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Subchronic elevation in ambient temperature drives alterations to the sperm epigenome and accelerates early embryonic development in mice6.34 MB
Published VersionCC BY-NC-ND V4.0, Open Access
Journal article
Subchronic elevation in ambient temperature drives alterations to the sperm epigenome and accelerates early embryonic development in mice
National Academy of Sciences. Proceedings, Vol.121(47), pp.1-12
2024
PMID: 39527742
Abstract
Forecasted increases in the prevalence and severity of extreme weather events accompanying changes in climatic behavior pose potential risk to the reproductive capacity of humans and animals of ecological and agricultural significance. While several studies have revealed that heat stress induced by challenges such as testicular insulation can elicit a marked negative effect on the male reproductive system, and particularly the production of spermatozoa, less is known about the immediate impact on male reproductive function following subchronic whole-body exposure to elevated ambient temperature. To address this knowledge gap, we exposed unrestrained male mice to heat stress conditions that emulate a heat wave (daily cycle of 8 h at 35 °C followed by 16 h at 25 °C) for a period of 7 d. Neither the testes or epididymides of heat-exposed male mice exhibited evidence of gross histological change, and similarly, spermatozoa of exposed males retained their functionality and ability to support embryonic development. However, the embryos generated from heat-exposed spermatozoa experienced pronounced changes in gene expression linked to acceleration of early embryo development, aberrant blastocyst hatching, and increased fetal:placental weight ratio. Such changes were causally associated with an altered sperm small noncoding RNA (sncRNA) profile, such that these developmental phenotypes were recapitulated by microinjection of wild-type embryos sired by control spermatozoa with RNAs extracted from heat-exposed spermatozoa. Such data highlight that even relatively modest excursions in ambient temperature can affect male reproductive function and identify the sperm sncRNA profile as a particular point of vulnerability to this imposed environmental stress.
Details
- Title
- Subchronic elevation in ambient temperature drives alterations to the sperm epigenome and accelerates early embryonic development in mice
- Authors
- Natalie Trigg - University of Newcastle AustraliaJohn E. Schjenken - University of Newcastle AustraliaJacinta H. Martin - University of Newcastle AustraliaDavid A. Skerrett-Byrne - University of Newcastle AustraliaShannon P. Smyth - University of Newcastle AustraliaIlana R. Bernstein - University of Newcastle AustraliaAmanda L. Anderson - University of Newcastle AustraliaSimone J. Stanger - University of Newcastle AustraliaEwan N. A. Simpson - University of Newcastle AustraliaArchana Tomar - Helmholtz Zentrum MünchenRaffaele Teperino - Helmholtz Zentrum MünchenColin C. Conine - University of Newcastle AustraliaGeoffry N. De Iuliis - University of Newcastle AustraliaShaun D. Roman - Hunter Medical Research InstituteElizabeth G. Bromfield - University of Newcastle AustraliaMatthew D. Dun - University of Newcastle AustraliaAndrew L. Eamens - University of the Sunshine Coast, Queensland, School of Health - BiomedicineBrett Nixon (Corresponding Author) - University of Newcastle Australia
- Publication details
- National Academy of Sciences. Proceedings, Vol.121(47), pp.1-12
- Publisher
- National Academy of Sciences
- Date published
- 2024
- DOI
- 10.1073/pnas.2409790121
- ISSN
- 1091-6490; 0027-8424
- PMID
- 39527742
- Copyright note
- Copyright © 2024 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
- Data Availability
- Raw and processed sequencing data have been deposited in NCBI’s Gene Expression Omnibus and are accessible via the following accession GSE252418 (86). All other data are included in the article and/or SI Appendix.
- Grants
- Grant note
- M.D.D. is the recipient a Defeat Diffuse Intrinsic Pontine Glimoa ChadTough New Investigator Fellowship.
- Organisation Unit
- School of Health - Biomedicine
- Language
- English
- Record Identifier
- 991078385502621
- Output Type
- Journal article
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