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Article

Early-Life Exposure to Environmental Contaminants Perturbs the Sperm Epigenome and Induces Negative Pregnancy Outcomes for Three Generations via the Paternal Lineage

1
Research Centre on Reproduction and Intergenerational Health, Department of Animal Sciences, Université Laval, Quebec City, QC G1V 0A6, Canada
2
Department of Animal Sciences, McGill University, Ste. Anne de Bellevue, Quebec, QC H9X 3V9, Canada
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Department of Pharmacology and Therapeutics, McGill University, Montreal, QC H3G 1Y6, Canada
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Department of Molecular Medicine, Research Center of CHU of Quebec City, Université Laval, Quebec City, QC G1V 4G, Canada
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Research Center of CHU Sainte-Justine, Department of Biochemistry and Molecular Medicine, Université de Montral, Montreal, QC H3T 1C5, Canada
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Research Institute of the McGill University Health Centre, Montreal, QC H3Z 2Z3, Canada
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Departments of Pediatrics, Human Genetics and Pharmacology & Therapeutics, McGill University, Montreal, QC H3Z 2Z3, Canada
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Institut Universitaire de Cardiologie et de Pneumologie de Québec, Université Laval, Quebec City, QC G1V 4G5, Canada
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Department of Comparative Biosciences, University of Illinois, Urbana-Champaign, IL 61802, USA
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Current address: Cold Spring Harbor Laboratory, New York, NY 11724, USA.
Academic Editors: Olga Kovalchuk, Gerlinde A.S. Metz and Ernesto Guccione
Epigenomes 2021, 5(2), 10; https://doi.org/10.3390/epigenomes5020010
Received: 22 March 2021 / Accepted: 27 April 2021 / Published: 1 May 2021
(This article belongs to the Special Issue Health and Disease through A Sex and Gender Lens)
Due to the grasshopper effect, the Arctic food chain in Canada is contaminated with persistent organic pollutants (POPs) of industrial origin, including polychlorinated biphenyls and organochlorine pesticides. Exposure to POPs may be a contributor to the greater incidence of poor fetal growth, placental abnormalities, stillbirths, congenital defects and shortened lifespan in the Inuit population compared to non-Aboriginal Canadians. Although maternal exposure to POPs is well established to harm pregnancy outcomes, paternal transmission of the effects of POPs is a possibility that has not been well investigated. We used a rat model to test the hypothesis that exposure to POPs during gestation and suckling leads to developmental defects that are transmitted to subsequent generations via the male lineage. Indeed, developmental exposure to an environmentally relevant Arctic POPs mixture impaired sperm quality and pregnancy outcomes across two subsequent, unexposed generations and altered sperm DNA methylation, some of which are also observed for two additional generations. Genes corresponding to the altered sperm methylome correspond to health problems encountered in the Inuit population. These findings demonstrate that the paternal methylome is sensitive to the environment and that some perturbations persist for at least two subsequent generations. In conclusion, although many factors influence health, paternal exposure to contaminants plays a heretofore-underappreciated role with sperm DNA methylation contributing to the molecular underpinnings involved. View Full-Text
Keywords: persistent organic pollutants (POPs); sperm methylome; intergenerational; transgenerational; epigenetic; paternal transmission; Inuit persistent organic pollutants (POPs); sperm methylome; intergenerational; transgenerational; epigenetic; paternal transmission; Inuit
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MDPI and ACS Style

Maurice, C.; Dalvai, M.; Lambrot, R.; Deschênes, A.; Scott-Boyer, M.-P.; McGraw, S.; Chan, D.; Côté, N.; Ziv-Gal, A.; Flaws, J.A.; Droit, A.; Trasler, J.; Kimmins, S.; Bailey, J.L. Early-Life Exposure to Environmental Contaminants Perturbs the Sperm Epigenome and Induces Negative Pregnancy Outcomes for Three Generations via the Paternal Lineage. Epigenomes 2021, 5, 10. https://doi.org/10.3390/epigenomes5020010

AMA Style

Maurice C, Dalvai M, Lambrot R, Deschênes A, Scott-Boyer M-P, McGraw S, Chan D, Côté N, Ziv-Gal A, Flaws JA, Droit A, Trasler J, Kimmins S, Bailey JL. Early-Life Exposure to Environmental Contaminants Perturbs the Sperm Epigenome and Induces Negative Pregnancy Outcomes for Three Generations via the Paternal Lineage. Epigenomes. 2021; 5(2):10. https://doi.org/10.3390/epigenomes5020010

Chicago/Turabian Style

Maurice, Clotilde, Mathieu Dalvai, Romain Lambrot, Astrid Deschênes, Marie-Pier Scott-Boyer, Serge McGraw, Donovan Chan, Nancy Côté, Ayelet Ziv-Gal, Jodi A. Flaws, Arnaud Droit, Jacquetta Trasler, Sarah Kimmins, and Janice L. Bailey 2021. "Early-Life Exposure to Environmental Contaminants Perturbs the Sperm Epigenome and Induces Negative Pregnancy Outcomes for Three Generations via the Paternal Lineage" Epigenomes 5, no. 2: 10. https://doi.org/10.3390/epigenomes5020010

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