β-Adrenergic Receptor Antagonism Prevents Anxiety-Like Behavior and Microglial Reactivity Induced by Repeated Social Defeat
Open accessAbstract
Psychosocial stress is associated with altered immune function and development of psychological disorders including anxiety and depression. Here we show that repeated social defeat in mice increased c-Fos staining in brain regions associated with fear and threat appraisal and promoted anxiety-like behavior in a β-adrenergic receptor-dependent manner. Repeated social defeat also significantly increased the number of CD11b + /CD45 high /Ly6C high macrophages that trafficked to the brain. In addition, several inflammatory markers were increased on the surface of microglia (CD14, CD86, and TLR4) and macrophages (CD14 and CD86) after social defeat. Repeated social defeat also increased the presence of deramified microglia in the medial amygdala, prefrontal cortex, and hippocampus. Moreover, mRNA analysis of microglia indicated that repeated social defeat increased levels of interleukin (IL)-1β and reduced levels of glucocorticoid responsive genes [glucocorticoid-induced leucine zipper (GILZ) and FK506 binding protein-51 (FKBP51)]. The stress-dependent changes in microglia and macrophages were prevented by propranolol, a β-adrenergic receptor antagonist. Microglia isolated from socially defeated mice and cultured ex vivo produced markedly higher levels of IL-6, tumor necrosis factor-α, and monocyte chemoattractant protein-1 after stimulation with lipopolysaccharide compared with microglia from control mice. Last, repeated social defeat increased c-Fos activation in IL-1 receptor type-1-deficient mice, but did not promote anxiety-like behavior or microglia activation in the absence of functional IL-1 receptor type-1. These findings indicate that repeated social defeat-induced anxiety-like behavior and enhanced reactivity of microglia was dependent on activation of β-adrenergic and IL-1 receptors.
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Initial microglial activation during social defeat stress appeared to be a result of neuronal activation by catecholamines and decreased neuronal production of CX3CL1.
“initial microglial activation during social defeat stress appeared to be a result of neuronal activation by catecholamines and decreased neuronal production of CX3C-chemokine ligand 1 (CX3CL1; also known as fractalkine), which maintains microglia in a quiescent state67,68.”
From The role of inflammation in depression: from evolutionary imperative to modern treatment target (2016) · cites this paper as [67]
The Introduction and Results (page unavailable) report that social defeat increased brain c-Fos activation and microglial inflammatory activity, and that β-adrenergic receptor antagonism blocked these changes. They do not establish that catecholamine-driven neuronal activation caused the microglial response. A search for CX3CL1 and fractalkine found no passage reporting decreased neuronal production of either. (LLM, conf=0.85)
Experimental — accuracy not yet measuredIn social defeat stress, GFP-labelled monocytes coalesced in several brain regions associated with detection of threat, such as the amygdala, an effect dependent on CCL2 and facilitated by mobilization of monocytes from bone marrow due to stress-induced release of catecholamines.
“in the context of social defeat stress, whereby GFP-labelled monocytes coalesced in several regions of the brain associated with the detection of threat (for example, amygdala) — an effect that was dependent on CCL2 and was facilitated by mobilization of monocytes from the bone marrow as a result of stress-induced release of catecholamines67,68”
From The role of inflammation in depression: from evolutionary imperative to modern treatment target (2016) · cites this paper as [67]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredSocial defeat stress impacts immune regulation in the amygdala and changes in social behavior.
“Previously, social defeat stress has been shown to impact immune regulation in the amygdala and changes in social behavior [62–64].”
