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Featured ArticleArticles, Behavioral/Cognitive

Paternal Stress Exposure Alters Sperm MicroRNA Content and Reprograms Offspring HPA Stress Axis Regulation

Ali B. Rodgers, Christopher P. Morgan, Stefanie L. Bronson, Sonia Revello and Tracy L. Bale
Journal of Neuroscience 22 May 2013, 33 (21) 9003-9012; DOI: https://doi.org/10.1523/JNEUROSCI.0914-13.2013
Ali B. Rodgers
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania Philadelphia, Pennsylvania 19104
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Christopher P. Morgan
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania Philadelphia, Pennsylvania 19104
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Stefanie L. Bronson
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania Philadelphia, Pennsylvania 19104
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Sonia Revello
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania Philadelphia, Pennsylvania 19104
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Tracy L. Bale
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania Philadelphia, Pennsylvania 19104
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Abstract

Neuropsychiatric disease frequently presents with an underlying hyporeactivity or hyperreactivity of the HPA stress axis, suggesting an exceptional vulnerability of this circuitry to external perturbations. Parental lifetime exposures to environmental challenges are associated with increased offspring neuropsychiatric disease risk, and likely contribute to stress dysregulation. While maternal influences have been extensively examined, much less is known regarding the specific role of paternal factors. To investigate the potential mechanisms by which paternal stress may contribute to offspring hypothalamic–pituitary–adrenal (HPA) axis dysregulation, we exposed mice to 6 weeks of chronic stress before breeding. As epidemiological studies support variation in paternal germ cell susceptibility to reprogramming across the lifespan, male stress exposure occurred either throughout puberty or in adulthood. Remarkably, offspring of sires from both paternal stress groups displayed significantly reduced HPA stress axis responsivity. Gene set enrichment analyses in offspring stress regulating brain regions, the paraventricular nucleus (PVN) and the bed nucleus of stria terminalis, revealed global pattern changes in transcription suggestive of epigenetic reprogramming and consistent with altered offspring stress responsivity, including increased expression of glucocorticoid-responsive genes in the PVN. In examining potential epigenetic mechanisms of germ cell transmission, we found robust changes in sperm microRNA (miR) content, where nine specific miRs were significantly increased in both paternal stress groups. Overall, these results demonstrate that paternal experience across the lifespan can induce germ cell epigenetic reprogramming and impact offspring HPA stress axis regulation, and may therefore offer novel insight into factors influencing neuropsychiatric disease risk.

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The Journal of Neuroscience: 33 (21)
Journal of Neuroscience
Vol. 33, Issue 21
22 May 2013
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Paternal Stress Exposure Alters Sperm MicroRNA Content and Reprograms Offspring HPA Stress Axis Regulation
Ali B. Rodgers, Christopher P. Morgan, Stefanie L. Bronson, Sonia Revello, Tracy L. Bale
Journal of Neuroscience 22 May 2013, 33 (21) 9003-9012; DOI: 10.1523/JNEUROSCI.0914-13.2013

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Paternal Stress Exposure Alters Sperm MicroRNA Content and Reprograms Offspring HPA Stress Axis Regulation
Ali B. Rodgers, Christopher P. Morgan, Stefanie L. Bronson, Sonia Revello, Tracy L. Bale
Journal of Neuroscience 22 May 2013, 33 (21) 9003-9012; DOI: 10.1523/JNEUROSCI.0914-13.2013
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