Stress-induced changes in blood leukocyte distribution. Role of adrenal steroid hormones
Abstract
The numbers and proportions of leukocytes in the blood provide an important representation of the state of activation of the immune system, and of the pattern of distribution of immune cells in the body. We have shown previously that acute stress induces large, rapid, and reversible changes in the distribution of peripheral blood leukocyte subpopulations in the rat. The studies described here specifically investigate the role played by adrenal steroid hormones in mediating stress-induced changes in blood leukocyte distribution. Since adrenal steroids act at two distinct receptor subtypes that show a heterogeneity of expression in immune cells and tissues, the role played by each subtype in mediating changes in leukocyte distribution is also investigated. Cyanoketone, a corticosterone (CORT) synthesis inhibitor, significantly reduced the decrease in lymphocyte numbers observed during stress and significantly enhanced the increase in neutrophil numbers observed after the cessation of stress. Acute administration of aldosterone (a specific type I adrenal steroid receptor agonist) to adrenalectomized animals did not have a significant effect on blood leukocyte numbers. In contrast, acute administration of CORT (the endogenous type I and type II receptor agonist), or RU28362 (a specific type II receptor agonist), to adrenalectomized animals produced changes in leukocyte distribution that were similar to those observed in intact animals during stress. These results suggest that CORT, acting at the type II adrenal steroid receptor, is a major mediator of the stress-induced changes in blood lymphocyte and monocyte distribution.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Greater levels of glucocorticoid are associated with higher numbers of circulating neutrophils, lower numbers of circulating lymphocytes, and a lower neutrophil-to-lymphocyte ratio.
“Greater levels of glucocorticoid are associated with higher numbers of circulating neutrophils, lower numbers of circulating lymphocytes, and a lower neutrophil-to-lymphocyte (N/L) ratio-an overall marker of the trafficking of these cells (e.g., refs.22,23).”
From Chronic stress, glucocorticoid receptor resistance, inflammation, and disease risk (2012) · cites this paper as [23]
Cited by
Sorted by citations
Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000) · Endocrine Reviews · doi:10.1210/edrv.21.1.0389 · Cited by 7,541 · see citing works
Protective and Damaging Effects of Stress Mediators
McEwen, B. S. (1998) · New England Journal of Medicine · doi:10.1056/nejm199801153380307 · Cited by 6,733 · see citing works
Self-citationStress, adaptation, and disease. Allostasis and allostatic load
McEWEN, B. S. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09546.x · Cited by 5,092 · see citing works
Self-citationThe use of leukocyte profiles to measure stress in vertebrates: a review for ecologists
Davis, A. K., Maney, D. L., & Maerz, J. C. (2008) · Functional Ecology · doi:10.1111/j.1365-2435.2008.01467.x · Cited by 1,558 · see citing works
“Early work by Dougherty & White (1944) demonstrated that total leukocyte numbers dropped in mice and rats after injection with ACTH, reaching a low at 9 h post-injection and returning to normal levels at 24 h. Similar trends were seen in rats subjected to restraint for 2 h (Dhabhar et al. 1996).”
BackgroundChronic stress, glucocorticoid receptor resistance, inflammation, and disease risk
Cohen, S., Janicki-Deverts, D., Doyle, W. J., Miller, G. E., Frank, E., Rabin, B. S., & Turner, R. B. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1118355109 · Cited by 1,419 · see citing works
Effects of stress on immune function: The good, the bad, and the beautiful
Dhabhar, F. S. (2014) · Immunologic Research · doi:10.1007/s12026-014-8517-0 · Cited by 1,343 · see citing works
Self-citationKorte, S. M., Koolhaas, J. M., Wingfield, J. C., & McEwen, B. S. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.08.009 · Cited by 1,097 · see citing works
“The specific GR agonist RU38362 caused a rapid decrease in blood lymphocytes, monocytes and NK cell numbers whereas a MR agonist failed to do so, suggesting that glucocorticoids via GRs are involved in the decrease in leukocytes [226,227].”
