Social stress up-regulates inflammatory gene expression in the leukocyte transcriptome via β-adrenergic induction of myelopoiesis
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Significance: Chronic exposure to adverse social environments is associated with increased risk of disease, and stress-related increases in the expression of proinflammatory genes appear to contribute to these effects. The present study identifies a biological mechanism of such effects in the ability of the sympathetic nervous system to up-regulate bone marrow production of immature, proinflammatory monocytes. These effects are mediated by β-adrenergic receptors and the myelopoietic growth factor GM-CSF, and suggest new targets for interventions to protect health in the context of chronic social stress.
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Chronic stress mobilizes the innate immune system and stimulates enhanced proliferation and release of inflammatory monocytes and neutrophils into the bloodstream.
“Chronic stress mobilizes the innate immune system and stimulates enhanced proliferation and release of inflammatory monocytes and neutrophils into the bloodstream12, 13.”
From Social stress induces neurovascular pathology promoting depression (2017) · cites this paper as [12]
The Mouse Monocyte Subset Differentiation section (page not available) reports increased proinflammatory monocytes and granulocytes in the blood and bone marrow after repeated social defeat; the mouse myeloid-lineage analysis also reports increased progenitors of both types. The paper does not identify the granulocytes specifically as neutrophils or directly measure their release into the bloodstream, and its human analysis concerns monocytes rather than neutrophils. (LLM, conf=0.84)
Experimental — accuracy not yet measuredSocial stress causes inflammatory gene expression in β-adrenergic pathways involving activation of the sympathetic nervous system.
“Powell et al. (2013) show that social stress causes inflammatory gene expression in 2-adrenergic pathways that involve the activation of the sympathetic nervous system.”
From Strong Enough to Suffer: Emotional Suppression, Stress Exposure, and Physiological Health Among Men Across the Life Course (2026) · cites this paper as Powell et al., 2013
Repeated social defeat causes rodents to release immature pro-inflammatory immune cells into circulation that promote inflammation at injury sites.
“RSD causes rodents to release immature, pro-inflammatory immune cells (CD11b+/Ly6C high) into circulation that serve to promote inflammation at the site of injury (Powell et al., 2013).”
From Developmental psychoneuroendocrine and psychoneuroimmune pathways from childhood adversity to disease (2017) · cites this paper as Powell et al., 2013
A diverse array of studies has documented similar leukocyte transcriptome shifts in adverse social conditions including low socioeconomic status, chronic stress, bereavement, post-traumatic stress disorder, and cancer diagnosis.
“Following the initial analyses of social isolation, a diverse array of studies has begun to document similar leukocyte transcriptome shifts in other adverse social conditions, including low socioeconomic status (SES) [9], [17]–[20], chronic stress (e.g., care-giving for a dying spouse) [21], [22], bereavement [23], post-traumatic stress disorder (PTSD) [24], [25], and cancer diagnosis [26], [27].”
From Human Social Genomics (2014) · cites this paper as [9]
Experimental animal models show that CTRA gene expression profiles can be induced in leukocytes by repeated social threat, unstable social hierarchies, and low social status.
“Subsequent studies using experimental animal models has shown that CTRA gene expression profiles can be induced in leukocytes by repeated social threat [9], unstable social hierarchies [8], [29], and low social status [7].”
From Human Social Genomics (2014) · cites this paper as [9]
Subsequent analysis of physically isolated leukocyte subpopulations confirmed that monocytes mediate many of the transcriptional effects of human social adversity, and animal mechanistic analyses determined that the SNS can up-regulate production of a distinct subpopulation of immature, proinflammatory monocytes by altering hematopoietic processes in the bone marrow.
“Subsequent analysis of physically isolated leukocyte subpopulations confirmed that monocytes mediate many of the transcriptional effects of human social adversity [21], [25], and mechanistic analyses in animal models determined that the SNS can up-regulate the production of a distinct subpopulation of immature, proinflammatory monocytes by altering hematopoietic processes in the bone marrow [9].”
From Human Social Genomics (2014) · cites this paper as [9]
These effects are mediated by beta-adrenergic signaling, which up-regulates transcription of GM-CSF (Csf3) and thereby enhances monocyte differentiation and development.
“These effects are again mediated by β-adrenergic signaling, which up-regulates transcription of the myelopoietic growth factor granulocyte-macrophage colony-stimulating factor (GM-CSF) (Csf3) and thereby enhances monocyte differentiation and development [9].”
From Human Social Genomics (2014) · cites this paper as [9]
In metastatic breast cancer, stress effects on tumor metastasis are mediated by beta-adrenergic up-regulation of monocytes and macrophages within the tumor microenvironment.
“In the context of metastatic breast cancer, for example, stress effects on tumor metastasis are mediated by β-adrenergic up-regulation of monocytes and macrophages within the tumor microenvironment [44] (i.e., the same dynamic that drives the CTRA transcriptome shift in circulating blood [9]).”
