Peripheral and central effects of repeated social defeat stress: monocyte trafficking, microglial activation, and anxiety
Open accessAbstract
The development and exacerbation of depression and anxiety are associated with exposure to repeated psychosocial stress. Stress is known to affect the bidirectional communication between the nervous and immune systems leading to elevated levels of stress mediators including glucocorticoids (GCs) and catecholamines and increased trafficking of proinflammatory immune cells. Animal models, like the repeated social defeat (RSD) paradigm, were developed to explore this connection between stress and affective disorders. RSD induces activation of the sympathetic nervous system (SNS) and hypothalamic-pituitary-adrenal (HPA) axis activation, increases bone marrow production and egress of primed, GC-insensitive monocytes, and stimulates the trafficking of these cells to tissues including the spleen, lung, and brain. Recently, the observation that these monocytes have the ability to traffic to the brain perivascular spaces and parenchyma have provided mechanisms by which these peripheral cells may contribute to the prolonged anxiety-like behavior associated with RSD. The data that have been amassed from the RSD paradigm and others recapitulate many of the behavioral and immunological phenotypes associated with human anxiety disorders and may serve to elucidate potential avenues of treatment for these disorders. Here, we will discuss novel and key data that will present an overview of the neuroendocrine, immunological and behavioral responses to social stressors.
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Chronic psychosocial stress promotes an increase in glucocorticoid-insensitive monocyte populations, which can transmigrate across the blood-brain barrier and potentially contribute to long-term anxiety-related behaviors.
“Furthermore, chronic psychosocial stress promotes an increase in glucocorticoid (GC)-insensitive monocyte populations. Recent studies have also observed that these monocytes possess the ability to transmigrate across the blood–brain barrier, potentially contributing to the development of long-term anxiety-related behaviors [23].”
From Comparative Analysis of HPA-Axis Dysregulation and Dynamic Molecular Mechanisms in Acute Versus Chronic Social Defeat Stress (2025) · cites this paper as [23]
The physiological consequences of repeated social defeat are robustly associated with structural changes in neural systems that modulate threat-sensitivity and anxiety-like behaviors.
“In addition, the physiological consequences of exposure to RSD are robustly associated with structural changes (e.g., atrophy, connectivity) to neural systems that modulate threat-sensitivity and anxiety-like behaviors (Reader et al., 2015).”
From Developmental psychoneuroendocrine and psychoneuroimmune pathways from childhood adversity to disease (2017) · cites this paper as Reader et al., 2015
RSD is an ethologically relevant social stressor that recapitulates many of the stress-induced immune and behavioral outcomes of stress.
“Repeated social defeat (RSD) is an ethologically relevant social stressor that recapitulates many of the stress-induced immune and behavioral outcomes of stress (Reader et al, 2015).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Reader et al, 2015
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BackgroundResultInfluentialSelf-citationMicroglia, seen from the CX3CR1 angle
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“Along these same lines, RSD primes and activates peripherally derived monocytes inducing increased cytokine expression and resistance to the immunosuppressive effects of GCs (Engler et al., 2005; Wohleb et al., 2011, 2014a; Powell et al., 2013).”
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“…et al., 2006; Dantzer et al., 2008; Miller et al., 2009; Norman et al., 2010; Capuron and Miller, 2011), while the case continues to build for the mechanistic association between inflammation and anxiety (Maes et al., 1998; Pitsavos et al., 2006; O’Donovan et al., 2010; Pace and Heim, 2012).”
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“…with substantial CNS-related tissue pathology and inflammation, e.g., multiple sclerosis, traumatic injury, stroke, Alzheimer’s disease, or infection (Hafler et al., 2005; Gate et al., 2010; Donnelly et al., 2011; Hawthorne and Popovich, 2011; McGavern and Kang, 2011; de Vries et al., 2012).”
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“In the bone marrow, RSD increases production, egress, and trafficking of proinflammatory immune cells that are insensitive to GCs (Avitsur et al., 2002; Engler et al., 2004, 2005; Kinsey et al., 2007; Hanke et al., 2012; Wohleb et al., 2012) (Fig.”
BackgroundSelf-citationIn vivo structure/function and expression analysis of the CX3C chemokine fractalkine
Kim, K.-W., Vallon-Eberhard, A., Zigmond, E., Farache, J., Shezen, E., Shakhar, G., Ludwig, A., Lira, S. A., & Jung, S. (2011) · Blood · doi:10.1182/blood-2011-04-348946 · Cited by 275 · cited 1× · see citing works
“Under homeostatic conditions within the CNS, fractalkine is highly and primarily expressed by neurons (Bazan et al., 1997; Kim et al., 2011), while the fractalkine receptor is highly expressed by microglia (Jung et al., 2000).”
BackgroundThe spleen contributes to stroke‐induced neurodegeneration
Ajmo, C. T., Vernon, D. O. L., Collier, L. A., Hall, A. A., Garbuzova-Davis, S. N., Willing, A. E., & Pennypacker, K. R. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21661 · Cited by 272 · cited 1× · see citing works
“This increased egress was associated with more severe pathology (Ajmo et al., 2008) that was dependent upon peripheral noradrenergic signaling (Ajmo et al., 2009).”
BackgroundHafler, D. A., Slavik, J. M., Anderson, D. E., O’Connor, K. C., Jager, P. L. D., & Baecher‐Allan, C. (2005) · Immunological Reviews · doi:10.1111/j.0105-2896.2005.00240.x · Cited by 261 · see citing works
Lyons, A., Downer, E. J., Crotty, S., Nolan, Y. M., Mills, K. H. G., & Lynch, M. A. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1781-07.2007 · Cited by 258 · cited 1× · see citing works
“Because the brain is highly sensitive to increases in proinflammatory cytokines, microglia tend to be highly regulated by anti-inflammatory ligands and receptors (e.g., CD200/CD200R (Lyons et al., 2007), CX3CR1/CX3CL1 (Cardona et al., 2006), or TGFb/TGFbR (Butovsky et al., 2014)).”
BackgroundSocial stress: From rodents to primates
Tamashiro, K. L., Nguyen, M. M. N., & Sakai, R. R. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.03.001 · Cited by 249 · cited 1× · see citing works
“In the laboratory, murine social stress is modeled using resident–intruder paradigms whereby the response to social stress involves protecting the resources of the cage from intruders (Tamashiro et al., 2005).”
BackgroundWalker, F. R., Beynon, S. B., Jones, K., Zhao, Z., Kongsui, R., Cairns, M. J., & Nilsson, M. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.12.010 · Cited by 237 · see citing works
Donnelly, D. J., Longbrake, E. E., Shawler, T. M., Kigerl, K. A., Lai, W., Tovar, C. A., Ransohoff, R. M., & Popovich, P. G. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2114-11.2011 · Cited by 219 · cited 1× · see citing works
“…with substantial CNS-related tissue pathology and inflammation, e.g., multiple sclerosis, traumatic injury, stroke, Alzheimer’s disease, or infection (Hafler et al., 2005; Gate et al., 2010; Donnelly et al., 2011; Hawthorne and Popovich, 2011; McGavern and Kang, 2011; de Vries et al., 2012).”