BackgroundSelf-citationDhabhar, F. S. (2009) · Neuroimmunomodulation · doi:10.1159/000216188 · Cited by 903 · see citing works
Self-citationMcEwen, B. S., Biron, C. A., Brunson, K. W., Bulloch, K., Chambers, W. H., Dhabhar, F. S., Goldfarb, R. H., Kitson, R. P., Miller, A. H., Spencer, R. L., et al. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(96)00012-4 · Cited by 837 · see citing works
Self-citationStress, inflammation and cardiovascular disease
Black, P. H., & Garbutt, L. D. (2002) · Journal of Psychosomatic Research · doi:10.1016/s0022-3999(01)00302-6 · Cited by 793 · see citing works
Stress and the inflammatory response: A review of neurogenic inflammation
Black, P. H. (2002) · Brain Behavior and Immunity · doi:10.1016/s0889-1591(02)00021-1 · Cited by 687 · see citing works
Enhancing versus suppressive effects of stress hormones on skin immune function
Dhabhar, F. S., & McEwen, B. S. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.3.1059 · Cited by 672 · see citing works
Self-citationDhabhar, F. S., Malarkey, W. B., Neri, E., & McEwen, B. S. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.05.008 · Cited by 589 · see citing works
“Numerous studies have examined the effects of specific stress hormones on blood immune cell numbers (Benschop et al., 1996; Dale et al., 1974; Dhabhar et al., 1995b, 1996; Fauci and Dale, 1974; Schedlowski et al., 1993a).”
BackgroundMethodResultInfluentialSelf-citationSeasonal changes in vertebrate immune activity: mediation by physiological trade-offs
Martin, L. B., Weil, Z. M., & Nelson, R. J. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2142 · Cited by 575 · see citing works
“In contrast, when animals were stressed briefly just before immune challenge, they enhanced responses relative to non-stressed control animals (Dhabhar et al. 1996).”
BackgroundThe immediate effects of stress on hormones and plasma lysozyme in rainbow trout
Demers, N. E., & Bayne, C. J. (1997) · Developmental & Comparative Immunology · doi:10.1016/s0145-305x(97)00009-8 · Cited by 509 · see citing works
Dhabhar, F. S. (2002) · Brain Behavior and Immunity · doi:10.1016/s0889-1591(02)00036-3 · Cited by 464 · see citing works
Self-citationAn inflammatory review of glucocorticoid actions in the CNS
Sorrells, S. F., & Sapolsky, R. M. (2006) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2006.11.006 · Cited by 461 · see citing works
Stress and immunity in wild vertebrates: Timing is everything
Martin, L. B. (2009) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2009.03.008 · Cited by 449 · see citing works
Zoccali, C., Vanholder, R. C., Massy, Z. A., Ortíz, A., Sarafidis, P. A., Dekker, F. W., Fliser, D., Fouque, D. P., Heine, G. H., Jager, K. J., et al. (2017) · Nature Reviews Nephrology · doi:10.1038/nrneph.2017.52 · Cited by 464 · see citing works
The Stressed CNS: When Glucocorticoids Aggravate Inflammation
Sorrells, S. F., Caso, J. R., Munhoz, C. D., & Sapolsky, R. M. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.032 · Cited by 425 · see citing works
Position statement. Part two: Maintaining immune health.
Walsh, N. P., Gleeson, M., Pyne, D. B., Nieman, D. C., Dhabhar, F. S., Shephard, R. J., Oliver, S. J., Bermon, S., & Kajėnienė, A. (2011) · PubMed · Cited by 365 · see citing works
Self-citationStress-Induced Changes in Skin Barrier Function in Healthy Women
Altemus, M. M., Rao, B. K., Dhabhar, F. S., Ding, W., & Granstein, R. D. (2001) · Journal of Investigative Dermatology · doi:10.1046/j.1523-1747.2001.01373.x · Cited by 347 · see citing works
Self-citationInterpreting Stress Responses during Routine Toxicity Studies
Everds, N. E., Snyder, P. W., Bailey, K. L., Bolon, B. N., Creasy, D. M., Foley, G. L., Rosol, T. J., & Sellers, T. S. (2013) · Toxicologic Pathology · doi:10.1177/0192623312466452 · Cited by 338 · see citing works
Burgos-Aceves, M. A., Lionetti, L., & Faggio, C. (2019) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2019.03.275 · Cited by 317 · see citing works
Dhabhar, F. S. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.03.004 · Cited by 333 · see citing works
“Studies have also shown that glucocorticoid [69; 81; 82], and catecholamine [47; 76; 83; 84; 85; 86] hormones induce rapid and significant changes in leukocyte distribution and that these hormones are the major mediators of the effects of stress.”