From Human Social Genomics (2014) · cites this paper as [9]
Studies show that isolation alters immune responses and promotes inflammation.
“For example, research demonstrates social isolation modulates immune responses and induces inflammation [40,41].”
From Social isolation: an underappreciated determinant of physical health (2022) · cites this paper as [40]
RSD increases monocyte and granulocyte progenitor cells in the BM that traffic into circulation and are redistributed throughout the body.
“For example, RSD increases monocyte and granulocyte progenitor cells in the BM that traffic into circulation and are redistributed throughout the body (Engler et al, 2004;Powell et al, 2013).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Powell et al, 2013
Chronic stressors or repeated exposure to social defeat shifts hematopoietic stem cell differentiation toward the myeloid cell lineage.
“Chronic stressors or repeated exposure to social defeat shifts hematopoietic stem cell differentiation toward the myeloid cell lineage.”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Powell et al, 2013
Treatment with a GM-CSF neutralizing antibody prevented RSD-induced expansion of granulocytes and monocytes.
“Furthermore, treatment with a GM-CSF neutralizing antibody prevented RSD-induced expansion of granulocytes and monocytes.”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Powell et al, 2013
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 Powell et al, 2013
RSD preferentially increases the amount of circulating Ly6C hi monocytes, which is prevented by blockage of the β-adrenergic receptor.
“Based on data from flow cytometry scatter properties, RSD preferentially increases the amount of circulating Ly6C hi monocytes (Powell et al, 2013;Wohleb et al, 2013;Ramirez et al, 2015a) that is prevented by blockage of the β-adrenergic receptor (Hanke et al, 2012;Powell et al, 2013).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Powell et al, 2013
Genome-wide transcriptional profiling indicates that splenetic monocytes upregulate MMP 8/9/13/14 in response to RSD.
“In support of this, genome-wide transcriptional profiling indicates that splenetic monocytes upregulate MMP 8/9/13/14 in response to RSD (Powell et al, 2013).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Powell et al, 2013
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 Powell et al, 2013
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 Powell et al, 2013
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Self-citationCheng, Y., Tang, X., Li, Y., Zhao, D., Cao, Q., Wu, H., Yang, H., Hao, K., & Yang, Y. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-18-2912 · Cited by 105 · see citing works
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Self-citationRamirez, K., Niraula, A., & Sheridan, J. F. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.08.011 · Cited by 101 · see citing works
Self-citation
- Authors
- Powell, N. D., Sloan, E. K., Bailey, M. T., Arevalo, J. M. G., Miller, G. E., Chen, E., Kobor, M. S., Reader, B. F., Sheridan, J. F., & Cole, S. W.
- Affiliations
- The Ohio State University (US)
- University of California, Los Angeles (US)
- Northwestern University (US)
- University of British Columbia (CA)
- Norman Cousins Center, Semel Institute for Neuroscience and Human Behavior, and Jonsson Comprehensive Cancer Center, University of California, Los Angeles, CA 90095;
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-09-23
- Volume
- 110
- Issue
- 41
- Pages
- 16574-16579
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3799381
- OpenAlex
- W2139463883
- Cited by
- 588
- References
- 66
- Citations by year
- 2026: 41 · 2025: 35 · 2024: 44 · 2023: 53 · 2022: 64 · 2021: 62 · 2020: 34 · 2019: 59 · 2018: 38 · 2017: 47 · 2016: 45 · 2015: 35 · 2014: 30 · 2013: 1
- FWCI
- 16.78
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- John D. and Catherine T. MacArthur Foundation
- National Institutes of Health (AG107265)
- University of California, Los Angeles
- National Institute on Aging (AG107265, P01AG018911, R37AG033590, R01AG034052, AG033590, P30AG017265)
- National Institute of Mental Health (MH46801, R01MH097243, R01MH046801, MH093473, R01MH093473)
- National Cancer Institute (R01CA116778, CA-116778)
- National Institute of Dental and Craniofacial Research (DE-014320, T32DE014320)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD058502, R01HD058502)
- 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 › Immunology and Microbiology › Immunology › Immune cells in cancer
- Keywords
- chronic social stress, social defeat, leukocyte transcriptome, inflammatory gene expression, myelopoiesis, beta-adrenergic signaling, sympathetic nervous system, inflammatory monocytes, Ly6C, peripheral blood mononuclear cells, low socioeconomic status, GM-CSF, PU.1, NF-κB, EGR1, MZF1, Nrf2, bone marrow hematopoiesis
- MeSH terms
- Animals, Flow Cytometry, Gene Expression Regulation, Humans, Male, Mice, Inbred C57BL, Monocytes, Propranolol, Receptors, Adrenergic, beta, Social Environment, Socioeconomic Factors, Stress, Psychological, Sympathetic Nervous System, Transcription Factors, Granulocyte-Macrophage Colony-Stimulating Factor, Computational Biology, Gene Expression Profiling, Myelopoiesis, Mice, Transcriptome
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