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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
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“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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InfluentialNeuroinflammatory Dynamics Underlie Memory Impairments after Repeated Social Defeat
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“Overall, these data indicate that kefir may modulate peripheral immunoregulation, which might have relevance to neuroimmune activation (Reader et al., 2015; Kim et al., 2018).”
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“Consecutively, activated microglia release proinflammatory cytokines and neurotoxic factors that negatively affect CNS cell functions and thus trigger anxietyand depression-like behaviors in mice (Reader et al., 2015; Lehmann et al., 2016; Ramirez et al., 2017; Stein et al., 2017).”
BackgroundContributions of monocytes to nervous system disorders
Garré, J. M., & Yang, G. (2018) · Journal of Molecular Medicine · doi:10.1007/s00109-018-1672-3 · Cited by 53
“amines control the trafficking and activation of monocytes [36].”
Bordoni, B., Marelli, F., Morabito, B., & Sacconi, B. (2017) · Monaldi Archives for Chest Disease · doi:10.4081/monaldi.2017.811 · Cited by 50
Oladapo, O. M., Ben‐Azu, B., Ajayi, A. M., Emokpae, O., Eneni, A.-E. O., Omogbiya, I. A., & Iwalewa, E. O. (2020) · Journal of Molecular Neuroscience · doi:10.1007/s12031-020-01664-y · Cited by 51
“Noteworthily, expanded preclinical evidences have shown a strong association between chronic psychosocial stress, dark microglia, and copious release of pro-inflammatory cytokines to reduced hippocampal neurogenesis, a highly plastic brain region that is strongly involved in memory impairment, anxiety, and depression…”
BackgroundResultInfluentialBrain–immune interaction mechanisms: Implications for cognitive dysfunction in psychiatric disorders
Zhao, F., Li, B., Yang, W., Ge, T., & Cui, R. (2022) · Cell Proliferation · doi:10.1111/cpr.13295 · Cited by 50
Tian, L., Hui, C. W., Bisht, K., Tan, Y., Sharma, K. P., Chen, S., Zhang, X., & Tremblay, M. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.01.007 · Cited by 52
Unique maternal immune and functional microbial profiles during prenatal stress
Antonson, A. M., Evans, M. V., Galley, J. D., Chen, H. J., Rajasekera, T. A., Lammers, S. M., Hale, V. L., Bailey, M. T., & Gur, T. (2020) · Scientific Reports · doi:10.1038/s41598-020-77265-x · Cited by 51
Chen, T., Chen, C., Zhang, Z., Zou, Y., Peng, M., & Wang, Y. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.04.004 · Cited by 46
“Cytokines have also been associated with a variety of behavior impairments linked to emotional and anxiety-related behaviors (Reader et al., 2015).”
BackgroundLee, W., Milewski, T. M., Dwortz, M. F., Young, R. L., Gaudet, A. D., Fonken, L. K., Champagne, F. A., & Curley, J. P. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.04.015 · Cited by 44
Neuroinflammaging: A Tight Line Between Normal Aging and Age-Related Neurodegenerative Disorders
Soraci, L., Corsonello, A., Paparazzo, E., Montesanto, A., Piacenza, F., Olivieri, F., Gambuzza, M. E., Savedra, E. V., Marino, S., Lattanzio, F., et al. (2024) · Aging and Disease · doi:10.14336/ad.2023.1001 · Cited by 49
Rodríguez‐Arias, M., Montagud‐Romero, S., Carrión, A. M. G., Perez, C. F., Pérez‐Villalba, A., Marco, E. M., López‐Gallardo, M., Viveros, M., & Miñarro, J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0206421 · Cited by 42
Galley, J. D., Mackos, A. R., Varaljay, V. A., & Bailey, M. T. (2017) · Scientific Reports · doi:10.1038/srep45012 · Cited by 37
Untangling PTSD and TBI: Challenges and Strategies in Clinical Care and Research
Hendrickson, R. C., Schindler, A. G., & Pagulayan, K. F. (2018) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-018-0908-5 · Cited by 39
Hasegawa, Y., Ma, M., Sawa, A., Lane, A. P., & Kamiya, A. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02081-y · Cited by 40
Cosma, N. C., Üsekes, B., Otto, L. R., Gerike, S., Heuser, I., Regen, F., & Hellmann‐Regen, J. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.02.009 · Cited by 37
A multispecies approach for understanding neuroimmune mechanisms of stress
Deak, T., Kudinova, A. Y., Lovelock, D. F., Gibb, B. E., & Hennessy, M. B. (2017) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2017.19.1/tdeak · Cited by 33