BackgroundNorman, G. J., Karelina, K., Zhang, N., Walton, J. C., Morris, J. S., & DeVries, A. C. (2010) · Molecular Psychiatry · doi:10.1038/mp.2009.91 · Cited by 209 · cited 2× · see citing works
“…are not fully understood, the individual response to prolonged or severe stressors contributes to the development and exacerbation of depression and anxiety (Maes et al., 1998; Kalynchuk et al., 2004; Raison et al., 2006; Norman et al., 2010; Capuron and Miller, 2011; Gilman et al., 2013).”
BackgroundEngler, H., Bailey, M. T., Engler, A., & Sheridan, J. F. (2004) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2003.11.011 · Cited by 209 · cited 8× · see citing works
“1a) and traffic to the spleen (Engler et al., 2004), lung (Curry et al., 2010), and brain (Wohleb et al., 2013) (Fig.”
BackgroundMethodInfluentialSelf-citationWohleb, E. S., Patterson, J. M., Sharma, V., Quan, N., Godbout, J. P., & Sheridan, J. F. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3723-13.2014 · Cited by 209 · cited 23× · see citing works
“Along these same lines, RSD primes and activates peripherally derived monocytes inducing increased cytokine expression and resistance to the immunosuppressive effects of GCs (Engler et al., 2005; Wohleb et al., 2011, 2014a; Powell et al., 2013).”
BackgroundMethodInfluentialSelf-citationCorona, A. W., Huang, Y., O’Connor, J. C., Dantzer, R., Kelley, K. W., Popovich, P. G., & Godbout, J. P. (2010) · Journal of Neuroinflammation · doi:10.1186/1742-2094-7-93 · Cited by 200 · cited 1× · see citing works
“Fractalkine receptor stimulation of brain microglia is anti-inflammatory (Cardona et al., 2006; Corona et al., 2010) and promotes microglial quiescence under homeostatic conditions (Wolf et al., 2013).”
BackgroundSelf-citationKinsey, S. G., Bailey, M. T., Sheridan, J. F., Padgett, D. A., & Avitsur, R. (2007) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2006.11.001 · Cited by 190 · cited 4× · see citing works
“Anxiety-like behavior is most robustly observed following the six cycles of RSD, but also occurs in a cycle-dependent manner persisting to at least 8 days past the termination of the stressor (Kinsey et al., 2007; Wohleb et al., 2013).”
BackgroundInfluentialSelf-citationKalynchuk, L. E., Gregus, A., Boudreau, D., & Perrot-Sinal, T. S. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.6.1365 · Cited by 188 · cited 2× · see citing works
“…are not fully understood, the individual response to prolonged or severe stressors contributes to the development and exacerbation of depression and anxiety (Maes et al., 1998; Kalynchuk et al., 2004; Raison et al., 2006; Norman et al., 2010; Capuron and Miller, 2011; Gilman et al., 2013).”
BackgroundStansfeld, S. A., Head, J. A., Fuhrer, R., Wardle, J., & Cattell, V. (2003) · Journal of Epidemiology & Community Health · doi:10.1136/jech.57.5.361 · Cited by 182 · cited 1× · see citing works
“…of social status in the workplace have demonstrated increased incidence of depression, anxiety, loss of self-esteem, increased incidence of illness, and other aberrant physiological and behavioral symptoms (Marmot and Feeney, 1997; Griffin et al., 2002; Stansfeld et al., 2003; Bilgel et al., 2006).”
BackgroundSeifert, H. A., Hall, A. A., Chapman, C. B., Collier, L. A., Willing, A. E., & Pennypacker, K. R. (2012) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-012-9406-8 · Cited by 177 · cited 3× · see citing works
“Although the literature regarding myeloid-derived cell trafficking from the spleen is relatively sparse, in the context of cardiovascular disease and stroke, substantial gains have been made (Leuschner et al., 2012; Seifert et al., 2012).”
BackgroundBone Marrow Cell Recruitment to the Brain in the Absence of Irradiation or Parabiosis Bias
Kierdorf, K., Katzmarski, N., Haas, C. A., & Prinz, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058544 · Cited by 165 · cited 1× · see citing works
“Additionally, the control chimeric mice in these studies displayed little or no GFP+ cells within the CNS parenchyma, which is consistent with previous studies demonstrating that microglia are not bone marrowderived under homeostatic conditions (Kierdorf et al., 2013).”
ResultBlockade of adrenoreceptors inhibits the splenic response to stroke
Ajmo, C. T., Collier, L. A., Leonardo, C. C., Hall, A. A., Green, S. M., Womble, T. A., Cuevas, J., Willing, A. E., & Pennypacker, K. R. (2009) · Experimental Neurology · doi:10.1016/j.expneurol.2009.03.044 · Cited by 150 · cited 1× · see citing works
“This increased egress was associated with more severe pathology (Ajmo et al., 2008) that was dependent upon peripheral noradrenergic signaling (Ajmo et al., 2009).”
BackgroundTissue glucocorticoid resistance/hypersensitivity syndromes
Kino, T., Martino, M. U. D., Charmandari, E., Mirani, M., & Chrousos, G. P. (2003) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(03)00218-8 · Cited by 150 · cited 1× · see citing works
“It is possible that cytokines or neuroendocrine mediators induce GC-insensitivity by altering the number or function of GC receptors (Kino et al., 2003).”
BackgroundBeta adrenergic blockade decreases the immunomodulatory effects of social disruption stress
Hanke, M. L., Powell, N. D., Stiner, L. M., Bailey, M. T., & Sheridan, J. F. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.07.011 · Cited by 143 · see citing works
Self-citationBullying in Turkish white-collar workers
Bilgel, N., Aytaç, S., & Bayram, N. (2006) · Occupational Medicine · doi:10.1093/occmed/kqj041 · Cited by 141 · cited 1× · see citing works
“…of social status in the workplace have demonstrated increased incidence of depression, anxiety, loss of self-esteem, increased incidence of illness, and other aberrant physiological and behavioral symptoms (Marmot and Feeney, 1997; Griffin et al., 2002; Stansfeld et al., 2003; Bilgel et al., 2006).”
BackgroundSocinski, M., Cannistra, S., Sullivan, R., ELIAS, A. D., Antman, K. H., Schnipper, L. E., & Griffin, J. D. (1988) · Blood · doi:10.1182/blood.v72.2.691.691 · Cited by 138 · see citing works
Social stress in laboratory rats: hormonal responses and immune cell distribution
Stefanski, V. (2000) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(99)00066-9 · Cited by 137 · cited 2× · see citing works
“stress and severe infection causes a rapid release of neutrophils and monocytes into circulation referred to as neutrophilia and monocytosis, respectively subsequently leading to the increased production of these cells in the bone marrow (Stefanski and Engler, 1998; Stefanski, 2000; Powell et al., 2013).”
