Stress increases vulnerability to inflammation in the rat prefrontal cortex
Open accessAbstract
Inflammation could be involved in some neurodegenerative disorders that accompany signs of inflammation. However, because sensitivity to inflammation is not equal in all brain structures, a direct relationship is not clear. Our aim was to test whether some physiological circumstances, such as stress, could enhance susceptibility to inflammation in the prefrontal cortex (PFC), which shows a relative resistance to inflammation. PFC is important in many brain functions and is a target for some neurodegenerative diseases. We induced an inflammatory process by a single intracortical injection of 2 microg of lipopolysaccharide (LPS), a potent proinflammogen, in nonstressed and stressed rats. We evaluated the effect of our treatment on inflammatory markers, neuronal populations, BDNF expression, and behavior of several mitogen-activated protein (MAP) kinases and the transcription factor cAMP response element-binding protein. Stress strengthens the changes induced by LPS injection: microglial activation and proliferation with an increase in the levels of the proinflammatory cytokine tumor necrosis factor-alpha; loss of cells such as astroglia, seen as loss of glial fibrillary acidic protein immunoreactivity, and neurons, studied by neuronal-specific nuclear protein immunohistochemistry and GAD67 and NMDA receptor 1A mRNAs expression by in situ hybridization. A significant increase in the BDNF mRNA expression and modifications in the levels of MAP kinase phosphorylation were also found. In addition, we observed a protective effect from RU486 [mifepristone (11beta-[p-(dimethylamino)phenyl]-17beta-hydroxy-17-(1-propynyl)estra-4,9-dien-3-one)], a potent inhibitor of the glucocorticoid receptor activation. All of these data show a synergistic effect between inflammation and stress, which could explain the relationship described between stress and some neurodegenerative pathologies.
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Chronic stress increases both neuronal death and astrocytic death in a GR-dependent manner after direct LPS injection into the cortex.
“Finally, chronic stress increases both neuronal death and astrocytic death in a GR-dependent manner after direct LPS injection into the cortex (de Pablos et al., 2006).”
From The Stressed CNS: When Glucocorticoids Aggravate Inflammation (2009) · cites this paper as de Pablos et al., 2006
In the frontal cortex, GR signaling is essential for chronic stress to increase LPS-induced activation of several components of the MAPK signaling pathway involved in activating NF-κB.
“Supporting these results, in the frontal cortex, GR signaling is essential for chronic stress to increase LPS-induced activation of several components of the MAPK signaling pathway involved in activating NF-κB (de Pablos et al., 2006).”
From The Stressed CNS: When Glucocorticoids Aggravate Inflammation (2009) · cites this paper as de Pablos et al., 2006
In one study, chronic stress occurred after injury but still increased LPS-induced TNF-α expression and microglia activation.
“Importantly, in this study, chronic stress occurred after the injury, but still increased LPS-induced TNF-α expression and microglia activation.”
From The Stressed CNS: When Glucocorticoids Aggravate Inflammation (2009) · cites this paper as de Pablos et al., 2006
Chronically stressed animals injected in the prefrontal cortex or hippocampus with endotoxin displayed exacerbated microglia activation and tissue damage.
“Chronically stressed animals injected either in the prefrontal cortex (144) or the hippocampus (145) with this endotoxin also displayed exacerbated microglia activation and tissue damage.”
From The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [144]
The priming effects of stress on the ensuing immune response could be abated with RU486 or by experimentally maintaining plasma GCs to basal levels in adrenalectomized animals.
“Interestingly, in these studies the priming effects of stress (regardless of its chronicity) on the ensuing immune response could be abated with RU486 or by experimentally maintaining plasma GCs to basal levels in adrenalectomized animals.”
From The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [144]
GR signaling is essential for the cross-sensitization between stress and the inflammatory response to LPS.
“GR signaling was thus proposed to be essential for the cross-sensitization between stress and the inflammatory response to LPS.”
From The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [144]
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- Authors
- de Pablos, R. M., Villarán, R. F., Argüelles, S., Herrera, A. J., Venero, J. L., Ayala, A., Cano, J., & Machado, A.
- Affiliations
- Universidad de Sevilla (ES)
- Corresponding author
- Machado, A.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-05-24
- Volume
- 26
- Issue
- 21
- Pages
- 5709-5719
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6675274
- OpenAlex
- W2158199077
- Cited by
- 215
- References
- 103
- Citations by year
- 2026: 3 · 2025: 12 · 2024: 7 · 2023: 10 · 2022: 11 · 2021: 11 · 2020: 7 · 2019: 10 · 2018: 8 · 2017: 14 · 2016: 17 · 2015: 14 · 2014: 17 · 2013: 17 · 2012: 12
- FWCI
- 5.48
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- idUS (Universidad de Sevilla) (publishedVersion, cc-by-nc-nd)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-nc-nd)
- 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
- psychological stress, neuroinflammation, prefrontal cortex, lipopolysaccharide, microglial activation, TNF-α, brain-derived neurotrophic factor, mitogen-activated protein kinase, CREB, glucocorticoid receptor, mifepristone, neurodegeneration, astrocyte loss, neuronal loss
- MeSH terms
- Animals, Disease Susceptibility, Encephalitis, Lipopolysaccharides, Male, Nerve Tissue Proteins, Stress, Physiological, Rats, Wistar, Prefrontal Cortex, Rats
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