From Rapid changes in plasma corticosterone and medial amygdala transcriptome profiles during social status change reveal molecular pathways associated with a major life history transition in mouse dominance hierarchies (2025) · cites this paper as [64]
The Abstract reports increased de-ramified microglia in the medial amygdala after repeated social defeat, supporting the immune-regulation portion. The Methods and Results report anxiety-like behavior measured with a light/dark preference test, not a change in social behavior specifically. (LLM, conf=0.85)
Experimental — accuracy not yet measuredDrugs that limit HPA axis and downstream SNS signaling, such as β-adrenergic receptor antagonists, COX2 inhibitors, anti-VEGFC therapeutics, or dopamine, have been shown in animal experiments to improve anxiety-like behavior, inhibit chronic tumor-promoting tumor growth, and block stress-induced increase in angiogenesis and lymphatic metastasis.
“These drugs have been shown in animal experiments to not only significantly improve anxiety-like behavior (47, 48), and inhibit chronic tumor-promoting tumor growth, but also to block a stress-induced increase in angiogenesis and lymphatic metastasis (60).”
From Chronic Stress Promotes Cancer Development (2020) · cites this paper as [47]
Microglia from socially defeated mice have an increased inflammatory profile and produce more IL-6 after lipopolysaccharide stimulation.
“Microglia from socially defeated mice have an increased inflammatory profile and produce more IL-6 after lipopolysaccharide (LPS) stimulation [191], similar to enhanced IL-6 release from the peripheral leukocytes of stressed mice [175].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [191]
Noradrenaline and glucocorticoids mediate the effects of stress on neuroinflammatory processes.
“A number of mediators of the stress response, most notably noradrenaline and glucocorticoids, have been found to mediate the effects of stress on neuroinflammatory processes (Frank et al, 2013;Wohleb et al, 2011).”
From Danger Signals and Inflammasomes: Stress-Evoked Sterile Inflammation in Mood Disorders (2017) · cites this paper as Wohleb et al, 2011
Interventions with noradrenergic receptor antagonists or GABAergic agonists prevent RSD-induced IL-6 increase, monocyte recruitment to the brain, and anxiety-like behavior.
“Interventions with noradrenergic receptor antagonist or GABAergic agonists prevented RSD-induced IL-6 increase, monocyte recruitment to the brain, and anxiety-like behavior following RSD [24, 25].”
From Interleukin-6 Induced by Social Stress Promotes a Unique Transcriptional Signature in the Monocytes That Facilitate Anxiety (2019) · cites this paper as [25]
Pharmacological blockage of the β-adrenergic receptor before RSD prevented BM-derived myeloid cell differentiation and redistribution in circulation.
“Furthermore, pharmacological blockage of the β-adrenergic receptor before RSD prevented BM-derived myeloid cell differentiation and redistribution in circulation (Wohleb et al, 2011;Hanke et al, 2012;Powell et al, 2013).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2011
The myelopoietic response of RSD is mediated by NE.
“Further investigation revealed that the myelopoietic response of RSD is mediated by NE (Wohleb et al, 2011;Hanke et al, 2012;Heidt et al, 2014).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2011
RSD increases anxiety-like behaviors on standard measures including reduced exploration on open field and elevated plus maze, and increases dark preference in the light/dark test.
“For example, RSD increases anxiety-like behaviors on standard measures including reduced exploration on open field and elevated plus maze, and increases dark preference in the light/dark test (Wohleb et al, 2011(Wohleb et al, , 2013(Wohleb et al, , 2014b;;Hanke et al, 2012).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2011
Increased c-fos expression occurred after a single cycle of social defeat that precedes any neuroinflammatory or anxiety-like behavior associated with 6 days of RSD.
“Importantly, increased c-fos expression occurred after a single cycle of social defeat that precedes any neuroinflammatory or anxiety-like behavior that is associated with 6 days of RSD.”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2011
Blocking monocyte trafficking to the brain attenuates stress-induced proinflammatory cytokine response and related changes to behavior.
“blocking monocyte trafficking to the brain attenuates stress-induced proinflammatory cytokine response, and related changes to behavior”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2011
GFP+ monocytes accumulated in the same threat appraisal areas that had increased c-Fos and IBA-1 activation after RSD, but not in other brain regions like the motor cortex or cerebellum, suggesting site-specific recruitment to stress-responsive brain regions.