BackgroundInfluentialSelf-citationStress as a neuroinflammatory condition in brain: Damaging and protective mechanisms
García‐Bueno, B., Caso, J. R., & Leza, J. C. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.04.001 · Cited by 280 · see citing works
Dhabhar, F. S. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb05454.x · Cited by 279 · see citing works
Self-citationProtective and Damaging Effects of Stress Mediators
McEwen, B. S. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/3077.003.0079 · Cited by 256 · see citing works
Self-citationEmbodying Psychological Thriving: Physical Thriving in Response to Stress
Epel, E. S., McEwen, B. S., & Ickovics, J. R. (1998) · Journal of Social Issues · doi:10.1111/j.1540-4560.1998.tb01220.x · Cited by 259 · see citing works
Self-citationStress-induced enhancement of leukocyte trafficking into sites of surgery or immune activation
Viswanathan, K., & Dhabhar, F. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501650102 · Cited by 246 · see citing works
Self-citationStress, testosterone, and the immunoredistribution hypothesis
Braude, S. H., Tang‐Martínez, Z., & Taylor, G. T. (1999) · Behavioral Ecology · doi:10.1093/beheco/10.3.345 · Cited by 244 · see citing works
Sopinka, N., Donaldson, M., O’Connor, C. M., Suski, C. D., & Cooke, S. J. (2016) · Fish physiology · doi:10.1016/b978-0-12-802728-8.00011-4 · Cited by 256 · see citing works
“WBC type are influenced by stressors (Dhabhar et al., 1996), and thus provide a useful”
BackgroundNeural immunoregulation: emerging roles for nerves in immune homeostasis and disease
Downing, J. R., & Miyan, J. A. (2000) · Immunology Today · doi:10.1016/s0167-5699(00)01635-2 · Cited by 235 · see citing works
Surgery induced immunosuppression
Hogan, B. V., Peter, M. B., Shenoy, H. G., Horgan, K. J., & Hughes, T. A. (2010) · The Surgeon · doi:10.1016/j.surge.2010.07.011 · Cited by 229 · see citing works
Stressor-specific alterations in corticosterone and immune responses in mice
Bowers, S. L., Bilbo, S. D., Dhabhar, F. S., & Nelson, R. J. (2008) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2007.07.012 · Cited by 222 · see citing works
“These cell population adjustments are not an indication of cell death; rather, they reflect a redistribution of cells to areas such as the skin, to prepare the organism for potential injury or infection (Dhabhar and McEwen, 1996a; 1997; Dhabhar et al., 1996).”
BackgroundResultSelf-citationDynamics of telomerase activity in response to acute psychological stress
Epel, E. S., Lin, J., Dhabhar, F. S., Wolkowitz, O. M., Puterman, E. M., Karan, L. D., & Blackburn, E. H. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.11.018 · Cited by 218 · see citing works
“During acute stress, immune cells mobilize into and then traffic out of the bloodstream (F. Dhabhar and McEwen, 1997; Dhabhar et al., 1996; F. S. Dhabhar, 1998; Schedlowski et al., 1993).”
BackgroundSelf-citationInterpreting indices of physiological stress in free-living vertebrates
Johnstone, C. P., Reina, R. D., & Lill, A. (2012) · Journal of Comparative Physiology B · doi:10.1007/s00360-012-0656-9 · Cited by 191 · see citing works
“N:L ratio is a traYcking of lymphocytes out of circulating blood to compartments such as the skin, spleen and lymph nodes, where they will be more useful in the event of injury (Dhabhar and McEwen 1997; Dhabhar et al. 1996).”
