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Stress-induced redistribution of immune cells–from barracks to boulevards to battlefields: a tale of three hormones–Curt Richter Award winner
Open accessAbstract
Background The surveillance and effector functions of the immune system are critically dependent on the appropriate distribution of immune cells in the body. An acute or short-term stress response induces a rapid and significant redistribution of immune cells among different body compartments. Stress-induced leukocyte redistribution may be a fundamental survival response that directs leukocyte subpopulations to specific target organs during stress, and significantly enhances the speed, efficacy and regulation of an immune response. Immune responses are generally enhanced in compartments (e.g., skin) that are enriched with leukocytes, and suppressed in compartments that are depleted of leukocytes during/following stress. The experiments described here were designed to elucidate the: (1) Time-course, trajectory, and subpopulation-specificity of stress-induced mobilization and trafficking of blood leukocytes. (2) Individual and combined actions of the principal stress hormones, norepinephrine (NE), epinephrine (EPI), and corticosterone (CORT), in mediating mobilization or trafficking of specific leukocyte subpopulations. (3) Effects of stress/stress hormones on adhesion molecule, L-selectin (CD62L), expression by each subpopulation to assess its adhesion/functional/maturation status.Methods Male Sprague Dawley rats were stressed (short-term restraint, 2-120 min), or adrenalectomized and injected with vehicle (VEH), NE, EPI, CORT, or their combinations, and blood was collected for measurement of hormones and flow cytometric quantification of leukocyte subpopulations.Results Acute stress induced an early increase/mobilization of neutrophils, lymphocytes, helper T cells (Th), cytolytic T cells (CTL), and B cells into the blood, followed by a decrease/trafficking of all cell types out of the blood, except neutrophil numbers that continued to increase. CD62L expression was increased on neutrophils, decreased on Th, CTL, and natural killer (NK) cells, and showed a biphasic decrease on monocytes & B cells, suggesting that CD62L is involved in mediating the redistribution effects of stress. Additionally, we observed significant differences in the direction, magnitude, and subpopulation specificity of the effects of each hormone: NE increased leukocyte numbers, most notably CD62L⁻/⁺ neutrophils and CD62L⁻ B cells. EPI increased monocyte and neutrophil numbers, most notably CD62L⁻/⁺ neutrophils and CD62L⁻ monocytes, but decreased lymphocyte numbers with CD62L⁻/⁺ CTL and CD62L⁺ B cells being especially sensitive. CORT decreased monocyte, lymphocyte, Th, CTL, and B cell numbers with CD62L⁻ and CD62L⁺ cells being equally affected. Thus, naïve (CD62L⁺) vs. memory (CD62L⁻) T cells, classical (CD62L⁺) vs. non-classical (CD62L⁻) monocytes, and similarly distinct functional subsets of other leukocyte populations are differentially mobilized into the blood and trafficked to tissues by stress hormones.Conclusion Stress hormones orchestrate a large-scale redistribution of immune cells in the body. NE and EPI mobilize immune cells into the bloodstream, and EPI and CORT induce traffic out of the blood possibly to tissue surveillance pathways, lymphoid tissues, and sites of ongoing or de novo immune activation. Immune cell subpopulations appear to show differential sensitivities and redistribution responses to each hormone depending on the type of leukocyte (neutrophil, monocyte or lymphocyte) and its maturation/functional characteristics (e.g., non-classical/resident or classical/inflammatory monocyte, naïve or central/effector memory T cell). Thus, stress hormones could be administered simultaneously or sequentially to induce specific leukocyte subpopulations to be mobilized into the blood, or to traffic from blood to tissues. Stress- or stress hormone-mediated changes in immune cell distribution could be clinically harnessed to: (1) Direct leukocytes to sites of vaccination, wound healing, infection, or cancer and thereby enhance protective immunity. (2) Reduce leukocyte traffic to sites of inflammatory/autoimmune reactions. (3) Sequester immune cells in relatively protected compartments to minimize exposure to cytotoxic treatments like radiation or localized chemotherapy. (4) Measure biological resistance/sensitivity to stress hormones in vivo. In keeping with the guidelines for Richter Award manuscripts, in addition to original data we also present a model and synthesis of findings in the context of the literature on the effects of short-term stress on immune cell distribution and function.
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“Immune responses and associated clinical signs require time to respond (40), and the lack of a sizable response in this study could indicate a response in development or a simple reduction in infection potential for these calves.”