BackgroundKirby, B. S., Carlson, R. E., Markwald, R. R., Voyles, W. F., & Dinenno, F. A. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.131250 · Cited by 136 · cited 1× · see citing works
“GM-CSF, in particular, is a potent chemoattractant, and, by up-regulating CD11b expression, increases the adhesion of blood neutrophils and monocytes to the vascular endothelium (Socinski et al., 1988; Kirby et al., 2007).”
BackgroundBailey, M. T., Engler, H., Powell, N. D., Padgett, D. A., & Sheridan, J. F. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00307.2007 · Cited by 124 · cited 1× · see citing works
“…are not only GC-insensitive, but also possess a primed and activated phenotype, i.e., they have elevated levels of Toll-like receptors (TLRs), adhesion molecules, and co-stimulatory receptors on their surface (Avitsur et al., 2003; Engler et al., 2004; Bailey et al., 2007; Powell et al., 2009).”
BackgroundSelf-citationEffects of acute and chronic social stress on blood cellular immunity in rats
Stefanski, V., & Engler, H. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00127-9 · Cited by 119 · cited 1× · see citing works
“…and severe infection causes a rapid release of neutrophils and monocytes into circulation referred to as neutrophilia and monocytosis, respectively subsequently leading to the increased production of these cells in the bone marrow (Stefanski and Engler, 1998; Stefanski, 2000; Powell et al., 2013).”
BackgroundKim, M. H., Gorouhi, F., Ramirez, S., Granick, J. L., Byrne, B. A., Soulika, A. M., Simon, S. I., & Isseroff, R. R. (2013) · Journal of Investigative Dermatology · doi:10.1038/jid.2013.415 · Cited by 116 · cited 1× · see citing works
“…context of stress, bAR activation appears to primarily mediate the proinflammatory actions of the high surge of stress-induced catecholamines and is able to increase the production of cytokines in immune cells (e.g., Izeboud et al., 1999; Tynan et al., 2010; Johnson et al., 2013; Kim et al., 2014).”
BackgroundAngiotensin II Increases Monocyte Binding to Endothelial Cells
Kim, J. A., Berliner, J. A., & Nadler, J. L. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1441 · Cited by 115 · cited 1× · see citing works
“In other contexts, these same microglia-derived cytokines and chemokines are capable of increasing CAM expression on the luminal surface of vascular endothelial cells and increasing the respective receptors on vascular monocytes (Kim et al., 1996; Wang et al., 2007; Shi et al., 2011).”
Backgroundde Vries, H. E., Kooij, G., Frenkel, D., Georgopoulos, S., Monsonego, A., & Janigro, D. (2012) · Epilepsia · doi:10.1111/j.1528-1167.2012.03702.x · Cited by 113 · cited 1× · see citing works
“…with substantial CNS-related tissue pathology and inflammation, e.g., multiple sclerosis, traumatic injury, stroke, Alzheimer’s disease, or infection (Hafler et al., 2005; Gate et al., 2010; Donnelly et al., 2011; Hawthorne and Popovich, 2011; McGavern and Kang, 2011; de Vries et al., 2012).”
BackgroundMolecular mechanisms of glucocorticoid resistance in splenocytes of socially stressed male mice
Quan, N. (2003) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(03)00042-0 · Cited by 113 · cited 3× · see citing works
“Quan et al. (2003) examined the molecular mechanisms of GC-insensitivity in RSD splenocytes and found that the GC receptor in RSD splenocytes (CD11b+ cells) did not have the ability to suppress NFjB activity due to a failure of the GC receptor to translocate to the nucleus (Quan et al., 2003).”
BackgroundInfluentialPowell, N. D., Bailey, M. T., Mays, J. W., Stiner-Jones, L. M., Hanke, M. L., Padgett, D. A., & Sheridan, J. F. (2009) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2008.09.010 · Cited by 112 · cited 2× · see citing works
“, they have elevated levels of Toll-like receptors (TLRs), adhesion molecules, and co-stimulatory receptors on their surface (Avitsur et al., 2003; Engler et al., 2004; Bailey et al., 2007; Powell et al., 2009).”
BackgroundSelf-citationSocial hierarchy and dominance
Schein, M. W. (1975) · Medical Entomology and Zoology · Cited by 111 · see citing works
Participation of β-Adrenergic Receptors on Macrophages in Modulation of LPS-Induced Cytokine Release
Izeboud, C. A., Mocking, J. A. J., Monshouwer, M., van Miert, A. S. J. P. A. M., & Witkamp, R. F. (1999) · Journal of Receptors and Signal Transduction · doi:10.3109/10799899909036645 · Cited by 109 · cited 1× · see citing works
“…context of stress, bAR activation appears to primarily mediate the proinflammatory actions of the high surge of stress-induced catecholamines and is able to increase the production of cytokines in immune cells (e.g., Izeboud et al., 1999; Tynan et al., 2010; Johnson et al., 2013; Kim et al., 2014).”
BackgroundEngler, H., Engler, A., Bailey, M. T., & Sheridan, J. F. (2005) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2005.03.002 · Cited by 108 · cited 12× · see citing works
“Along these same lines, RSD primes and activates peripherally derived monocytes inducing increased cytokine expression and resistance to the immunosuppressive effects of GCs (Engler et al., 2005; Wohleb et al., 2011, 2014a; Powell et al., 2013).”
BackgroundInfluentialSelf-citationMacrophages in Alzheimer’s disease: the blood-borne identity
Gate, D., Rezai-Zadeh, K., Jodry, D., Rentsendorj, A., & Town, T. (2010) · Journal of Neural Transmission · doi:10.1007/s00702-010-0422-7 · Cited by 107 · cited 2× · see citing works
“, multiple sclerosis, traumatic injury, stroke, Alzheimer’s disease, or infection (Hafler et al., 2005; Gate et al., 2010; Donnelly et al., 2011; Hawthorne and Popovich, 2011; McGavern and Kang, 2011; de Vries et al., 2012).”
BackgroundPsychosocial stressors and the prognosis of major depression: a test of Axis IV
Gilman, S. E., Trinh, N., Smoller, J. W., D, M. F. M., Murphy, J. M., & Breslau, J. A. (2012) · Psychological Medicine · doi:10.1017/s0033291712001080 · Cited by 102 · cited 2× · see citing works
“…are not fully understood, the individual response to prolonged or severe stressors contributes to the development and exacerbation of depression and anxiety (Maes et al., 1998; Kalynchuk et al., 2004; Raison et al., 2006; Norman et al., 2010; Capuron and Miller, 2011; Gilman et al., 2013).”