BackgroundInfluentialDhabhar, F. S. (2008) · Allergy Asthma and Clinical Immunology · doi:10.1186/1710-1492-4-1-2 · Cited by 190 · see citing works
“Third, stress- or pharmacologically induced increases in glucocorticoid hormones induce a significant decrease in blood lymphocyte and monocyte numbers.(1,25,41,47) Thus, stress conditions that result in a significant and sustained activation of the hypothalamic-pituitary-adrenal (HPA) axis result in a decrease in blo…”
BackgroundSelf-citationPinto, R. A., Arredondo, S. M., Bono, M. R., Gaggero, A. A., & DÍAZ, P. V. (2006) · PEDIATRICS · doi:10.1542/peds.2005-2119 · Cited by 180 · see citing works
NEUROENDOCRINE AND IMMUNE SYSTEM INTERACTIONS IN STRESS AND DEPRESSION
Miller, A. H. (1998) · Psychiatric Clinics of North America · doi:10.1016/s0193-953x(05)70015-0 · Cited by 177 · see citing works
Self-citationBilbo, S. D., Dhabhar, F. S., Viswanathan, K., Saul, A. N., Yellon, S. M., & Nelson, R. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.062001899 · Cited by 174 · see citing works
Self-citationSheriff, M. J., Krebs, C. J., & Boonstra, R. (2011) · Oecologia · doi:10.1007/s00442-011-1907-2 · Cited by 176 · see citing works
“because they are altered in a predictable manner (Dhabhar et al. 1996; Davis et al. 2008).”
BackgroundBlandino, P., Barnum, C. J., & Terrence Deak, B. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2005.11.021 · Cited by 175 · see citing works
“, 1984), whereas lower concentrations of CORT have been shown to facilitate immune function (Dhabhar et al., 1996; Fleshner et al., 2002).”
BackgroundInfluentialNeuroendocrine–immune interactions in fish: a role for interleukin-1
Engelsma, M. Y., Huising, M. O., van Muiswinkel, W. B., Flik, G., Kwang, J., Savelkoul, H. F. J., & Kemenade, B. M. L. V.-V. (2002) · Veterinary Immunology and Immunopathology · doi:10.1016/s0165-2427(02)00077-6 · Cited by 175 · see citing works
Martin, L. B., Gilliam, J., Han, P., Lee, K., & Wikelski, M. C. (2004) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2004.10.010 · Cited by 169 · see citing works
Dhabhar, F. S. (2009) · Integrative and Comparative Biology · doi:10.1093/icb/icp045 · Cited by 171 · see citing works
Self-citationStress, Leukocyte Trafficking, and the Augmentation of Skin Immune Function
Dhabhar, F. S. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb03151.x · Cited by 166 · see citing works
Self-citationDavis, A. K., & Maney, D. L. (2018) · Methods in Ecology and Evolution · doi:10.1111/2041-210x.13020 · Cited by 164 · see citing works
“As Dhabhar et al. (1996) put it, the cells can be thought of as foot soldiers in the body’s defensive army; during stress, they become mobilized and are shunted to different body compartments, depending on their function.”
BackgroundStress‐Induced Enhancement of Cell‐Mediated Immunity<sup>a</sup>
DHABHAR, F. S. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09575.x · Cited by 165 · see citing works
Self-citationEvolution of glucocorticoid receptors with different glucocorticoid sensitivity
Stolte, E. H., Kemenade, B. M. L. V.-V., Savelkoul, H. F. J., & Flik, G. (2006) · Journal of Endocrinology · doi:10.1677/joe.1.06703 · Cited by 162 · see citing works
“This stress-induced neutrophilia is considered to improve peripheral surveillance and is also reported in mammals (Dhabhar et al. 1996).”
BackgroundThe welfare of gestating sows in conventional stalls and large groups on deep litter
Karlen, G. A., Hemsworth, P. H., Gonyou, H. W., et al. (2006) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2006.05.014 · Cited by 158 · see citing works
“Several studies across a number of species have shown that increasing corticosteroids (endogenous or exogenous) concentrations result in a redistribution of white blood cells involved in the defence and immunological response against antigens, such as an increase of neutrophils (heterophils in poultry), a decrease of…”
BackgroundRomano, T. A., Keogh, M. J., Kelly, C., Feng, P., van Berk, L. H., Schlundt, C. E., Carder, D. A., & Finneran, J. J. (2004) · Canadian Journal of Fisheries and Aquatic Sciences · doi:10.1139/f04-055 · Cited by 156 · see citing works
“…bringing about changes in numbers and distribution of white blood cells including specific subsets of lymphocytes (e.g., T cells, T helper cells, cytotoxic T cells, and B cells) as well as changes in immune function (Sgoutas-Emch et al. 1994; Dhabhar et al. 1995, 1996) in both animals and humans.”
