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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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“Acute stress and inflammatory cytokines can actually induce early mobilization of neutrophils [30,31], though this effect may be enhanced or impaired pending exposure to different sex hormones [32].”
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“The underlying mechanisms that transduce mental states into molecular changes in mitochondria remain mostly to be de fi ned but certainly involve hormones acting directly on mitochondria, through the nucleus where they trigger bioenergetic recalibrations, or by diverting energy away from repair…”
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“However, although mainly anti-inflammatory, GCs’ effects on the immune system are known to vary depending on the specific immune process as well as by timing and dose of GC exposure (e.g. short-term vs. long-term effects on cell trafficking, Dhabhar et al., 2012).”
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“…end products of the HPA axis, there is also an effect of sympathetic activity (via the release of catecholamines, CATs) on immunological functioning during stress (for a review on the time-course, trajectory, and immune subpopulation-specificity, see Dhabhar et al., 2012; Nance and Sanders, 2007).”
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“stimulate glucocorticoid release, specifically cortisol, from the adrenal cortex, mobilizing immune cell trafficking in the body (Dhabhar et al., 2012; Faravelli et al., 2012).”
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“It has been argued that stress-induced increases in circulating glucocorticoids sensitise cells to pathogen-associated molecular patterns (PAMPs), dangerassociated molecular patterns (DAMPs) and inflammatory cytokines (Dhabhar et al., 2012; Del Giudice and Gangestad, 2018).”
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“Simultaneously, stress increases myelopoiesis and enhances the number of monocytes but also neutrophil granulocytes in the circulation via the release of catecholamines [40,41] by the sympathetic nervous system [42].”
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“The acute stress response seems to be important for supporting the redistribution of immune cells from source tissue over the blood stream and into target organs (Dhabhar et al. 2012).”
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“Additionally, experimentally induced psychological stress (Dhabhar et al. 2012) and physical exercise (Pedersen & Hoffman-Goetz, 2000), both of which increase circulating catecholamines, lead to increases in lymphocyte and neutrophil concentrations.”
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“The composition of this CD8þ T-cell pool is markedly altered to favour increased immune surveillance for antigen-presentation at secondary lymphoid organs and inflamed tissues (Dhabhar et al., 2012).”
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“This allocation of certain cells to defined parts of the body might represent a homeostatic immune-surveillance response (10), or, instead, it has been hypothesised that senescent T cells are mobilised into the blood to facilitate their subsequent apoptosis in peripheral tissues (21, 34), which may contribute to proge…”
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“Catecholamines induce the T and NK cells to move from the marginated pool (eg, bone marrow and lymph nodes) to the bloodstream temporarily.(64) Consequently, the T cells and monocytes were induced out of the bloodstream to the surgical site or the marginated pool.”
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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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