BackgroundSawicki, C. M., McKim, D. B., Wohleb, E. S., Jarrett, B. L., Reader, B. F., Norden, D. M., Godbout, J. P., & Sheridan, J. F. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2014.10.004 · Cited by 101 · see citing works
Hypertension, Angiotensin, and Stroke: Beyond Blood Pressure
Iadecola, C., & Gorelick, P. B. (2004) · Stroke · doi:10.1161/01.str.0000115162.16321.aa · Cited by 101 · cited 2× · see citing works
“However, this concept has expanded to explain vascular–neuronal interactions in the context of inflammatory CNS pathology, e.g., Alzheimer’s disease and stroke (Iadecola and Gorelick, 2004).”
BackgroundEngler, H., Bailey, M. T., Engler, A., Stiner-Jones, L. M., Quan, N., & Sheridan, J. F. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.10.007 · Cited by 97 · cited 5× · see citing works
“…data using the RSD paradigm had an intense focus on the stress-induced modulation of peripheral immune compartments (Avitsur et al., 2001; Bailey et al., 2004; Engler et al., 2004, 2008; Hanke et al., 2012), recent focus has shifted toward the effects of social defeat on behavior and the brain.”
BackgroundMethodInfluentialSelf-citationSystemic Inflammation‐Associated Glucocorticoid Resistance and Outcome of ARDS
Meduri, G. U., & Yates, C. R. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1321.004 · Cited by 97 · cited 1× · see citing works
“Associated with the experience of social stress, it is this prolonged inflammatory state that has the potential to contribute to the etiology of depression and anxiety (Meduri and Yates, 2004; Barnes and Adcock, 2009).”
BackgroundSocial disruption-induced glucocorticoid resistance: kinetics and site specificity
Avitsur, R., Stark, J. L., Dhabhar, F. S., Padgett, D. A., & Sheridan, J. F. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00010-3 · Cited by 92 · cited 11× · see citing works
“For instance, the RSD-induced establishment and resolution of GC-insensitivity (Avitsur et al., 2002) and increased myelopoiesis (Engler et al., 2004; Wohleb et al., 2013) follow similar kinetics to the development of anxiety-like behavior (Wohleb et al., 2013).”
BackgroundInfluentialSelf-citationEmerging Concepts in Myeloid Cell Biology after Spinal Cord Injury
Hawthorne, A. L., & Popovich, P. G. (2011) · Neurotherapeutics · doi:10.1007/s13311-011-0032-6 · Cited by 90 · cited 2× · see citing works
“, multiple sclerosis, traumatic injury, stroke, Alzheimer’s disease, or infection (Hafler et al., 2005; Gate et al., 2010; Donnelly et al., 2011; Hawthorne and Popovich, 2011; McGavern and Kang, 2011; de Vries et al., 2012).”
BackgroundAtaka, K., Asakawa, A., Nagaishi, K., Kaimoto, K., Sawada, A., Hayakawa, Y., Tatezawa, R., Inui, A., & Fujimiya, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0081744 · Cited by 89 · cited 5× · see citing works
“Interestingly, the stress associated with simply observing other mice undergoing foot shock was sufficient to recruit monocytes to the brain parenchyma (Ataka et al., 2013).”
BackgroundResultInfluentialGeneral explanations for social inequalities in health.
Marmot, M. G., & Feeney, A. (1997) · PubMed · Cited by 87 · see citing works
Sawada, A., Niiyama, Y., Ataka, K., Nagaishi, K., Yamakage, M., & Fujimiya, M. (2014) · Pain · doi:10.1016/j.pain.2014.05.031 · Cited by 86 · cited 14× · see citing works
“Additionally, both chemokine (C–C motif) receptor 2 (CCR2) and bAR signaling contributed to the trafficking of bone marrow-derived monocytes to the brain (Ataka et al., 2013; Sawada et al., 2014).”
BackgroundResultInfluentialBailey, M. T., Kinsey, S. G., Padgett, D. A., Sheridan, J. F., & Leblebicioğlu, B. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.06.013 · Cited by 84 · cited 1× · see citing works
“One response to RSD is the development of anxietylike behavior, which is evident in tests like open field, novel object, and light/dark assays (Kinsey et al., 2007; Bailey et al., 2009; Wohleb et al., 2011; Hanke et al., 2012).”
BackgroundSelf-citationExpression of glucocorticoid resistance following social stress requires a second signal
Avitsur, R., Padgett, D. A., Dhabhar, F. S., Stark, J. L., Kramer, K. A., Engler, H., & Sheridan, J. F. (2003) · Journal of Leukocyte Biology · doi:10.1189/jlb.0303090 · Cited by 81 · cited 1× · see citing works
“…are not only GC-insensitive, but also possess a primed and activated phenotype, i.e., they have elevated levels of Toll-like receptors (TLRs), adhesion molecules, and co-stimulatory receptors on their surface (Avitsur et al., 2003; Engler et al., 2004; Bailey et al., 2007; Powell et al., 2009).”
BackgroundSelf-citationFreeman, D., Thompson, C., Vorontsova, N., Dunn, G., Carter, L.-A., Garety, P., Kuipers, E., Slater, M., Antley, A., Glucksman, E., et al. (2013) · Psychological Medicine · doi:10.1017/s003329171300038x · Cited by 79 · cited 1× · see citing works
“For example, both RSD and PTSD involve a sensitizing event that is often both physical and psychological in nature (Bailey et al., 2004; American Psychiatric Association, 2013; Freeman et al., 2013).”
BackgroundBailey, M. T., Avitsur, R., Engler, H., Padgett, D. A., & Sheridan, J. F. (2003) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2003.09.012 · Cited by 74 · cited 4× · see citing works
“Defeated subordinate animals receive bite wounds and experience pain that is not life-threatening, but contributes to significant changes in the immune system, cellular activation in the CNS, and expression of prolonged anxiety-like behavior (Bailey et al., 2004).”
BackgroundMethodInfluentialSelf-citationChronic foot‐shock stress potentiates the influx of bone marrow‐derived microglia into hippocampus
Brevet, M., Kojima, H., Asakawa, A., Atsuchi, K., Ushikai, M., Ataka, K., Inui, A., Kimura, H., Sevestre, H., & Fujimiya, M. (2010) · Journal of Neuroscience Research · doi:10.1002/jnr.22362 · Cited by 62 · cited 4× · see citing works
“For example, following 5 days of foot shock stress, bone marrow-derived monocytes trafficked to the ventral hippocampus and demonstrated a ramified, microglia-like morphological phenotype (Brevet et al., 2010).”
BackgroundResultInfluentialBeta-adrenergic receptor activation primes microglia cytokine production
Johnson, J. D., Zimomra, Z. R., & Stewart, L. T. (2012) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2012.08.007 · Cited by 60 · cited 1× · see citing works
“…context of stress, bAR activation appears to primarily mediate the proinflammatory actions of the high surge of stress-induced catecholamines and is able to increase the production of cytokines in immune cells (e.g., Izeboud et al., 1999; Tynan et al., 2010; Johnson et al., 2013; Kim et al., 2014).”