BackgroundSocial regulation of leukocyte homeostasis: the role of glucocorticoid sensitivity
Cole, S. W. (2008) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2008.02.006 · Cited by 156 · see citing works
Stress-induced enhancement of skin immune function: A role for γ interferon
Dhabhar, F. S., Satoskar, A. R., Bluethmann, H., David, J. R., & McEwen, B. S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.050569397 · Cited by 156 · see citing works
Self-citationLeukocyte subsets and neutrophil function after short-term spaceflight
Stowe, R. P., Sams, C. F., Mehta, S. K., Kaur, I., Jones, M. L., Feeback, D. L., & Pierson, D. L. (1999) · Journal of Leukocyte Biology · doi:10.1002/jlb.65.2.179 · Cited by 152 · see citing works
“cyte distribution in the body and the state of activation of the immune system [16, 17].”
BackgroundReview of the Amphibian Immune Response to Chytridiomycosis, and Future Directions
Grogan, L. F., Robert, J., Berger, L., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02536 · Cited by 152 · see citing works
“These results are consistent with a classic mammalian acute stress response [with the exception of the absence of lymphopaenia in the former study, (166)].”
ResultReyes, T. M., Walker, J. R., DeCino, C., Hogenesch, J. B., & Sawchenko, P. E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05607.2003 · Cited by 149 · see citing works
A hassle a day may keep the doctor away: stress and the augmentation of immune function
Dhabhar, F. S. (2002) · Integrative and Comparative Biology · doi:10.1093/icb/42.3.556 · Cited by 146 · see citing works
“…the corticosterone and epinephrine stress response) (Jensen, 1969; Keller et al., 1983; Dhabhar et al., 1995, 1996), or cyanoketone treatment (which eliminates only the corticosterone stress reponse), virtually eliminate the stress-induced redistribution of blood leukocytes (Dhabhar et al., 1996).”
BackgroundInfluentialSelf-citationCortisol Exerts bi-phasic Regulation of Inflammation in Humans
Yeager, M. P., Pioli, P. A., & Guyre, P. M. (2010) · Dose-Response · doi:10.2203/dose-response.10-013.yeager · Cited by 145 · see citing works
“…important consequences of these regulatory effects including enhanced adaptive immune responses to local antigen injection (Lyte et al. 1990; Dhabhar et al. 1996; Fleshner et al. 1998) and enhanced local inflammation in tissue injury models (Dinkel et al. 2003; Viswanathan and Dhabhar 2005).”
BackgroundTarcic, N., Ovadia, H., Weiss, D. W., & Weidenfeld, J. (1998) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(97)00186-0 · Cited by 142 · see citing works
Stress as an endogenous adjuvant: augmentation of the immunization phase of cell-mediated immunity
Viswanathan, K., Daugherty, C., & Dhabhar, F. S. (2005) · International Immunology · doi:10.1093/intimm/dxh286 · Cited by 138 · see citing works
“Contrary to the popular notion that stress is necessarily immunosuppressive, we initially suggested and showed that acute or naturalistic stressors have novel adjuvant-like immunoenhancing effects while chronic stress is immunosuppressive (2, 3, 18, 40).”
BackgroundSelf-citationEngelsma, M. Y. (2003) · Fish & Shellfish Immunology · doi:10.1016/s1050-4648(03)00006-8 · Cited by 140 · see citing works
Rohleder, N. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.12.015 · Cited by 136 · see citing works
Cīrule, D., Krama, T., Vrublevska, J., Rantala, M. J., & Krams, I. A. (2011) · Journal für Ornithologie · doi:10.1007/s10336-011-0719-9 · Cited by 137 · see citing works
“These changes in number of heterophiles, lymphocytes and eosinophils are thought to ensure that the different types of cells are routed to where they are needed during the stress response (Maxwell 1987; Maxwell and Robertson 1998; Dhabhar et al. 1994; Dhabhar et al. 1996 ).”
