Role of Monocyte-Derived MicroRNA106b∼25 in Resilience to Social Stress
Open accessAbstract
Background Clinical studies suggest that heightened peripheral inflammation contributes to the pathogenesis of stress-related disorders, including major depressive disorder. However, the molecular mechanisms within peripheral immune cells that mediate enhanced stress vulnerability are not well known. Because microRNAs (miRs) are important regulators of immune response, we sought to examine their role in mediating inflammatory and behavioral responses to repeated social defeat stress (RSDS), a mouse model of stress vulnerability that produces susceptible and resilient phenotypes.Methods We isolated Ly6c high monocytes via fluorescence-activated cell sorting in the blood of susceptible and resilient mice following RSDS and profiled miR expression via quantitative real-time polymerase chain reaction. Bone marrow chimeric mice were generated to confirm a causal role of the miR-106b∼25 cluster in bone marrow-derived leukocytes in mediating stress resilience versus susceptibility.Results We found that RSDS produces an increase in circulating Ly6c high inflammatory monocytes in both susceptible and resilient mice. We next investigated whether intrinsic leukocyte posttranscriptional mechanisms contribute to individual differences in stress response and the resilient phenotype. Of the miRs profiled in our panel, eight were significantly regulated by RSDS within Ly6c high monocytes, including miR-25-3p, a member of the miR-106b∼25 cluster. Selective knockout of the miR-106b∼25 cluster in peripheral leukocytes promoted behavioral resilience to RSDS.Conclusions Our results identify the miR-106b∼25 cluster as a key regulator of stress-induced inflammation and depression that may represent a novel therapeutic target for drug development.
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Stress changes blood cell formation so that monocytes and neutrophils increase, lymphocytes decrease, and pro-inflammatory activity rises in peripheral immune tissues.
“Recent studies have reported stress-induced alterations in hematopoiesis that result in monocytosis, neutrophilia and lymphocytopenia and, consequently, upregulation of pro-inflammatory processes in immunologically-relevant peripheral tissues.”
From Central regulation of stress-evoked peripheral immune responses (2023) · cites this paper as [57]
The Results section (page unavailable) reports that repeated social defeat stress increased circulating inflammatory monocytes and neutrophils and decreased B cells in mice; T cells decreased only in susceptible mice. The Introduction (page unavailable) describes stress-induced myelopoiesis and elevated peripheral IL-6, but the paper does not establish that these blood-cell changes consequently upregulate pro-inflammatory processes in peripheral tissues. (LLM, conf=0.85)
Experimental — accuracy not yet measuredMDD in humans and chronic stress in rodents are linked to monocytosis, neutrophilia and lymphocytopenia, which may result from altered HSC subpopulation proliferation or leukocyte mobilization from bone marrow.
“MDD in humans and chronic stress in rodents are associated with monocytosis, neutrophilia and lymphocytopenia, which can be attributed to altered proliferation of hematopoietic stem cell (HSC) subpopulations or mobilization of leukocytes from the bone marrow33,56–58.”
From Central regulation of stress-evoked peripheral immune responses (2023) · cites this paper as [57]
The Introduction reports increased inflammatory monocytes and neutrophils in subsets of patients with MDD, and the Results report increased monocytes and neutrophils and decreased B cells after chronic social stress in mice; T-cell counts decreased only in susceptible mice. The paper does not establish lymphocytopenia in humans with MDD or attribute these changes to altered HSC-subpopulation proliferation or leukocyte mobilization from bone marrow. Page numbers are unavailable in our copy. (LLM, conf=0.88)
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The missing hallmark of health: psychosocial adaptation
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The Neurobiology of Resilience: Complexity and Hope
Murrough, J. W., & Russo, S. J. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.07.016 · Cited by 20 · see citing works
Self-citationHuang, Y. X., Huang, L., Li, L., Ge, Z., Feng, G., Liu, L., & Song, Y. (2020) · Annals of Translational Medicine · doi:10.21037/atm-20-6595 · Cited by 19 · see citing works
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SUMO E3 ligase PIAS1 is a potential biomarker indicating stress susceptibility
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MicroRNA–Messenger RNA Regulatory Network Mediates Disrupted TH17 Cell Differentiation in Depression
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Regulation of hippocampal miRNA expression by intestinal flora in anxiety-like mice
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Peripheral immune-derived matrix metalloproteinase promotes stress susceptibility
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“These findings, which emphasize the role of peripheral myeloid cells in stress-linked disorders such as MDD, are in line with several pre-clinical studies 13,34,12,35 and studies in humans 36,37,38 .”
ResultSelf-citationImmunity in Rodent Models of Stress
Hachenberg, S., Russo, S. J., & Cathomas, F. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.11.007 · Cited by 2 · see citing works
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Social stress induces autoimmune responses against the brain to promote stress susceptibilityPreprint
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Self-citationCirculating extracellular vesicle microRNAs mediate immune modulation of social behavior in micePreprint
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- Authors
- Pfau, M. L., Menard, C., Cathomas, F., Desland, F., Kana, V., Chan, K. L., Shimo, Y., LeClair, K., Flanigan, M. E., Aleyasin, H., Walker, D. M., Bouchard, S., Mack, M., Hodes, G. E., Merad, M. M., & Russo, S. J.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Tisch Cancer Institute (US)
- University Hospital Regensburg (DE)
- Virginia Tech (US)
- Corresponding author
- Russo, Scott J.
- ORCID
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2019-09
- Volume
- 86
- Issue
- 6
- Pages
- 474-482
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC6717005
- OpenAlex
- W2926139416
- Cited by
- 46
- References
- 60
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 11 · 2023: 6 · 2022: 11 · 2021: 3 · 2020: 6 · 2019: 5
- FWCI
- 4.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- University of Regensburg Publication Server (University of Regensburg) (submittedVersion)
- Funders
- National Institutes of Health
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Keywords
- miR-25-3p, social defeat stress, stress resilience, major depressive disorder, Ly6Chi monocytes, peripheral inflammation, bone marrow chimeric mice, individual differences in stress response, post-transcriptional regulation
- MeSH terms
- Animals, Behavior, Animal, Depression, Male, Mice, Inbred C57BL, Monocytes, Stress, Psychological, Bone Marrow Transplantation, Transplantation Chimera, Mice, Knockout, MicroRNAs, Mice, Resilience, Psychological
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