BackgroundSocial disruption induces lung inflammation
Curry, J. M., Hanke, M. L., Piper, M. G., Bailey, M. T., Bringardner, B. D., Sheridan, J. F., & Marsh, C. B. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.10.019 · Cited by 51 · cited 1× · see citing works
“1a) and traffic to the spleen (Engler et al., 2004), lung (Curry et al., 2010), and brain (Wohleb et al., 2013) (Fig.”
BackgroundSelf-citationKerfoot, S. M., & Kubes, P. (2005) · Journal of Leukocyte Biology · doi:10.1189/jlb.1004607 · Cited by 30 · cited 1× · see citing works
“Likewise, in a model of inflammatory liver disease, Kerfoot and Kubes (2005) demonstrated that recruitment of TNF-a-expressing monocytes to the brain promoted depressive-like behavior and fatigue.”
BackgroundSubordinate social status modulates the vulnerability to the immunological effects of social stress
Avitsur, R., Kinsey, S. G., Bidor, K., Bailey, M. T., Padgett, D. A., & Sheridan, J. F. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.09.005 · Cited by 29 · cited 5× · see citing works
“It is important to note that not all RSD mice develop this state of GC-insensitivity in the spleen; it is most robust in mice that exhibited more subordinate behaviors during the stress treatment (Avitsur et al., 2007).”
BackgroundInfluentialSelf-citationMolecular Mechanisms of Clucocorticoid Resistance/Hypersensitivity: Potential Clinical Implications
Chrousos, G. P., de Castro, M., Leung, D. Y. M., Webster, E., Kino, T., Bamberger, C. M., Elliot, S. J., Stratakis, C. A., & Karl, M. (1996) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm/154.2_pt_2.s39 · Cited by 26 · see citing works
Conditions required for myelopoiesis in murine spleen
Ohno, H., Ogawa, M., Nishikawa, S., Hayashi, S.-I., Kunisada, T., & Nishikawa, S.-I. (1993) · Immunology Letters · doi:10.1016/0165-2478(93)90091-f · Cited by 22 · cited 1× · see citing works
“The murine spleen has low myelopoietic activity and most of the granulocytes and monocytes that circulate come from the bone marrow (Ohno et al., 1993).”
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Microglia in physiology and disease
Wolf, S. A., Boddeke, H. W. G. M., & Kettenmann, H. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034406 · Cited by 1,426 · see citing works
Neuroimmune mechanisms of depression
Hodes, G. E., Kana, V., Menard, C., Merad, M., & Russo, S. J. (2015) · Nature Neuroscience · doi:10.1038/nn.4113 · Cited by 585 · see citing works
Pathogenesis of depression: Insights from human and rodent studies
Ménard, C., Hodes, G. E., & Russo, S. J. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2015.05.053 · Cited by 593 · see citing works
“…of monocytes originating from the periphery in the brain (Wohleb et al., 2013), suggesting that blood brain-barrier (BBB) permeability may be affected by stress and could contribute to the establishment of depressive-like behaviors and mood disorders (Wohleb et al., 2014b, Reader et al., 2015).”
BackgroundAnimal models of major depression: drawbacks and challenges
Planchez, B., Surget, A., & Belzung, C. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02084-y · Cited by 480 · see citing works
Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal
Weber, M. D., Godbout, J. P., & Sheridan, J. F. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.102 · Cited by 283 · see citing works
“Repeated social defeat (RSD) is an ethologically relevant social stressor that recapitulates many of the stress-induced immune and behavioral outcomes of stress (Reader et al, 2015).”
BackgroundSelf-citationLiu, Y., Zhao, J., & Guo, W. (2018) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.02201 · Cited by 268 · see citing works
Deslauriers, J., Tóth, M., Der‐Avakian, A., & Risbrough, V. B. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.11.019 · Cited by 253 · see citing works
“SDS also robustly induces enduring peripheral and central inflammation (68).”
Kuhlman, K. R., Chiang, J. J., Horn, S., & Bower, J. E. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.05.020 · Cited by 208 · see citing works
“In rodents, the repeated social defeat (RSD) paradigm (Avitsur et al., 2001; Reader et al., 2015) involves placing a large, aggressive rat in the participant rat’s cage for 2 h each day for a week.”
InfluentialNeuroinflammatory Dynamics Underlie Memory Impairments after Repeated Social Defeat
McKim, D. B., Niraula, A., Tarr, A. J., Wohleb, E. S., Sheridan, J. F., & Godbout, J. P. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2394-15.2016 · Cited by 204 · see citing works
“Recent work reveals that chronic stress triggers immune dysfunction that is causally implicated in mental health disturbances (Glaser and Kiecolt-Glaser, 2005; Wohleb et al., 2014b; Reader et al., 2015).”
BackgroundSelf-citationCirculating myeloid-derived MMP8 in stress susceptibility and depression
Cathomas, F., Lin, H.-Y., Chan, K. L., Li, L., Parise, L. F., Alvarez, J., Durand-de Cuttoli, R., Aubry, A. V., Muhareb, S., Desland, F., et al. (2024) · Nature · doi:10.1038/s41586-023-07015-2 · Cited by 189 · see citing works
“…morphological, transcriptional and functional changes indicative of an inflammatory signature in microglia from other brain regions 37,38 , to our knowledge, this is the first study investigating g , Uniform manifold approximation and projection (UMAP) representation of four clusters…”
BackgroundModulation of anti-tumor immunity by the brain’s reward system
Ben-Shaanan, T. L., Schiller, M., Azulay‐Debby, H., Korin, B., Boshnak, N., Koren, T., Krot, M., Shakya, J., Rahat, M. A., Hakim, F., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05283-5 · Cited by 174 · see citing works
Control of Leukocyte Trafficking by Stress-Associated Hormones
Ince, L. M., Weber, J., & Scheiermann, C. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2018.03143 · Cited by 168 · see citing works
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Social Stress Mobilizes Hematopoietic Stem Cells to Establish Persistent Splenic Myelopoiesis
McKim, D. B., Yin, W., Wang, Y., Cole, S. W., Godbout, J. P., & Sheridan, J. F. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.102 · Cited by 153 · see citing works
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“poor sleep [38] and severe stress [31,39,40] each can result in such aberrant glial activation.”
BackgroundInfluentialNiraula, A., Wang, Y., Godbout, J. P., & Sheridan, J. F. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.2568-17.2018 · Cited by 137 · see citing works
“The clinical features of chronic stress (e.g., glucocorticoid resistance, enhanced proinflammatory profile, and elevated plasma IL-6) are recapitulated in the repeated social defeat (RSD) model of stress in mice (Wohleb et al., 2014a; Reader et al., 2015).”
BackgroundSelf-citationStein, D. J., Vasconcelos, M., Albrechet‐Souza, L., Ceresér, K. M., & de Almeida, R. M. M. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00207 · Cited by 137 · see citing works
“This process can worsen tissue damage and negatively impact disease outcome, leading to anxiety- and depressive-like states (Reader et al., 2015; Ramirez and Sheridan, 2016).”