“Notably, GFP+ monocytes accumulated in the same threat appraisal areas that had increased c-Fos and IBA-1 activation after RSD, but not in other brain regions like the motor cortex or cerebellum, suggesting site-specific recruitment to stress-responsive brain regions (Wohleb et al, 2011(Wohleb et al, , 2013)).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2011
RSD increased the presence of CD11b+/CD45 high monocyte population in the CNS, and these cells highly expressed Ly6C.
“Here, RSD increased the presence of CD11b + /CD45 high monocyte population in CNS (Wohleb et al, 2011).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2011
IL-1β is critical for the neuroinflammatory and behavioral response to RSD.
“As mentioned above, IL-1β is critical for the neuroinflammatory and behavioral response to RSD (Wohleb et al, 2011(Wohleb et al, , 2014b)).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2011
These morphological alterations were associated with the classical activation profile, characterized by the increased expression of antigen presentation molecule (MHCII), cell surface markers (TLR4 and CD14), and pro-inflammatory cytokines and chemokines (IL-1β, TNFα, IL-6, and CCL2).
“These morphological alterations were associated with the classical activation profile, characterized by the increased expression of antigen presentation molecule (MHCII), cell surface markers (TLR4 and CD14), and pro-inflammatory cytokines and chemokines (IL-1β, TNFα, IL-6, and CCL2) (Frank et al, 2007;Ramirez et al, 2016;Wohleb et al, 2011).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Wohleb et al, 2011
Microglia in the stressed brain undergo profound morphological changes, marked by large amoeboid cell bodies and thicker processes.
“For example, microglia in the stressed brain undergo profound morphological changes, marked by large amoeboid cell bodies and thicker processes (Frank et al, 2007;Wohleb et al, 2011).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Wohleb et al, 2011
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- Authors
- Wohleb, E. S., Hanke, M. L., Corona, A. W., Powell, N. D., Stiner, L. M., Bailey, M. T., Nelson, R. J., Godbout, J. P., & Sheridan, J. F.
- Affiliations
- The Ohio State University (US)
- Institute for Behavioral Medicine (US)
- Corresponding author
- Sheridan, John F.
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-04-27
- Volume
- 31
- Issue
- 17
- Pages
- 6277-6288
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3160240
- OpenAlex
- W2047570180
- Cited by
- 638
- References
- 59
- Citations by year
- 2026: 27 · 2025: 27 · 2024: 33 · 2023: 45 · 2022: 44 · 2021: 51 · 2020: 47 · 2019: 60 · 2018: 49 · 2017: 50 · 2016: 42 · 2015: 48 · 2014: 33 · 2013: 36 · 2012: 38
- FWCI
- 20.12
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (R01AG033028)
- National Institute of Mental Health (R01MH046801, R01MH093473)
- National Institute of Dental and Craniofacial Research (T32DE014320)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- beta-adrenergic receptor antagonism, propranolol, repeated social defeat, anxiety-like behavior, microglial activation, brain macrophages, psychosocial stress, c-fos, IL1R1, IL-1β, GILZ, FKBP51, neuroinflammation, microglial inflammation
- MeSH terms
- Tacrolimus Binding Protein 5, Adrenergic beta-Antagonists, Analysis of Variance, Animals, Anxiety Disorders, Behavior, Animal, Cells, Cultured, Dose-Response Relationship, Drug, Flow Cytometry, Gene Expression Regulation, Inflammation, Lipopolysaccharides, Male, Mice, Inbred C57BL, Propranolol, RNA, Messenger, Social Behavior, Stress, Psychological, Transcription Factors, Antigens, CD, Cytokines, Proto-Oncogene Proteins c-fos, Prefrontal Cortex, Receptors, Interleukin-1, Microglia, Mice, Knockout, Tacrolimus Binding Proteins, Toll-Like Receptor 4, Mice
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