles in placental function. We demonstrate links between placental DNAm, MSDP and poor birth outcomes, which may better inform the mechanisms through which MSDP impacts placental function and fetal growth.

AB - Maternal smoking during pregnancy (MSDP) contributes to poor birth outcomes, in part through disrupted placental functions, which may be reflected in the placental epigenome. Here we present a meta-analysis of the associations between MSDP and placental DNA methylation (DNAm) and between DNAm and birth outcomes within the Pregnancy And Childhood Epigenetics (PACE) consortium (N = 1700, 344 with MSDP). We identify 443 CpGs that are associated with MSDP, of which 142 associated with birth outcomes, 40 associated with gene expression, and 13 CpGs are associated with all three. Only two CpGs have consistent associations from a prior meta-analysis of cord blood DNAm, demonstrating substantial tissue-specific responses to MSDP. The placental MSDP-associated CpGs are enriched for environmental response genes, growth-factor signaling, and inflammation, which play important roles in placental function. We demonstrate links between placental DNAm, MSDP and poor birth outcomes, which may better inform the mechanisms through which MSDP impacts placental function and fetal growth.

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SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

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Placental DNA methylation signatures of maternal smoking during pregnancy and potential impacts on fetal growth

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