BackgroundSympathetic Release of Splenic Monocytes Promotes Recurring Anxiety Following Repeated Social Defeat
McKim, D. B., Patterson, J. M., Wohleb, E. S., Jarrett, B. L., Reader, B. F., Godbout, J. P., & Sheridan, J. F. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.07.010 · Cited by 137 · see citing works
“Taken together, monocyte trafficking to the brain represents a novel axis of immune-to-brain signaling that promotes prolonged behavioral responses to stress (30,31).”
BackgroundSelf-citationGuo, M., Li, C., Lei, Y., Xu, S., Zhao, D., & Lu, X.-Y. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.225 · Cited by 128 · see citing works
Bajinka, O., Simbilyabo, L., Tan, Y., Jabang, J. N., & Saleem, S. A. (2021) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2021.1960483 · Cited by 128 · see citing works
“The lung RAS involves acute respiratory distress syndrome, inflammation, pulmonary fibrosis and COPD (Reader et al. 2015).”
BackgroundInfluentialFluoxetine Inhibits NLRP3 Inflammasome Activation: Implication in Depression
Du, R., Tan, J., Sun, X., Lu, M., Ding, J., & Hu, G. (2016) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyw037 · Cited by 128 · see citing works
“Several lines of evidence have demonstrated that peripheral inflammation plays an important role in the progression of depression (Reader et al., 2015).”
BackgroundWohleb, E. S., & Delpech, J.-C. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.04.013 · Cited by 128 · see citing works
Self-citationBower, J. E., & Kuhlman, K. R. (2023) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-080621-045153 · Cited by 133 · see citing works
Ramírez, K., Trías, J. F., & Sheridan, J. F. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_25 · Cited by 112 · see citing works
“Specifically, RSD causes an increase of IL-6, TNF-α, keratinocyte chemoattractant, macrophage inflammatory protein-2 (CCL8/MCP-2), and monocyte chemoattractant protein-1 (CCL2/MCP-1) [3].”
BackgroundInfluentialSelf-citationMitochondria, Microglia, and the Immune System—How Are They Linked in Affective Disorders?
Culmsee, C., Michels, S., Scheu, S., Arolt, V., Dannlowski, U., & Alferink, J. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00739 · Cited by 110 · see citing works
Cheng, Y., Wang, Y., Wang, X., Jiang, Z., Zhu, L., & Fang, S. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.893097 · Cited by 110 · see citing works
Ramirez, 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
“Neuroinflammatory mediators such as IL1-b, TNF-a, and IL-6, are related in the neurobiological changes that reinforce fear/anxiety and threat circuitry (Wohleb et al., 2015), promoting the development and maintenance of anxiety-like behavior (Reader et al., 2015).”
BackgroundSelf-citationDiSabato, D. J., Nemeth, D. P., Liu, X., Witcher, K. G., O’Neil, S. M., Oliver, B., Bray, C. E., Sheridan, J. F., Godbout, J. P., & Quan, N. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0788-3 · Cited by 93 · see citing works
Self-citationA survey of neuroimmune changes in pregnant and postpartum female rats
Haim, A., Julian, D. L., Albin-Brooks, C., Brothers, H. M., Lenz, K. M., & Leuner, B. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.09.026 · Cited by 82 · see citing works
Role of the androgen receptor in the central nervous system
Mhaouty‐Kodja, S. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.08.001 · Cited by 84 · see citing works
“Indeed, novel data suggest the involvement of the immune system including microglia cells in the development of anxiety in response to stress (reviewed in Reader et al., 2015).”
BackgroundThe effects of trauma on brain and body: A unifying role for the midbrain periaqueductal gray
Terpou, B. A., Harricharan, S., McKinnon, M. C., Frewen, P., Jetly, R., & Lanius, R. A. (2019) · Journal of Neuroscience Research · doi:10.1002/jnr.24447 · Cited by 82 · see citing works
“…somatic syndromes such as irritable bowel syndrome and esophageal reflux are associated with autonomic‐related altera‐ tions and have high comorbidities in PTSD and other anxiety disor‐ ders (Cohen et al., 2006; Jarrett et al., 2015; Kendall‐Tackett, 2000; for a review, see Afari et al., 2014).”
BackgroundWalsh, C. P., Bovbjerg, D. H., & Marsland, A. L. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.013 · Cited by 81 · see citing works
Pires, G. N., Bezerra, A. G., Tufik, S. B., & Andersen, M. L. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.06.028 · Cited by 79 · see citing works
Picard, K., St‐Pierre, M., Vecchiarelli, H. A., Bordeleau, M., & Tremblay, M. (2021) · Neurochemistry International · doi:10.1016/j.neuint.2021.104987 · Cited by 77 · see citing works
Inflammation in the pathogenesis of depression: a disorder of neuroimmune origin
Corrigan, M., O’Rourke, A. M., Moran, B., Fletcher, J. M., & Harkin, A. (2023) · Neuronal Signaling · doi:10.1042/ns20220054 · Cited by 77 · see citing works
Sawicki, C. M., Kim, J. K., Weber, M. D., Faw, T. D., McKim, D. B., Madalena, K. M., Lerch, J. K., Basso, D. M., Humeidan, M., Godbout, J. P., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2785-18.2018 · Cited by 76 · see citing works
“Much of our previous work has focused on microglia in the brain and their regulation of complex behavioral responses to stress (Reader et al., 2015; Wohleb et al., 2015).”
BackgroundSelf-citationIntegrative neurobiology of metabolic diseases, neuroinflammation, and neurodegeneration
van Dijk, G., van Heijningen, S., Reijne, A. C., Nyakas, C., van der Zee, E. A., & Eisel, U. L. M. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00173 · Cited by 75 · see citing works
“Reader et al used a repeated social defeat (RSD) stress model for induction of chronic psychological/psychosocial stress and observed increased microglial activation, which is a proxy for neuroinflammation (Reader et al., 2015).”
BackgroundExercise and adrenergic regulation of immunity
Simpson, R. J., Boßlau, T. K., Weyh, C., Niemiro, G. M., Batatinha, H., Smith, K. A., & Krüger, K. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.07.010 · Cited by 76 · see citing works
Neuroinflammation disorders exacerbated by environmental stressors
O'Callaghan, J. P., & Miller, D. B. (2019) · Metabolism · doi:10.1016/j.metabol.2019.153951 · Cited by 73 · see citing works
Zhu, Y., Klomparens, E. A., Guo, S., & Geng, X. (2019) · Neurological Research · doi:10.1080/01616412.2019.1615670 · Cited by 71 · see citing works
“Studies have confirmed that stress can increase production, egress, and trafficking of pro-inflammatory immune cells to the spleen, lung, and brain [37].”