BackgroundKrüger, K., & Mooren, F. C. (2026) · PubMed · doi:10.22029/eir.2007.1629 · Cited by 137 · see citing works
Regulation of Macrophage Migration Inhibitory Factor Expression by Glucocorticoids in Vivo
Fingerle‐Rowson, G., Koch, P., Bikoff, R., Lin, X., Metz, C. N., Dhabhar, F. S., Meinhardt, A., & Bucala, R. (2003) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63797-2 · Cited by 134 · see citing works
“Glucocorticoids regulate the turnover and trafficking of leukocytes between immune compartments,(30) and selective changes in the number and/or the proportion of peripheral blood subpopulations have been shown to be a function of corticosterone levels in rodents.(35) To examine the physiological role of endogenous MIF…”
BackgroundSelf-citationFang, C. Y., Reibel, D. K., Longacre, M. L., Rosenzweig, S., Campbell, D. E., & Douglas, S. D. (2010) · The Journal of Alternative and Complementary Medicine · doi:10.1089/acm.2009.0018 · Cited by 130 · see citing works
Psychological stress and immunoprotection versus immunopathology in the skin
Dhabhar, F. S. (2012) · Clinics in Dermatology · doi:10.1016/j.clindermatol.2011.11.003 · Cited by 128 · see citing works
Self-citationPruett, S. B. (2003) · Pathophysiology · doi:10.1016/s0928-4680(03)00003-8 · Cited by 126 · see citing works
Effects of social stress on blood leukocyte distribution: the role of α- and β-adrenergic mechanisms
Engler, H., Dawils, L., Hoves, S., Kurth, S., Stevenson, J. R., Schauenstein, K., & Stefanski, V. (2004) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2004.08.005 · Cited by 122 · see citing works
Inbar, S., Neeman, E., Avraham, R., Benish, M., Rosenne, E., & Ben‐Eliyahu, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019246 · Cited by 121 · see citing works
“Stimulation of these receptors affects cytokine release [66], controls proliferation [67] and cell distribution [68,69,70,71], and has repeatedly been shown to suppress many aspects of CMI, NK cell and CTL activity in particular [17,48,72,73].”
BackgroundRefining approaches and diversifying directions in ecoimmunology
Martin, L. B., Weil, Z. M., & Nelson, R. J. (2006) · Integrative and Comparative Biology · doi:10.1093/icb/icl039 · Cited by 119 · see citing works
Dhabhar, F. S., Saul, A. N., Daugherty, C., Holmes, T. H., Bouley, D. M., & Oberyszyn, T. M. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.09.004 · Cited by 116 · see citing works
“…the time of immune activation or antigen exposure induces a redistribution of circulating immune cells to organs like the skin, subcutaneous tissues, and sentinel lymph nodes (Dhabhar and McEwen, 1997; Dhabhar et al., 1995b, 1996), increases leuko- 0889-1591/$ - see front matter 2009 Elsevier Inc.”
BackgroundSelf-citationHemond, C., Glanz, B., Bakshi, R., Chitnis, T., & Healy, B. (2019) · BMC Neurology · doi:10.1186/s12883-019-1245-2 · Cited by 115 · see citing works
“The NLR has a well-established short-term response to both endogenous and exogenous corticosteroids [12] and links to perceived stress in humans [13].”
BackgroundAssis, V. R., Titon, S. C. M., Barsotti, A. M. G., Titon, B., & Gomes, F. R. (2015) · PLoS ONE · doi:10.1371/journal.pone.0121005 · Cited by 112 · see citing works
Inflammatory Bowel Disease: A Stressed “Gut/Feeling”
Oligschlaeger, Y., Yadati, T., Houben, T., Oliván, C. M. C., & Shiri‐Sverdlov, R. (2019) · Cells · doi:10.3390/cells8070659 · Cited by 116 · see citing works
“Several preclinical studies have shown that short-term stress induces significant changes in absolute numbers and composition of blood leukocytes [116,117].”
