Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress
Open accessAbstract
Significance: Studies examining paternal exposure to diverse environmental stimuli propose that epigenetic marks in germ cells, including small noncoding RNAs such as microRNA (miR), transmit experience-dependent information from parent to offspring. However, these nongenetic mechanisms of transgenerational inheritance are poorly understood, specifically how these germ-cell marks may act postfertilization to enact long-term changes in offspring behavior or physiology. In this study, through zygote microinjection of nine specific sperm miRs previously identified in our paternal stress mouse model, we demonstrate that sperm miRs function to reduce maternal mRNA stores in early zygotes, ultimately reprogramming gene expression in the offspring hypothalamus and recapitulating the offspring stress dysregulation phenotype.
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Studies of environmentally driven histone modifications and long noncoding RNAs have almost exclusively been done in animal models, with a few exceptions in human cohorts.
“This has almost exclusively been done in animal models, 63 , 64 , 65 , 66 with a few exceptions of studies in human cohorts. 67”
From Epigenetics and depression (2019) · cites this paper as [64]
The Abstract describes a mouse model of paternal stress, supporting this paper as an example of animal-model research on environmentally responsive epigenetic marks. The study tests sperm microRNAs, not long noncoding RNAs or histone modifications; its Discussion mentions histone modifications only as background. It does not establish that this research has been done almost exclusively in animals. (LLM, conf=0.83)
Experimental — accuracy not yet measuredA few studies have shown environmentally driven changes in the epigenetic landscape via histone modifications and long noncoding RNAs.
“Nonetheless, a few studies have shown environmentally driven changes of the epigenetic landscape in other ways, such as via histone modifications and long noncoding RNAs.”
From Epigenetics and depression (2019) · cites this paper as [64]
The Discussion (page unavailable) reports environmentally associated changes in sperm epigenetic marks, including histone modifications. It discusses small noncoding RNAs, particularly microRNAs, but does not support the claim about long noncoding RNAs. (LLM, conf=0.87)
Experimental — accuracy not yet measuredA mechanistic role for sperm microRNAs in the transgenerational transmission of stress reactivity to the offspring has been demonstrated.
“and a mechanistic role for sperm microRNAs in the transgenerational transmission of stress reactivity to the offspring has also been demonstrated [70].”
Animal studies provide compelling evidence for the transgenerational transmission and inheritance of environmentally acquired risk factors across generations via the germline, with epigenetic mechanisms strongly implicated.
“They provide some compelling evidence for the transgenerational transmission and inheritance of environmentally acquired risk factors across generations via the germline [69], with epigenetic mechanisms strongly implicated [70].”
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- Authors
- Rodgers, A. B., Morgan, C. P., Leu, N. A., & Bale, T. L.
- Affiliations
- University of Pennsylvania (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2015-10-19
- Volume
- 112
- Issue
- 44
- Pages
- 13699-13704
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4640733
- OpenAlex
- W1949928978
- Cited by
- 751
- References
- 48
- Citations by year
- 2026: 50 · 2025: 40 · 2024: 54 · 2023: 74 · 2022: 69 · 2021: 70 · 2020: 81 · 2019: 67 · 2018: 107 · 2017: 72 · 2016: 61 · 2015: 3
- FWCI
- 35.19
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Institute of Mental Health (MH073030, MH091258, MH087597, MH099910, MH104184)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Keywords
- sperm microRNA, paternal stress, chronic stress, hypothalamic-pituitary-adrenal axis, zygote microinjection, blood-brain barrier permeability, extracellular matrix, collagen, maternal mRNA degradation, SIRT1, chromatin remodeling, germ cells, single-cell transcriptomics
- MeSH terms
- Animals, Hypothalamo-Hypophyseal System, Male, Mice, Inbred C57BL, Spermatozoa, Stress, Physiological, Paternal Exposure, MicroRNAs, Epigenesis, Genetic, Mice, Transcriptome
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