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Paternal under and over nutrition modify semen composition and preimplantation embryo developmental kinetics in mice

Morgan, Hannah L.; Eid, Nader; Holmes, Nadine; Henson, Sonal; Wright, Victoria; Coveney, Clare; Winder, Catherine; O’Neil, Donna M.; Dunn, Warwick B.; Boocock, David J.; Watkins, Adam J.

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Authors

Hannah L. Morgan

Nader Eid

Nadine Holmes

Victoria Wright

Clare Coveney

Catherine Winder

Donna M. O’Neil

Warwick B. Dunn

David J. Boocock

Adam J. Watkins



Abstract

Background: The importance of parental diet in relation to eventual offspring health is increasing in prominence due to the increased frequency of parents of reproductive age consuming poor diets. Whilst maternal health and offspring outcome have been studied in some detail, the paternal impacts are not as well understood. A father’s poor nutritional status has been shown to have negative consequences on fetal growth and development and ultimately impact the long-term adult health of the offspring. In this study, we examined sperm- and seminal vesicle fluid-mediated mechanisms of preimplantation embryo development alterations in response to sub-optimal paternal diets.

Results: Male mice were fed a diet to model either under (low protein diet (LPD)) or over (high fat/sugar ‘Western’ diet (WD)) nutrition, LPD or WD supplemented with methyl-donors or a control diet (CD) before mating with age-matched females. Male metabolic health was influenced by WD and MD-WD; with significant changes in multiple serum lipid classes and hepatic 1-carbon metabolites. Sperm RNA sequencing revealed significant changes to mRNA profiles in all groups when compared to CD (LPD: 32, MD-LPD: 17, WD: 53, MD-WD: 35 transcripts). Separate analysis of the seminal vesicle fluid proteome revealed a significant number of differentially expressed proteins in all groups (LPD: 13, MD-LPD: 27, WD: 24, MD-WD: 19) when compared to control. Following mating, in vitro time-lapse imaging of preimplantation embryos revealed a significant increase in the timing of development in all experimental groups when compared to CD embryos. Finally, qPCR analysis of uterine tissue at the time of implantation identified perturbed expression of Cd14 and Ptgs1 following mating with WD fed males.

Conclusions: Our current study shows that paternal nutritional status has the potential to influence male metabolic and reproductive health, impacting on embryonic development and the maternal reproductive tract. This study highlights potential direct (sperm-mediated) and indirect (seminal vesicle fluid-mediated) pathways in which a father's poor diet could shape the long-term health of his offspring.

Citation

Morgan, H. L., Eid, N., Holmes, N., Henson, S., Wright, V., Coveney, C., Winder, C., O’Neil, D. M., Dunn, W. B., Boocock, D. J., & Watkins, A. J. (2024). Paternal under and over nutrition modify semen composition and preimplantation embryo developmental kinetics in mice. BMC Biology, 22, Article 207. https://doi.org/10.1186/s12915-024-01992-0

Journal Article Type Article
Acceptance Date Aug 24, 2024
Online Publication Date Sep 16, 2024
Publication Date Sep 16, 2024
Deposit Date Sep 4, 2024
Publicly Available Date Sep 16, 2024
Journal BMC Biology
Electronic ISSN 1741-7007
Publisher Springer Verlag
Peer Reviewed Peer Reviewed
Volume 22
Article Number 207
DOI https://doi.org/10.1186/s12915-024-01992-0
Keywords Paternal diet, Sperm RNA, Semen profle, Embryo development, Uterine response
Public URL https://nottingham-repository.worktribe.com/output/39169641

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