Paternal undernutrition and overnutrition modify semen composition and preimplantation embryo developmental kinetics in mice

Morgan, HL, Eid, N, Holmes, N, Henson, S, Wright, V, Coveney, C, Winder, C, O’Neil, DM, Dunn, WB, Boocock, DJ ORCID logoORCID: https://orcid.org/0000-0002-7333-3549 and Watkins, AJ, 2024. Paternal undernutrition and overnutrition modify semen composition and preimplantation embryo developmental kinetics in mice. BMC Biology, 22: 207. ISSN 1741-7007

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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 foetal 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.

Item Type: Journal article
Publication Title: BMC Biology
Creators: 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. and Watkins, A.J.
Publisher: Springer Science and Business Media LLC
Date: 2024
Volume: 22
ISSN: 1741-7007
Identifiers:
Number
Type
10.1186/s12915-024-01992-0
DOI
2277748
Other
Rights: © The Author(s) 2024. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/
Divisions: Schools > School of Science and Technology
Record created by: Laura Ward
Date Added: 04 Dec 2024 09:08
Last Modified: 04 Dec 2024 09:08
URI: https://irep.ntu.ac.uk/id/eprint/52691

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