Peripheral innate immune challenge exaggerated microglia activation, increased the number of inflammatory CNS macrophages, and prolonged social withdrawal in socially defeated mice
Open accessAbstract
Repeated social defeat (RSD) activates neuroendocrine pathways that have a significant influence on immunity and behavior. Previous studies from our lab indicate that RSD enhances the inflammatory capacity of CD11b⁺ cells in the brain and promotes anxiety-like behavior in an interleukin (IL)-1 and β-adrenergic receptor-dependent manner. The purpose of this study was to determine the degree to which mice subjected to RSD were more responsive to a secondary immune challenge. Therefore, RSD or control (HCC) mice were injected with saline or lipopolysaccharide (LPS) and activation of brain CD11b⁺ cells and behavioral responses were determined. Peripheral LPS (0.5 mg/kg) injection caused an extended sickness response with exaggerated weight loss and prolonged social withdrawal in socially defeated mice. LPS injection also amplified mRNA expression of IL-1β, tumor necrosis factor (TNF)-α, inducible nitric oxide synthase (iNOS), and CD14 in enriched CD11b⁺ cells isolated from socially defeated mice. In addition, IL-1β mRNA levels in enriched CD11b⁺ cells remained elevated in socially defeated mice 24 h and 72 h after LPS. Moreover, microglia and CNS macrophages isolated from socially defeated mice had the highest CD14 expression after LPS injection. Both social defeat and LPS injection increased the percentage of CD11b⁺/CD45(high) macrophages in the brain and the number of inflammatory macrophages (CD11b⁺/CD45(high)/CCR2⁺) was highest in RSD-LPS mice. Anxiety-like behavior was increased by social defeat, but was not exacerbated by the LPS challenge. Nonetheless, reduced locomotor activity and increased social withdrawal were still present in socially defeated mice 72 h after LPS. Last, LPS-induced microglia activation was most evident in the hippocampus of socially defeated mice. Taken together, these findings demonstrate that repeated social defeat enhanced the neuroinflammatory response and caused prolonged sickness following innate immune challenge.
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Functionally, microglia are primed to later activation, as they produce an exaggerated proinflammatory response to subsequent immunological challenges.
“Functionally, microglia are 'primed' to later activation, as they produce an exaggerated proinflammatory response to subsequent immunological challenges (Wohleb et al, 2012).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2012
RSD also increases depressive-like behaviors, including social avoidance, and these effects can persist at least 8 days after stressor termination with some persisting up to 24 days.
“RSD also increases depressive-like behaviors, including social avoidance (Wohleb et al, 2012;Ramirez et al, 2015b).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2012
Neuroinflammatory signaling is increased by RSD and is argued to facilitate vulnerability toward mood disorders.
“In addition to activating neuronal fear/anxiety circuitry, neuroinflammatory signaling is increased by RSD (Kinsey et al, 2007;Wohleb et al, 2012) that is argued to facilitate vulnerability toward mood disorders (Haroon et al, 2012).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2012
The increase of CD11b+/CD45 high persisted despite vascular perfusion, indicating that the monocyte/macrophages adhered to the vasculature or entered the parenchyma.
“It is important to note that the increase of CD11b + /CD45 high persisted despite vascular perfusion, and hence the CD11b + /CD45 high monocyte/macrophages adhered to the vasculature or entered the parenchyma (Wohleb et al, 2012).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2012
Stress exposure activates microglia and increases proinflammatory cytokine (IL-1β, TNF-α, IL-6) and chemokine (CCL2) signaling, thereby providing a direct pathway to upregulate adhesion molecules.
“As discussed above, stress exposure activates microglia and increases proinflammatory cytokine (IL-1β, TNF-α, IL-6) and chemokine (CCL2) signaling (Wohleb et al, 2012), thereby providing a direct pathway to upregulate adhesion molecules.”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Wohleb et al, 2012
HMGB1 signals through Toll-like receptors to translocate NF-κB to the nucleus that drives transcription of pro-IL-1β and NLRP3.
“HMGB1 signals through Toll-like receptors to translocate NF-κB to the nucleus that drives transcription of pro-IL-1β and NLRP3.”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as [138]
HMGB-1 primes the NLRP3 inflammasome in the CNS after stress exposure.
“First evidence that HMGB-1 primes the NLRP3 inflammasome in the CNS after stress exposure.”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as [138]
Intraperitoneal LPS induced a markedly higher production of microglial IL-1β, TNFα, iNOS, and CD14 in stress-exposed mice compared with naive mice.
“For example, intraperitoneal LPS induced a markedly higher production of microglial IL-1β, TNFα, iNOS, and CD14 in stress-exposed mice compared with naive mice (Wohleb et al, 2012).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Wohleb et al, 2012
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- Authors
- Wohleb, E. S., Fenn, A. M., Pacenta, A. M., Powell, N. D., Sheridan, J. F., & Godbout, J. P.
- Affiliations
- The Ohio State University (US)
- Corresponding author
- Godbout, Jonathan P.
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2012-09
- Volume
- 37
- Issue
- 9
- Pages
- 1491-1505
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC3368999
- OpenAlex
- W2068671283
- Cited by
- 275
- References
- 69
- Citations by year
- 2026: 7 · 2025: 15 · 2024: 10 · 2023: 15 · 2022: 24 · 2021: 23 · 2020: 33 · 2019: 28 · 2018: 20 · 2017: 19 · 2016: 24 · 2015: 21 · 2014: 17 · 2013: 15 · 2012: 4
- FWCI
- 9.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Dental and Craniofacial Research (T32DE014320)
- National Institute on Aging (R01AG033028)
- Howard Hughes Medical Institute
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- repeated social defeat, microglial activation, neuroinflammation, lipopolysaccharide challenge, sickness behavior, social withdrawal, CD11b+ macrophages, CCR2, IL-1β, CD14, TNF-α, inducible nitric oxide synthase, anxiety-like behavior, hippocampus, innate immunity, neuroendocrine-immune interaction
- MeSH terms
- Animals, Behavior, Animal, Brain, Cell Count, Dominance-Subordination, Immunity, Innate, Inflammation, Lipopolysaccharides, Macrophages, Male, Social Isolation, Tumor Necrosis Factor-alpha, Microglia, Mice, Nitric Oxide Synthase Type II, Interleukin-1beta
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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