From Effect of source and journey on physiological variables in calves transported by road and ferry between Ireland and the Netherlands (2023) · cites this paper as [40]
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“Monocytes showed a similar but delayed pattern, which was expected as monocyte count typically responds to stress and infection slower than other immune subsets (40).”
From Effect of source and journey on physiological variables in calves transported by road and ferry between Ireland and the Netherlands (2023) · cites this paper as [40]
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“an acute stressor activates an acquired immune response via mediation by catecholamines and glucocorticoids and locally produced immune mediators; and, yet, a chronic exposure to the same stressor over several weeks has the opposite effect and results in immune suppression.”
From Neurobiological and Systemic Effects of Chronic Stress (2017) · cites this paper as [5]
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A REVIEW ON PAOM (PRAKRITI, AGNI, OJAS, MANAS): THE FOUR DOMAINS OF IMMUNITY
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The itch-scratch reflex generates protective immunityPreprint
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The Brain is not Mental! Coupling Neuronal and Immune Cellular Processing in Human OrganismsPreprint
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Interpersonal immune and emotion dynamics in couples
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“Specific to venous blood, previous studies have observed stress-induced changes in cell type composition in whole blood (Ožura et al. 2012; Dhabhar et al. 2012; Gotovac et al. 2010; Vidović et al. 2007; Boscarino and Chang 1999; Amati et al. 2010; Atanackovic et al. 2006).”
BackgroundEarly and subsequent life stress: physiological responses, moderating events and outcome
Muller, D. (2015) · University of the Witwatersrand, Johannesburg Institutional Repository on DSpace (University of the Witwatersrand, Johannesburg)
Temporal Mapping of Acute Stress-Induced Central and Circulating Cytokine Production
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The Science of Neuromuscular Healing
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Bibliometric Analysis of Psychological Literature Based on Web of Science Data
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“This idea aligns with findings and conclusions from other studies (Schwab et al. 2005; Dhabhar et al. 2012).”
ResultDiurnal and photoperiodic effects on the immune system and glucocorticoid signaling in domestic pigs
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“One best example that supports this statement is that short bouts of stress cause the immediate mobilization of immune cells in blood as a way to get us ready to “fight the danger” (causing our stress) (Dhabhar et al., 2012).”
BackgroundA new index of psychological stress reaction: Mitochondrial DNA
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LYMPHOCYTE TRAFFICKING FOLLOWING ACUTE STRESS AND ALTITUDE HYPOXIA IN LOW AND HIGH HEMATOCRIT SHEEP
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NEUROIMUNOMODULAÇÃO DO ESTRESSE E SUA BIDIRECIONALIDADE
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РЕАКЦІЯ ОРГАНІЗМУ КУРЕЙ НА ЗМІНУ ВИСОТИ РОЗТАШУВАННЯ КЛІТКОВОЇ БАТАРЕЇ
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Holding Together for Curing This Wounded World
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Metadata
- Authors
- Dhabhar, F. S., Malarkey, W. B., Neri, E., & McEwen, B. S.
- Affiliations
- Stanford Medicine (US)
- The Ohio State University (US)
- Rockefeller University (US)
- Corresponding author
- Dhabhar, Firdaus S.
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2012-09
- Volume
- 37
- Issue
- 9
- Pages
- 1345-1368
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC3412918
- OpenAlex
- W2042565214
- Cited by
- 589
- References
- 126
- Citations by year
- 2026: 45 · 2025: 38 · 2024: 46 · 2023: 52 · 2022: 53 · 2021: 69 · 2020: 50 · 2019: 51 · 2018: 36 · 2017: 34 · 2016: 38 · 2015: 33 · 2014: 27 · 2013: 13 · 2012: 4
- FWCI
- 10.22
- 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
- The John D. & Catherine T. MacArthur Foundation
- The DeWitt Wallace Foundation Fellowship
- The Dana Foundation
- NIH (AI48995, AR46299, CA107498)
- Carl & Elizabeth Naumann Fund
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Stress, Anesthesia, and Immune Response
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Keywords
- immune cell trafficking, norepinephrine, epinephrine, corticosterone, neutrophils, monocytes, B cells, T cells, natural killer cells, adrenalectomy, acute restraint stress, stress hormones, leukocyte mobilization, adhesion molecules, rats
- MeSH terms
- Adrenalectomy, Animals, Catecholamines, Cell Movement, Corticosterone, Epinephrine, Immune System, Leukocyte Count, Leukocytes, Male, Restraint, Physical, Stress, Physiological, Stress, Psychological, Rats, Sprague-Dawley, L-Selectin, Rats
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