Greater inflammatory activity and blunted glucocorticoid signaling in monocytes of chronically stressed caregivers
Open accessAbstract
Chronic stress is associated with morbidity and mortality from numerous conditions, many of whose pathogenesis involves persistent inflammation. Here, we examine how chronic stress influences signaling pathways that regulate inflammation in monocytes. The sample consisted of 33 adults caring for a family member with glioblastoma and 47 controls whose lives were free of major stressors. The subjects were assessed four times over eight months. Relative to controls, caregivers' monocytes showed increased expression of genes bearing response elements for nuclear-factor kappa B, a key pro-inflammatory transcription factor. Simultaneously, caregivers showed reduced expression of genes with response elements for the glucocorticoid receptor, a transcription factor that conveys cortisol's anti-inflammatory signals to monocytes. Transcript origin analyses revealed that CD14+/CD16- cells, a population of immature monocytes, were the predominate source of inflammatory gene expression among caregivers. We considered hormonal, molecular, and functional explanations for caregivers' decreased glucocorticoid-mediated transcription. Across twelve days, the groups displayed similar diurnal cortisol profiles, suggesting that differential adrenocortical activity was not involved. Moreover, the groups' monocytes expressed similar amounts of glucocorticoid receptor protein, suggesting that differential receptor availability was not involved. In ex vivo studies, subjects' monocytes were stimulated with lipopolysaccharide, and caregivers showed greater production of the inflammatory cytokine interleukin-6 relative to controls. However, no group differences in functional glucocorticoid sensitivity were apparent; hydrocortisone was equally effective at inhibiting cytokine production in caregivers and controls. These findings may help shed light on the mechanisms through which caregiving increases vulnerability to inflammation-related diseases.
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Peripheral blood cells isolated from stressed individuals show increased production of spontaneous IL-6 and in response to immune challenge.
“Peripheral blood cells isolated from stressed individuals show increased production of spontaneous IL-6 and in response to immune challenge [12, 13].”
From Interleukin-6 Induced by Social Stress Promotes a Unique Transcriptional Signature in the Monocytes That Facilitate Anxiety (2019) · cites this paper as [12]
Transcriptional analysis of blood monocytes from stressed humans revealed an increased expression of chemotaxis and inflammation-related genes, and a corresponding decrease in regulatory (CX3CR1) genes, viral response genes, and glucocorticoid signaling genes.
“Transcriptional analysis of blood monocytes from stressed humans revealed an increased expression of chemotaxis and inflammation-related genes, and a corresponding decrease in regulatory (CX3CR1) genes, viral response genes, and glucocorticoid signaling genes [12, 32].”
From Interleukin-6 Induced by Social Stress Promotes a Unique Transcriptional Signature in the Monocytes That Facilitate Anxiety (2019) · cites this paper as [12]
PBMCs in WT mice show an exaggerated immune reactivity to ex vivo LPS after stress.
“Consistent with clinical studies of stress, our findings from the peripheral blood mononuclear cells (PBMCs) in WT mice show an exaggerated immune reactivity to ex vivo LPS after stress [12].”
From Interleukin-6 Induced by Social Stress Promotes a Unique Transcriptional Signature in the Monocytes That Facilitate Anxiety (2019) · cites this paper as [12]
There is an increased prevalence of circulating CD14+/CD16- monocytes (analogous to the CD11b+/Ly6Chi monocytes in mice) in individuals suffering from chronic stress.
“There is an increased prevalence of circulating CD14+/CD16- monocytes (analogous to the CD11b+/Ly6Chi monocytes in mice) in individuals suffering from chronic stress [12].”
From Interleukin-6 Induced by Social Stress Promotes a Unique Transcriptional Signature in the Monocytes That Facilitate Anxiety (2019) · cites this paper as [12]
Ex vivo LPS stimulation of peripheral monocytes from stressed individuals triggered an exaggerated production of IL-6.
“Furthermore, ex vivo LPS stimulation of peripheral monocytes from stressed individuals triggered an exaggerated production of IL-6 [12].”
From Interleukin-6 Induced by Social Stress Promotes a Unique Transcriptional Signature in the Monocytes That Facilitate Anxiety (2019) · cites this paper as [12]
CD14+/CD16- monocytes produced higher levels of IL-6 when stimulated with LPS ex vivo, suggesting that similar immune process occur in humans.
“Similar to Ly6C hi monocytes in mice, CD14 + /CD16 -monocytes produced higher levels of IL-6 when stimulated with LPS ex vivo (Miller et al, 2014), suggesting that similar immune process occur in humans.”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Miller et al, 2014
The primary source of upregulated inflammatory genes among caretakers was derived from an increased CD14+/CD16- monocyte population.
“Further investigation revealed that the primary source of upregulated inflammatory genes among caretakers was derived from an increased CD14 + /CD16 -monocyte population (Powell et al, 2013;Miller et al, 2014).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Miller et al, 2014
High circulating IL-6 predicted depressive episodes 6 months later.
“Furthermore, high circulating IL-6 predicted depressive episodes 6 months later (Miller and Cole, 2012).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as [100]
Childhood adversity promotes clustering of depressive episodes along with elevated circulating IL-6 and CRP.
“Childhood adversity promotes clustering of depressive episodes along with elevated circulating IL-6 and CRP”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as [100]
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- Authors
- Miller, G. E., Murphy, M. L. M., Cashman, R., Ma, R., Ma, J., Arevalo, J. M. G., Kobor, M. S., & Cole, S. W.
- Affiliations
- Northwestern University (US)
- BC Cancer Agency (CA)
- University of California, Los Angeles (US)
- University of British Columbia (CA)
- Corresponding author
- Miller, Gregory E.
- ORCID
- Venue
- Brain Behavior and Immunity
- Publisher
- Elsevier BV
- Published
- 2014-10
- Volume
- 41
- Pages
- 191-199
- ISSN
- 0889-1591 (ISSN-L)
- PMC
- PMC4973629
- OpenAlex
- W2140711005
- Cited by
- 166
- References
- 53
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 9 · 2023: 19 · 2022: 19 · 2021: 22 · 2020: 13 · 2019: 20 · 2018: 16 · 2017: 17 · 2016: 16 · 2015: 6 · 2014: 1
- FWCI
- 6.55
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Canadian Institutes of Health Research (89736)
- National Institute on Aging (R24AG037898, P30AG017265)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Psychiatry and Mental health › Cancer, Stress, Anesthesia, and Immune Response
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- chronic stress, caregivers, monocytes, inflammation, glucocorticoid signaling, glucocorticoid receptor, NF-κB, cortisol, CD14+CD16+ monocytes, interleukin-6, glucocorticoid sensitivity
- MeSH terms
- Adult, Brain Neoplasms, C-Reactive Protein, Cells, Cultured, Chronic Disease, Female, Glioblastoma, Humans, Hydrocortisone, Inflammation, Leukocytes, Lipopolysaccharides, Male, Middle Aged, Monocytes, Receptors, Glucocorticoid, Saliva, Stress, Psychological, Transcription, Genetic, Signal Transduction, Biomarkers, Caregivers, Gene Expression Profiling
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