High-Fat Diet Reprograms the Epigenome of Rat Spermatozoa and Transgenerationally Affects Metabolism of the Offspring
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OBJECTIVES: Chronic and high consumption of fat constitutes an environmental stress that leads to metabolic diseases. We hypothesized that high-fat diet (HFD) transgenerationally remodels the epigenome of spermatozoa and metabolism of the offspring. METHODS: F0-male rats fed either HFD or chow diet for 12 weeks were mated with chow-fed dams to generate F1 and F2 offspring. Motile spermatozoa were isolated from F0 and F1 breeders to determine DNA methylation and small non-coding RNA (sncRNA) expression pattern by deep sequencing. RESULTS: Newborn offspring of HFD-fed fathers had reduced body weight and pancreatic beta-cell mass. Adult female, but not male, offspring of HFD-fed fathers were glucose intolerant and resistant to HFD-induced weight gain. This phenotype was perpetuated in the F2 progeny, indicating transgenerational epigenetic inheritance. The epigenome of spermatozoa from HFD-fed F0 and their F1 male offspring showed common DNA methylation and small non-coding RNA expression signatures. Altered expression of sperm miRNA let-7c was passed down to metabolic tissues of the offspring, inducing a transcriptomic shift of the let-7c predicted targets. CONCLUSION: Our results provide insight into mechanisms by which HFD transgenerationally reprograms the epigenome of sperm cells, thereby affecting metabolic tissues of offspring throughout two generations.
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Molecular analyses confirmed histone modifications in the promoter regions of leptin and adiponectin, including reduced H3K9 acetylation and increased H3K9 demethylation and H4K20 monomethylation, consistent with altered gene transcription and circulating adipokine levels.
“Molecular analyses confirmed histone modifications in the promoter regions of leptin and adiponectin, including reduced H3K9 acetylation and increased H3K9 demethylation and H4K20 monomethylation, consistent with altered gene transcription and circulating adipokine levels [176].”
From Maternal Overnutrition and Fetal Programming: Long-Term Metabolic, Cognitive, and Epigenetic Consequences (2026) · cites this paper as [176]
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- Authors
- de Castro Barbosa, T., Ingerslev, L. R., Alm, P. S., Versteyhe, S., Massart, J., Rasmussen, M., Donkin, I., Sjögren, R., Mudry, J. M., Vetterli, L., Gupta, S., Krook, A., Zierath, J. R., & Barrès, R.
- Affiliations
- University of Copenhagen (DK)
- Karolinska Institutet (SE)
- Corresponding author
- Barrès, Romain
- ORCID
- Venue
- Molecular Metabolism
- Publisher
- Elsevier BV
- Published
- 2016-03
- Volume
- 5
- Issue
- 3
- Pages
- 184-197
- ISSN
- 2212-8778 (ISSN-L)
- PMC
- PMC4770269
- OpenAlex
- W2203634181
- Cited by
- 417
- References
- 42
- Citations by year
- 2026: 22 · 2025: 30 · 2024: 52 · 2023: 40 · 2022: 38 · 2021: 58 · 2020: 38 · 2019: 44 · 2018: 45 · 2017: 35 · 2016: 14 · 2014: 1
- FWCI
- 31.29
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Molecular Metabolism (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Karolinska Institutet
- Vetenskapsrådet (2009-1068, 2011-3550)
- Diabetesförbundet (DIA2012-082)
- European Research Council (233285)
- Novo Nordisk Fonden
- Fredrik och Ingrid Thurings Stiftelse (4-3202/2013)
- Stiftelsen för Strategisk Forskning (10-0027)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Keywords
- high-fat diet, transgenerational epigenetic inheritance, sperm epigenome, DNA methylation, small RNA, let-7c microRNA, paternal diet, insulin resistance, beta-cell mass, body weight, metabolic reprogramming, spermatozoa
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