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Peripheral and central effects of repeated social defeat stress: Monocyte trafficking, microglial activation, and anxiety
Open accessAbstract
The development and exacerbation of depression and anxiety are associated with exposure to repeated psychosocial stress. Stress is known to affect the bidirectional communication between the nervous and immune systems leading to elevated levels of stress mediators including glucocorticoids (GCs) and catecholamines and increased trafficking of proinflammatory immune cells. Animal models, like the repeated social defeat (RSD) paradigm, were developed to explore this connection between stress and affective disorders. RSD induces activation of the sympathetic nervous system (SNS) and hypothalamic-pituitary-adrenal (HPA) axis activation, increases bone marrow production and egress of primed, GC-insensitive monocytes, and stimulates the trafficking of these cells to tissues including the spleen, lung, and brain. Recently, the observation that these monocytes have the ability to traffic to the brain perivascular spaces and parenchyma have provided mechanisms by which these peripheral cells may contribute to the prolonged anxiety-like behavior associated with RSD. The data that have been amassed from the RSD paradigm and others recapitulate many of the behavioral and immunological phenotypes associated with human anxiety disorders and may serve to elucidate potential avenues of treatment for these disorders. Here, we will discuss novel and key data that will present an overview of the neuroendocrine, immunological and behavioral responses to social stressors.
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“Furthermore, chronic psychosocial stress promotes an increase in glucocorticoid (GC)-insensitive monocyte populations. Recent studies have also observed that these monocytes possess the ability to transmigrate across the blood–brain barrier, potentially contributing to the development of long-term anxiety-related behaviors [23].”
From Comparative Analysis of HPA-Axis Dysregulation and Dynamic Molecular Mechanisms in Acute Versus Chronic Social Defeat Stress (2025) · cites this paper as [23]
In the citing paper
“In addition, the physiological consequences of exposure to RSD are robustly associated with structural changes (e.g., atrophy, connectivity) to neural systems that modulate threat-sensitivity and anxiety-like behaviors (Reader et al., 2015).”
From Developmental psychoneuroendocrine and psychoneuroimmune pathways from childhood adversity to disease (2017) · cites this paper as Reader et al., 2015
In the citing paper
“Repeated social defeat (RSD) is an ethologically relevant social stressor that recapitulates many of the stress-induced immune and behavioral outcomes of stress (Reader et al, 2015).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Reader et al, 2015
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BackgroundInfluentialFate Mapping Reveals Origins and Dynamics of Monocytes and Tissue Macrophages under Homeostasis
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Swirski, F. K., Nahrendorf, M., Etzrodt, M., Wildgruber, M., Cortez-Retamozo, V., Panizzi, P., Figueiredo, J.-L., Kohler, R. H., Chudnovskiy, A., Waterman, P., et al. (2009) · Science · doi:10.1126/science.1175202 · Cited by 2,221 · cited 1×
“The idea that the spleen serves as an alternative source of monocyte trafficking is seen in several studies involving inflammatory challenges including myocardial infarction (Swirski et al., 2009) and stroke (Seifert et al., 2012).”
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“This model is known as repeated social defeat stress (RSDS), and incorporates aspects of both physical and psychological trauma (Reader et al., 2015; Moshfegh et al., 2019; Weber et al., 2017).”
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“Repeated social defeat (RSD) is a rodent model of psychosocial stress that recapitulates many of the human immune and behavioral responses to stress (Wohleb et al., 2014, Reader et al., 2015, Weber et al., 2017).”
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Schnieder, T. P., Qin, I. D. Z., Trencevsja-Ivanovska, I., Rosoklija, G. B., Stankov, A., Pavlovski, G., Mann, J. J., & Dwork, A. J. (2018) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nly103 · Cited by 15
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“These primed cells have elevated levels of TLR receptors and have been shown to promote anxiety-like behavior (55,56).”
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“Recent studies have also observed that these monocytes possess the ability to transmigrate across the blood–brain barrier, potentially contributing to the development of long-term anxiety-related behaviors [23].”
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“As peripheral macrophages which are recruited to the brain upon stress stimulation can also drive behavioral deficits by producing high levels of pro-inflammatory cytokines [50, 51], we should also clarify the roles of these cells in the preventive effect of MPL on CSDSinduced anxiety-like behaviors.”
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“These stress paradigms were shown to induce activation of the HPA axis and to stimulate the trafficking of CG-insensitive monocytes to tissues including the spleen, lung, and brain (Reader et al., 2015).”
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“Studies indicate that anxiety-like behaviour persists even when the stressor is no longer present (Patki et al. 2013, Wohleb et al. 2013, Reader et al. 2015).”
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“…RSDS increased bone marrow-derived monocyte recruitment to specific brain regions associated with anxiety-related symptoms Moreover, RSDS traffics peripheral monocytes to the brain that contrib - ute to the prolonged anxiety-like behavior in response to social defeat stress (Reader et al. 2015).”
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“…reported stress-induced morphological, transcriptional and functional changes indicative of an inflammatory signature in microglia from other brain regions 47,48,49,50 , this is the first study investigating cell type-specific gene expression signatures at the single-cell level in NAc microglia.”
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“RSD also increases outflow of stress signalling from the brain (both sympathetic nervous system and hypo-thalamic pituitary axis (Reader et al., 2015) to the peripheral immune system which increases myelopoiesis and shifts the phenotype of peripheral monocytes to be proinflammatory and…”
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“Interestingly, in a murine model of repeated social defeat, myeloid cell recruitment into the central nervous system required both CCR2 and CX3CR1 [49].”
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Repeated social defeat causes bone loss from mouse femur
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Self-citation
Metadata
- Authors
- Reader, B. F., Jarrett, B. L., McKim, D. B., Wohleb, E. S., Godbout, J. P., & Sheridan, J. F.
- Affiliations
- The Ohio State University Wexner Medical Center (US)
- Yale University (US)
- Corresponding author
- Sheridan, J.F.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2015-03
- Volume
- 289
- Pages
- 429-442
- ISSN
- 0306-4522 (ISSN-L)
- PMC
- PMC4536813
- OpenAlex
- W2024776501
- Cited by
- 179
- References
- 110
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 13 · 2023: 12 · 2022: 18 · 2021: 20 · 2020: 9 · 2019: 19 · 2018: 20 · 2017: 20 · 2016: 20 · 2015: 12
- FWCI
- 1.92
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01-MH-093473, R01-MH093472)
- NIH/NIDCR (T32-DE014320)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- repeated social defeat stress, anxiety-like behavior, monocyte trafficking, microglial activation, neuroimmune interactions, hypothalamic-pituitary-adrenal axis, sympathetic nervous system, depression, psychosocial stress
- MeSH terms
- Animals, Anxiety, Dominance-Subordination, Humans, Monocytes, Stress, Psychological, Microglia
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