Liu, Y., Xie, X., Xia, L., Lv, H., Lou, F., Ren, Y., He, Z., & Luo, X.-G. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0994-3 · Cited by 33
“We speculated that the neuroinflammatory alleviation was induced by peripheral immune tolerance preconditioning through the following ways: (a) Monocytes and microglia are considered to share the same origin of the myeloid lineage [37]; thus, immune tolerance pre-treatment induced hypo-responsiveness of monocytes may…”
BackgroundCCR2 monocytes repair cerebrovascular damage caused by chronic social defeat stress
Lehmann, M. L., Samuels, J. D., Kigar, S. L., Poffenberger, C. N., Lotstein, M. L., & Herkenham, M. A. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.01.011 · Cited by 31
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“Brain inflammation, driven by nonneuronal cells such as astrocytes and microglia, has been demonstrated to be associated with several neurological diseases including depression and anxiety [5], with neuropsychiatric pathologies such as mood disorders and psychosis [6], and with neurodegenerative diseases such as Parki…”
BackgroundIngestion of Lactobacillus rhamnosus modulates chronic stress-induced feather pecking in chickens
Mindus, C., van Staaveren, N., Bharwani, A., Fuchs, D., Gostner, J. M., Kjær, J. B., Kunze, W., Mian, M. F., Shoveller, A. K. K., Forsythe, P., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-96615-x · Cited by 34
Reid, B. M., & Georgieff, M. (2023) · Nutrients · doi:10.3390/nu15173798 · Cited by 38
Neuroimmune Mechanisms and Sex/Gender-Dependent Effects in the Pathophysiology of Mental Disorders
Kokkosis, A. G., & Tsirka, S. E. (2020) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.120.266163 · Cited by 29
A cord blood monocyte–derived cell therapy product accelerates brain remyelination
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“cytes do not enter the uninjured, adult mouse brain but may infiltrate the CNS following insult such as brain irradiation (5, 6), chemotherapy or injury (7), demyelinating conditions (8), or chronic stress (9, 10).”
BackgroundInfluentialInsights into psychosis risk from leukocyte microRNA expression
Jeffries, C. D., Perkins, D. O., Chandler, S. D., Stark, T., Yeo, E., Addington, J., Bearden, C. E., Cadenhead, K. S., Cannon, T. D., Cornblatt, B. A., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.148 · Cited by 29
Oxidation and Inflammation in the Immune and Nervous Systems, a Link Between Aging and Anxiety
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Brzozowska, N., Smith, K. L., Zhou, C., Waters, P. M., Cavalcante, L. M., Abelev, S. V., Kuligowski, M., Clarke, D. J., Todd, S. M., & Arnold, J. C. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.05.008 · Cited by 28
“Another is that P-gp may moderate stress-induced activation of microglia (Calcia et al., 2016; Kao et al., 2016; Reader et al., 2015; Tynan et al., 2010).”
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Neuroimmune mechanisms in fear and panic pathophysiology
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“Exposure to RSD leads to increased sympathetic activation promoting elevated noradrenergic signaling in the periphery and increased production and release of glucocorticoid-insensitive monocytes into the circulation from the bone marrow and spleen [reviewed in (114, 183)].”
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“2,34,35 For analyzing social stress in mice, the chronic social defeat paradigm is a widely used model.”
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T cell-mediated skin-brain axis: Bridging the gap between psoriasis and psychiatric comorbidities
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“duced depression have shown to induce both depressive behaviour and microglia activation [73].”
BackgroundMechanistic Understanding of Socioeconomic Disparities in Cardiovascular Disease
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“Monocyte trafficking to the brain is required for increased anxiety-like behaviors after exposure to chronic social defeat stress (Reader et al., 2015; Wohleb, McKim, Shea, et al., 2014; Wohleb, McKim, Sheridan, et al., 2014), and numerous studies have shown increased Iba1 expressing cells (likely…”
BackgroundLu, Y., Sun, M., Li, Y., Wu, L., Zhang, X., Wang, J., Huang, Y., & Cao, F. (2022) · Journal of Clinical Psychology in Medical Settings · doi:10.1007/s10880-022-09915-3 · Cited by 23
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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