BackgroundKuhlman, K. R., Robles, T. F., Dooley, L. N., Boyle, C. C., Haydon, M. D., & Bower, J. E. (2018) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2018.02.001 · Cited by 67 · see citing works
Encore: Behavioural animal models of stress, depression and mood disorders
Petković, A., & Chaudhury, D. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.931964 · Cited by 70 · see citing works
Yin, W., Gallagher, N. R., Sawicki, C. M., McKim, D. B., Godbout, J. P., & Sheridan, J. F. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.01.015 · Cited by 65 · see citing works
Self-citationMicroglial Cells as a Link between Cannabinoids and the Immune Hypothesis of Psychiatric Disorders
Lisboa, S. F. D. S., Gomes, F. V., Guimarães, F. S., & Campos, A. C. (2016) · Frontiers in Neurology · doi:10.3389/fneur.2016.00005 · Cited by 69 · see citing works
“These effects could be due to an inhibitory effect on stress-induced peripheral immune system activation (12).”
BackgroundImmune signaling mechanisms of PTSD risk and symptom development: insights from animal models
Deslauriers, J., Powell, S. B., & Risbrough, V. B. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.01.005 · Cited by 67 · see citing works
Inflammation, stress and depression: An exploration of ketamine’s therapeutic profile
Johnston, J. N., Greenwald, M. S., Henter, I. D., Kraus, C., Mkrtchian, A., Clark, N. G., Park, L. T., Gold, P. W., Zarate, C. A., & Kadriu, B. (2023) · Drug Discovery Today · doi:10.1016/j.drudis.2023.103518 · Cited by 66 · see citing works
Stress primes microglial polarization after global ischemia: Therapeutic potential of progesterone
Espinosa‐García, C., Sayeed, I., Yousuf, S., Atif, F., Sergeeva, E. G., Neigh, G. N., & Stein, D. G. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.06.012 · Cited by 65 · see citing works
Animal models of post-traumatic stress disorder and novel treatment targets
Aspesi, D., & Pinna, G. (2019) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000467 · Cited by 65 · see citing works
Xiao, R., Bergin, S. M., Huang, W., Slater, A. M., Liu, X., Judd, R. T., Lin, E.-J. D., Widstrom, K. J., Scoville, S. D., Yu, J., et al. (2016) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-15-0297 · Cited by 62 · see citing works
IL-4/10 prevents stress vulnerability following imipramine discontinuation
Han, A., Yeo, H.-L., Park, M.-J., Kim, S. H., Choi, H. J., Hong, C.-W., & Kwon, M. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0416-3 · Cited by 59 · see citing works
“Previous study has found that bone marrow-derived monocytes infiltrated into the paraventricular nucleus upon exposure to chronic psychological stress, which may be associated to regional neuronal and microglial activation [50, 51].”
BackgroundJianhua, F., Wei, W., Xiaomei, L., & Wang, S. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.09.011 · Cited by 59 · see citing works
Sociology, biology and mechanisms in urban mental health
Manning, N. (2018) · Social Theory & Health · doi:10.1057/s41285-018-00085-7 · Cited by 63 · see citing works
Applying nanomedicine in maladaptive inflammation and angiogenesis
Alaarg, A., Pérez‐Medina, C., Metselaar, J. M., Nahrendorf, M., Fayad, Z. A., Storm, G., & Mulder, W. J. M. (2017) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2017.05.009 · Cited by 59 · see citing works
Oxidative stress: a potential link between emotional wellbeing and immune response
Salim, S. (2016) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2016.06.006 · Cited by 68 · see citing works
Bekhbat, M., Howell, P. A., Rowson, S. A., Kelly, S. D., Tansey, M. G., & Neigh, G. N. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.12.005 · Cited by 56 · see citing works
Jones, K., Zouikr, I., Patience, M., Clarkson, A. N., Isgaard, J., Johnson, S. J., Spratt, N. J., Nilsson, M., & Walker, F. R. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.02.014 · Cited by 54 · see citing works
The Endocannabinoid System and Anxiety
Lisboa, S. F. D. S., Gomes, F. V., Terzian, A. L. B., de Aguiar, D. C., Moreira, F. A., Resstel, L. B. M., & Guimarães, F. S. (2016) · Vitamins and hormones · doi:10.1016/bs.vh.2016.09.006 · Cited by 56 · see citing works
Multifaceted Regulations of the Serotonin Transporter: Impact on Antidepressant Response
Baudry, A., Pietri, M., Launay, J., Kellermann, O., & Schneider, B. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00091 · Cited by 55 · see citing works
Brás, J. P., de Suduiraut, I. G., Zanoletti, O., Monari, S., Meijer, M., Grosse, J., Barbosa, M. A., Santos, S. G., Sandi, C., & Almeida, M. I. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.10.018 · Cited by 54 · see citing works
van de Wouw, M., Walsh, C. J., Vigano, G. M. D., Lyte, J. M., Boehme, M., Gual‐Grau, A., Crispie, F., Walsh, A. M., Clarke, G. A., Dinan, T. G., et al. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.07.004 · Cited by 57 · see citing works
“Overall, these data indicate that kefir may modulate peripheral immunoregulation, which might have relevance to neuroimmune activation (Reader et al., 2015; Kim et al., 2018).”
Lafuse, W. P., Gearinger, R. L., Fisher, S., Nealer, C., Mackos, A. R., & Bailey, M. T. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601269 · Cited by 50 · see citing works
Alterations of the Innate Immune System in Susceptibility and Resilience After Social Defeat Stress
Ambrée, O., Ruland, C., Scheu, S., Arolt, V., & Alferink, J. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00141 · Cited by 51 · see citing works
“Consecutively, activated microglia release proinflammatory cytokines and neurotoxic factors that negatively affect CNS cell functions and thus trigger anxietyand depression-like behaviors in mice (Reader et al., 2015; Lehmann et al., 2016; Ramirez et al., 2017; Stein et al., 2017).”
BackgroundContributions of monocytes to nervous system disorders
Garré, J. M., & Yang, G. (2018) · Journal of Molecular Medicine · doi:10.1007/s00109-018-1672-3 · Cited by 51 · see citing works
“amines control the trafficking and activation of monocytes [36].”
Bordoni, B., Marelli, F., Morabito, B., & Sacconi, B. (2017) · Monaldi Archives for Chest Disease · doi:10.4081/monaldi.2017.811 · Cited by 50 · see citing works
Oladapo, O. M., Ben‐Azu, B., Ajayi, A. M., Emokpae, O., Eneni, A.-E. O., Omogbiya, I. A., & Iwalewa, E. O. (2020) · Journal of Molecular Neuroscience · doi:10.1007/s12031-020-01664-y · Cited by 50 · see citing works
“Noteworthily, expanded preclinical evidences have shown a strong association between chronic psychosocial stress, dark microglia, and copious release of pro-inflammatory cytokines to reduced hippocampal neurogenesis, a highly plastic brain region that is strongly involved in memory impairment, anxiety, and depression…”
BackgroundResultInfluentialBrain–immune interaction mechanisms: Implications for cognitive dysfunction in psychiatric disorders
Zhao, F., Li, B., Yang, W., Ge, T., & Cui, R. (2022) · Cell Proliferation · doi:10.1111/cpr.13295 · Cited by 47 · see citing works
Tian, L., Hui, C. W., Bisht, K., Tan, Y., Sharma, K. P., Chen, S., Zhang, X., & Tremblay, M. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.01.007 · Cited by 47 · see citing works
Unique maternal immune and functional microbial profiles during prenatal stress
Antonson, A. M., Evans, M. V., Galley, J. D., Chen, H. J., Rajasekera, T. A., Lammers, S. M., Hale, V. L., Bailey, M. T., & Gur, T. (2020) · Scientific Reports · doi:10.1038/s41598-020-77265-x · Cited by 47 · see citing works
Chen, T., Chen, C., Zhang, Z., Zou, Y., Peng, M., & Wang, Y. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.04.004 · Cited by 46 · see citing works
“Cytokines have also been associated with a variety of behavior impairments linked to emotional and anxiety-related behaviors (Reader et al., 2015).”