BackgroundZhu, X., Liu, S.-J., Liu, Y., Wang, S., & Ni, X. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0250-9 · Cited by 111 · see citing works
“It was reported that GCs enhanced migration of leukocytes from the bloodstream to wound sites [ 22 ], and low physiological doses of cortisol stimulated the pro-inflammatory cytokine migration inhibitory factor (MIF) production in macrophages [23].”
BackgroundRestraint stress is associated with changes in glucocorticoid immunoregulation
Bauer, M. E., Perks, P., Lightman, S. L., & Shanks, N. M. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00503-0 · Cited by 110 · see citing works
Opposing Effects of Short- and Long-term Stress on Airway Inflammation
Forsythe, P., Ebeling, C., Gordon, J., Befus, A. D., & Vliagoftis, H. (2003) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200307-979oc · Cited by 108 · see citing works
Shini, S., & Kaiser, P. (2008) · Stress · doi:10.1080/10253890802526894 · Cited by 106 · see citing works
“Although immunosuppressive and anti-inflammatory actions of GCs have been recognised for decades, enhancement of immune function by GCs has been also reported (Jefferies 1991, 1994; Dhabhar et al. 1995, 1996; Dhabhar and McEwen 1997).”
BackgroundFrench, S. S., McLemore, R. Y., Vernon, B. L., et al. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.005348 · Cited by 104 · see citing works
“These stress-induced effects on immune function are likely regulated via redistribution of leukocytes throughout the body (Dhabhar et al., 1996) and/or CORT receptors present on lymphatic tissues and leukocytes themselves (Cidlowski et al., 1996; Leonard and Song, 2002; Weyts et al., 1998; Wiegers…”
BackgroundLeukocyte Coping Capacity: A Novel Technique for Measuring the Stress Response in Vertebrates
McLaren, G. W., Macdonald, D. W., Georgiou, C., Mathews, F., Newman, C., & Mian, R. (2003) · Experimental Physiology · doi:10.1113/eph8802571 · Cited by 103 · see citing works
Keil, D. E., Luebke, R. W., & Pruett, S. B. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.8.4543 · Cited by 103 · see citing works
Caroprese, M., Albenzio, M., Marzano, A., Schena, L., Annicchiarico, G., & Sevi, A. (2010) · Journal of Dairy Science · doi:10.3168/jds.2009-2604 · Cited by 97 · see citing works
Goessling, J. M., Kennedy, H., Mendonça, M. T., & Wilson, A. E. (2015) · Functional Ecology · doi:10.1111/1365-2435.12442 · Cited by 96 · see citing works
Delahanty, D. L., Bogart, L. M., & Figler, J. L. (2003) · AIDS Care · doi:10.1080/09540120410001641084 · Cited by 93 · see citing works
Minias, P. (2019) · Journal of Animal Ecology · doi:10.1111/1365-2656.12941 · Cited by 92 · see citing works
Lymphocyte subset numbers depend on the bacterial origin of sepsis
Holub, M., Klučková, Z., Helcl, M., PříAhodov, J., Rokyta, R., & Beran, O. (2003) · Clinical Microbiology and Infection · doi:10.1046/j.1469-0691.2003.00518.x · Cited by 88 · see citing works
Effects of hand massage on anxiety in cataract surgery using local anesthesia
Kim, M. S., Cho, K. S., Woo, H., et al. (2001) · Journal of Cataract & Refractive Surgery · doi:10.1016/s0886-3350(00)00730-6 · Cited by 90 · see citing works
Turner, J. E., Aldred, S., Witard, O. C., Drayson, M. T., Moss, P. M., & Bosch, J. A. (2010) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.07.239 · Cited by 90 · see citing works
“However, both animal and human evidence provide only limited support for this idea (Dhabhar et al., 1995, 1996).”
Does habitat fragmentation cause stress in the agile antechinus? A haematological approach
Johnstone, C. P., Lill, A., & Reina, R. D. (2011) · Journal of Comparative Physiology B · doi:10.1007/s00360-011-0598-7 · Cited by 83 · see citing works
“We suggest that it is unlikely that the N:L ratio represented an attenuated acute stress response in the pseudofragment males stemming from chronic stress in the undisturbed forest sites (Fig. 3) (Dhabhar and McEwen 1997; Dhabhar et al. 1996 ).”
