Stress increases sperm respiration and motility in mice and men

Nickole Moon, Christopher P. Morgan, Ruth Marx-Rattner, Alyssa Jeng, Rachel L. Johnson, Ijeoma Chikezie, Carmen Mannella, Mary D. Sammel, C. Neill Epperson and Tracy L. Bale ()
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Nickole Moon: University of Colorado Anschutz Medical Campus School of Medicine
Christopher P. Morgan: University of Maryland Baltimore
Ruth Marx-Rattner: University of Maryland Baltimore
Alyssa Jeng: University of Colorado Anschutz Medical Campus School of Medicine
Rachel L. Johnson: University of Colorado Anschutz Medical Campus
Ijeoma Chikezie: University of Maryland Baltimore
Carmen Mannella: University of Maryland Baltimore
Mary D. Sammel: University of Colorado Anschutz Medical Campus
C. Neill Epperson: University of Colorado Anschutz Medical Campus School of Medicine
Tracy L. Bale: University of Colorado Anschutz Medical Campus School of Medicine

Nature Communications, 2024, vol. 15, issue 1, 1-20

Abstract: Abstract Semen quality and fertility has declined over the last 50 years, corresponding to ever-increasing environmental stressors. However, the cellular mechanisms involved and their impact on sperm functions remain unknown. In a repeated sampling human cohort study, we identify a significant effect of prior perceived stress to increase sperm motility 2-3 months following stress, timing that expands upon our previous studies revealing significant stress-associated changes in sperm RNA important for fertility. We mechanistically examine this post-stress timing in mice using an in vitro stress model in the epididymal epithelial cells responsible for sperm maturation and find 7282 differentially H3K27me3 bound DNA regions involving genes critical for mitochondrial and metabolic pathways. Further, prior stress exposure significantly changes the composition and size of epithelial cell-secreted extracellular vesicles that when incubated with mouse sperm, increase mitochondrial respiration and sperm motility, adding to our prior work showing impacts on embryo development. Together, these studies identify a time-dependent, translational signaling pathway that communicates stress experience to sperm, ultimately affecting reproductive functions.

Date: 2024
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DOI: 10.1038/s41467-024-52319-0

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