BackgroundLee, W., Milewski, T., Dwortz, M., Young, R. L., Gaudet, A. D., Fonken, L., Champagne, F., & Curley, J. (2022) · Brain, behavior, and immunity · doi:10.1016/j.bbi.2022.04.015 · Cited by 37 · see citing works
Neuroinflammaging: A Tight Line Between Normal Aging and Age-Related Neurodegenerative Disorders
Soraci, L., Corsonello, A., Paparazzo, E., Montesanto, A., Piacenza, F., Olivieri, F., Gambuzza, M. E., Savedra, E. V., Marino, S., Lattanzio, F., et al. (2024) · Aging and Disease · doi:10.14336/ad.2023.1001 · Cited by 46 · see citing works
Rodríguez‐Arias, M., Montagud‐Romero, S., Carrión, A. M. G., Perez, C. F., Pérez‐Villalba, A., Marco, E. M., López‐Gallardo, M., Viveros, M., & Miñarro, J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0206421 · Cited by 41 · see citing works
Galley, J. D., Mackos, A. R., Varaljay, V. A., & Bailey, M. T. (2017) · Scientific Reports · doi:10.1038/srep45012 · Cited by 37 · see citing works
Untangling PTSD and TBI: Challenges and Strategies in Clinical Care and Research
Hendrickson, R. C., Schindler, A. G., & Pagulayan, K. F. (2018) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-018-0908-5 · Cited by 37 · see citing works
Hasegawa, Y., Ma, M., Sawa, A., Lane, A. P., & Kamiya, A. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02081-y · Cited by 39 · see citing works
Cosma, N. C., Üsekes, B., Otto, L. R., Gerike, S., Heuser, I., Regen, F., & Hellmann‐Regen, J. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.02.009 · Cited by 37 · see citing works
A multispecies approach for understanding neuroimmune mechanisms of stress
Deak, T., Kudinova, A. Y., Lovelock, D. F., Gibb, B. E., & Hennessy, M. B. (2017) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2017.19.1/tdeak · Cited by 33 · see citing works
Liu, Y., Xie, X., Xia, L., Lv, H., Lou, F., Ren, Y., He, Z., & Luo, X.-G. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0994-3 · Cited by 33 · see citing works
“We speculated that the neuroinflammatory alleviation was induced by peripheral immune tolerance preconditioning through the following ways: (a) Monocytes and microglia are considered to share the same origin of the myeloid lineage [37]; thus, immune tolerance pre-treatment induced hypo-responsiveness of monocytes may…”
BackgroundCCR2 monocytes repair cerebrovascular damage caused by chronic social defeat stress
Lehmann, M. L., Samuels, J. D., Kigar, S. L., Poffenberger, C. N., Lotstein, M. L., & Herkenham, M. A. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.01.011 · Cited by 30 · see citing works
Schrepf, A., Kaplan, C. M., Harris, R. E., Williams, D. A., Clauw, D. J., As‐Sanie, S., Till, S., Clemens, J. Q., Rodríguez, L. V., van Bokhoven, A., et al. (2022) · Pain · doi:10.1097/j.pain.0000000000002813 · Cited by 33 · see citing works
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“Brain inflammation, driven by nonneuronal cells such as astrocytes and microglia, has been demonstrated to be associated with several neurological diseases including depression and anxiety [5], with neuropsychiatric pathologies such as mood disorders and psychosis [6], and with neurodegenerative diseases such as Parki…”
BackgroundIngestion of Lactobacillus rhamnosus modulates chronic stress-induced feather pecking in chickens
Mindus, C., van Staaveren, N., Bharwani, A., Fuchs, D., Gostner, J. M., Kjær, J. B., Kunze, W., Mian, M. F., Shoveller, A. K. K., Forsythe, P., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-96615-x · Cited by 31 · see citing works
Reid, B. M., & Georgieff, M. (2023) · Nutrients · doi:10.3390/nu15173798 · Cited by 38 · see citing works
Neuroimmune Mechanisms and Sex/Gender-Dependent Effects in the Pathophysiology of Mental Disorders
Kokkosis, A. G., & Tsirka, S. E. (2020) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.120.266163 · Cited by 28 · see citing works
A cord blood monocyte–derived cell therapy product accelerates brain remyelination
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“cytes do not enter the uninjured, adult mouse brain but may infiltrate the CNS following insult such as brain irradiation (5, 6), chemotherapy or injury (7), demyelinating conditions (8), or chronic stress (9, 10).”
BackgroundInfluentialInsights into psychosis risk from leukocyte microRNA expression
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Oxidation and Inflammation in the Immune and Nervous Systems, a Link Between Aging and Anxiety
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“Monocyte trafficking to the brain is required for increased anxiety-like behaviors after exposure to chronic social defeat stress (Reader et al., 2015; Wohleb, McKim, Shea, et al., 2014; Wohleb, McKim, Sheridan, et al., 2014), and numerous studies have shown increased Iba1 expressing cells (likely…”
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- Authors
- Reader, B. F., Jarrett, B. L., McKim, D. B., Wohleb, E. S., Godbout, J. P., & Sheridan, J. F.
- Affiliations
- The Ohio State University Wexner Medical Center (US)
- Yale University (US)
- Corresponding author
- Sheridan, J.F.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2015-03
- Volume
- 289
- Pages
- 429-442
- ISSN
- 0306-4522 (ISSN-L)
- PMC
- PMC4536813
- OpenAlex
- W2024776501
- Cited by
- 179
- References
- 110
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 13 · 2023: 12 · 2022: 18 · 2021: 20 · 2020: 9 · 2019: 19 · 2018: 20 · 2017: 20 · 2016: 20 · 2015: 12
- FWCI
- 1.92
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01-MH-093473, R01-MH093472)
- NIH/NIDCR (T32-DE014320)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- repeated social defeat stress, anxiety-like behavior, monocyte trafficking, microglial activation, neuroimmune interactions, hypothalamic-pituitary-adrenal axis, sympathetic nervous system, depression, psychosocial stress
- MeSH terms
- Animals, Anxiety, Dominance-Subordination, Humans, Monocytes, Stress, Psychological, Microglia
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.
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