Reduced levels of miRNAs 449 and 34 in sperm of mice and men exposed to early life stress
Open accessAbstract
Exposure of male mice to early life stress alters the levels of specific sperm miRNAs that promote stress-associated behaviors in their offspring. To begin to evaluate whether similar phenomena occur in men, we searched for sperm miRNA changes that occur in both mice and men exposed to early life stressors that have long-lasting effects. For men, we used the Adverse Childhood Experience (ACE) questionnaire. It reveals the degree of abusive and/or dysfunctional family experiences when young, which increases risks of developing future psychological and physical disorders. For male mice, we used adolescent chronic social instability (CSI) stress, which not only enhances sociability defects for >1 year, but also anxiety and defective sociability in female offspring for multiple generations through the male lineage. Here we found a statistically significant inverse correlation between levels of multiple miRNAs of the miR-449/34 family and ACE scores of Caucasian males. Remarkably, we found members of the same sperm miRNA family are also reduced in mice exposed to CSI stress. Thus, future studies should be designed to directly test whether reduced levels of these miRNAs could be used as unbiased indicators of current and/or early life exposure to severe stress. Moreover, after mating stressed male mice, these sperm miRNA reductions persist in both early embryos through at least the morula stage and in sperm of males derived from them, suggesting these miRNA changes contribute to transmission of stress phenotypes across generations. Since offspring of men exposed to early life trauma have elevated risks for psychological disorders, these findings raise the possibility that a portion of this risk may be derived from epigenetic regulation of these sperm miRNAs.
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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 [67]
The Materials and methods section describes human sperm samples grouped by adverse childhood experience scores, and the Discussion identifies sperm miRNA changes associated with childhood trauma in men. This makes the paper an example of a human study of stress-associated miRNAs, but it does not study histone modifications or long noncoding RNAs, or establish that such studies have been almost exclusively conducted in animals. No page numbers are available in our copy. (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 [67]
The Introduction (page unavailable) discusses environmentally induced changes in sperm DNA methylation and stress-related changes in sperm miRNAs. It lists long noncoding RNAs among sperm RNAs, but does not say environmental exposure changed them; it also does not report environmentally driven histone modifications. The specified mechanisms are therefore not supported by this paper. (LLM, conf=0.83)
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- Authors
- Dickson, D. A., Paulus, J. K., Mensah, V., Lem, J., Saavedra-Rodriguez, L., Gentry, A., Pagidas, K., & Feig, L. A.
- Affiliations
- Tufts University (US)
- Brown University (US)
- Tufts Medical Center (US)
- University of Louisville (US)
- Corresponding author
- Feig, Larry A.
- Venue
- Translational Psychiatry
- Published
- 2018-05-23
- Volume
- 8
- Issue
- 1
- Pages
- 101-101
- ISSN
- 2158-3188 (ISSN-L)
- PMC
- PMC5966454
- OpenAlex
- W2803802792
- Cited by
- 208
- References
- 41
- Citations by year
- 2026: 11 · 2025: 20 · 2024: 16 · 2023: 61 · 2022: 16 · 2021: 25 · 2020: 27 · 2019: 28 · 2018: 4
- FWCI
- 22.53
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Translational Psychiatry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- National Institutes of Health
- Center for Neuroscience Research (P30 NS047243)
- National Institute of Mental Health (R01MH107536)
- National Institute of Neurological Disorders and Stroke (P30NS047243)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- sperm microRNA, miR-449, miR-34, early life stress, adverse childhood experiences, epigenetic regulation, sociability, anxiety, male fertility, embryonic development, stress biomarkers
- MeSH terms
- Adult Survivors of Child Adverse Events, Adult, Animals, Humans, Male, Spermatozoa, Stress, Psychological, MicroRNAs, White People, Mice
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