BackgroundSmall, B. C., & Bilodeau, A. L. (2005) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2004.12.004 · Cited by 83 · see citing works
Physiology in conservation translocations
Tarszisz, E., Dickman, C. R., & Munn, A. J. (2014) · Conservation Physiology · doi:10.1093/conphys/cou054 · Cited by 83 · see citing works
“Additionally, persistent endocrinological responses to stressors can dampen the immune systems of animals, depressing their abilities to respond to immune challenges (Dhabhar et al., 1996), such as injury or exposure to pathogens or parasites (Bortolotti et al., 2009).”
BackgroundZhang, D., Kishihara, K., Wang, B., Mizobe, K., Kubo, C., & Nomoto, K. (1998) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(98)00197-0 · Cited by 75 · see citing works
Hagenaars, A., Meyer, I. J., Herzke, D., Pardo, B. G., Martinez, P., Pabon, M., De Coen, W., & Knapen, D. (2011) · Aquatic Toxicology · doi:10.1016/j.aquatox.2011.04.012 · Cited by 74 · see citing works
Rosenberger, P. H., Ickovics, J. R., Epel, E. S., Nadler, E., Jokl, P., Fulkerson, J. P., Tillie, J. M., & Dhabhar, F. S. (2009) · Journal of Bone and Joint Surgery · doi:10.2106/jbjs.h.00989 · Cited by 76 · see citing works
Self-citationCole, S. W., Mendoza, S. P., & Capitanio, J. P. (2009) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3181aa95a9 · Cited by 74 · see citing works
“Because this process is mediated specifically by GR signaling (42,47), the strength of association between circulating cortisol levels and leukocyte subset redistribution in circulating blood provides an in vivo hematological measure of immune cell sensitivity to regulation by endogenous glucocorticoids (30).”
BackgroundEffect of repeated restraint stress on the levels of intestinal IgA in mice
Jarillo‐Luna, A., Rivera‐Aguilar, V., Reyna-Garfias, H., Lara‐Padilla, E., Kormanovski, A., & Campos-Rodrı́guez, R. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.04.009 · Cited by 74 · see citing works
“Since glucocorticoids induce a redistribution of lymphocytes in several tissues (Dhabhar et al., 1995; Dhabhar et al., 1996; Dhabhar, 2002), they may reduce the homing of primed B-IgA+ cells to the mucosa.”
BackgroundNakamura, A., Fujiwara, S., Matsumoto, I., & Abe, K. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf900420g · Cited by 72 · see citing works
Smyth, G. P., Stapleton, P. P., Freeman, T. A., Concannon, E. M., Mestre, J. R., Duff, M., Maddali, S., & Daly, J. M. (2004) · Journal of Surgical Research · doi:10.1016/s0022-4804(03)00300-7 · Cited by 72 · see citing works
- Authors
- Dhabhar, F. S., Miller, A. H., McEwen, B. S., & Spencer, R. L.
- Affiliations
- Rockefeller University (US)
- University of Colorado Boulder (US)
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 1996-08
- Volume
- 157
- Issue
- 4
- Pages
- 1638-1644
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W2127386463
- Cited by
- 480
- References
- 0
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 11 · 2023: 9 · 2022: 13 · 2021: 15 · 2020: 13 · 2019: 17 · 2018: 14 · 2017: 14 · 2016: 14 · 2015: 21 · 2014: 21 · 2013: 13 · 2012: 23
- FWCI
- 5.48
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Health Sciences › Medicine › Psychiatry and Mental health › Cancer, Stress, Anesthesia, and Immune Response
- Keywords
- acute stress, adrenal steroids, corticosterone, type II glucocorticoid receptor, aldosterone, lymphocyte distribution, adrenalectomy, cyanoketone, immune activation
- MeSH terms
- Adrenal Cortex, Adrenal Cortex Hormones, Adrenalectomy, Aldosterone, Animals, Corticosterone, Cyanoketone, Enzyme Inhibitors, Leukocyte Count, Male, Receptors, Glucocorticoid, Restraint, Physical, Stress, Psychological, 3-Hydroxysteroid Dehydrogenases, Lymphocyte Subsets, Rats, Sprague-Dawley, Receptors, Mineralocorticoid, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
