Dynamic microglial alterations underlie stress-induced depressive-like behavior and suppressed neurogenesis
Abstract
The limited success in understanding the pathophysiology of major depression may result from excessive focus on the dysfunctioning of neurons, as compared with other types of brain cells. Therefore, we examined the role of dynamic alterations in microglia activation status in the development of chronic unpredictable stress (CUS)-induced depressive-like condition in rodents. We report that following an initial period (2-3 days) of stress-induced microglial proliferation and activation, some microglia underwent apoptosis, leading to reductions in their numbers within the hippocampus, but not in other brain regions, following 5 weeks of CUS exposure. At that time, microglia displayed reduced expression of activation markers as well as dystrophic morphology. Blockade of the initial stress-induced microglial activation by minocycline or by transgenic interleukin-1 receptor antagonist overexpression rescued the subsequent microglial apoptosis and decline, as well as the CUS-induced depressive-like behavior and suppressed neurogenesis. Similarly, the antidepressant drug imipramine blocked the initial stress-induced microglial activation as well as the CUS-induced microglial decline and depressive-like behavior. Treatment of CUS-exposed mice with either endotoxin, macrophage colony-stimulating factor or granulocyte-macrophage colony-stimulating factor, all of which stimulated hippocampal microglial proliferation, partially or completely reversed the depressive-like behavior and dramatically increased hippocampal neurogenesis, whereas treatment with imipramine or minocycline had minimal or no anti-depressive effects, respectively, in these mice. These findings provide direct causal evidence that disturbances in microglial functioning has an etiological role in chronic stress-induced depression, suggesting that microglia stimulators could serve as fast-acting anti-depressants in some forms of depressive and stress-related conditions.
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?
Stress diminishes adult neurogenesis and impairs hippocampal function, reduces the size and number of astrocytes, and triggers microglial reactivity.
“Stress, on the other hand, which diminishes adult neurogenesis and impairs hippocampal function, has been shown to reduce the size and number of astrocytes (Czéh et al., 2006; Tynan et al., 2013) as well as trigger microglial reactivity (Kreisel et al., 2014; Llorens-Martín et al., 2016).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Kreisel et al., 2014
In mice previously exposed to CUS, LPS decreases forced-swim immobility.
“However, in mice previously exposed to CUS, LPS decreases forced-swim immobility [188].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [188]
Chronic stress alters microglia density, morphology, and function dependent on stress duration and brain region.
“Chronic stress alters microglia density, morphology, and function dependent on stress duration and brain region [188].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [188]
Inhibiting microglia during stress exposure with minocycline attenuated the increase of proinflammatory cytokines normally produced by stress and protected against stress-associated deficits in cognitive memory tasks and depressive-like and anxiety-like behaviors.
“In each case, inhibiting microglia during stress exposure attenuated the increase of proinflammatory cytokines normally produced by stress (Hinwood et al, 2012(Hinwood et al, , 2013;;Kreisel et al, 2014;McKim et al, 2016).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Kreisel et al, 2014
Cites
1 retracted
Kern, S., Skoog, I., Börjesson-Hanson, A., Blennow, K., Zetterberg, H., Östling, S., Kern, J., Gudmundsson, P., Marlow, T., Rosengren, L., et al. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2013.03.011 · Cited by 13 · see citing works
RetractedGapped BLAST and PSI-BLAST: a new generation of protein database search programs
Altschul, S. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.17.3389 · Cited by 73,302 · see citing works
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,240 · see citing works
Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction
Chomczyński, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90021-2 · Cited by 47,092 · see citing works
From inflammation to sickness and depression: when the immune system subjugates the brain
Dantzer, R., O'Connor, J. C., Freund, G. G., Johnson, R. W., & Kelley, K. W. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2297 · Cited by 7,395 · see citing works
A Meta-Analysis of Cytokines in Major Depression
Dowlati, Y., Herrmann, N., Swardfager, W., Liu, H., Sham, L., Reim, E. K., & Lanctôt, K. L. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.09.033 · Cited by 4,729 · see citing works
Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants
Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., et al. (2003) · Science · doi:10.1126/science.1083328 · Cited by 4,321 · see citing works
Kettenmann, H., Hanisch, U.-K., Noda, M., & Verkhratsky, A. (2011) · Physiological Reviews · doi:10.1152/physrev.00011.2010 · Cited by 3,547 · see citing works
Nestler, E. J., Barrot, M., DiLeone, R. J., Eisch, A. J., Gold, S. J., & Monteggia, L. M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00653-0 · Cited by 3,217 · see citing works
Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus
Malberg, J. E., Eisch, A. J., Nestler, E. J., & Duman, R. S. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09104.2000 · Cited by 3,111 · see citing works
Cytokines sing the blues: inflammation and the pathogenesis of depression
Raison, C. L., Capuron, L., & Miller, A. H. (2006) · Trends in Immunology · doi:10.1016/j.it.2005.11.006 · Cited by 3,009 · see citing works
Hammen, C. (2005) · Annual Review of Clinical Psychology · doi:10.1146/annurev.clinpsy.1.102803.143938 · Cited by 2,979 · see citing works
Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis.
Howren, M. B., Lamkin, D. M., & Suls, J. (2009) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3181907c1b · Cited by 2,766 · see citing works
Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A., & Littman, D. R. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.11.4106-4114.2000 · Cited by 2,632 · see citing works
Causal Relationship Between Stressful Life Events and the Onset of Major Depression
Kendler, K. S., Karkowski, L. M., & Prescott, C. A. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.6.837 · Cited by 2,486 · see citing works
Inflammatory Blockade Restores Adult Hippocampal Neurogenesis
Monje, M. L., Toda, H., & Palmer, T. D. (2003) · Science · doi:10.1126/science.1088417 · Cited by 2,426 · see citing works
Belmaker, R. H., & Agam, G. (2008) · New England Journal of Medicine · doi:10.1056/nejmra073096 · Cited by 2,166 · see citing works
Hippocampal atrophy in recurrent major depression
Sheline, Y. I., Wang, P. W., Gado, M. H., Csernansky, J. G., & Vannier, M. W. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.9.3908 · Cited by 1,932 · see citing works
Willner, P. (1997) · Psychopharmacology · doi:10.1007/s002130050456 · Cited by 1,832 · see citing works
Mechanisms of Caspase Activation and Inhibition during Apoptosis
Shi, Y. (2002) · Molecular Cell · doi:10.1016/s1097-2765(02)00482-3 · Cited by 1,824 · see citing works
Stress, Depression, and Neuroplasticity: A Convergence of Mechanisms
Pittenger, C., & Duman, R. S. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301574 · Cited by 1,795 · see citing works
Hippocampal Volume Reduction in Major Depression
Bremner, J. D., Narayan, M., Anderson, E. R., Staib, L. H., Miller, H. L., & Charney, D. S. (2000) · American Journal of Psychiatry · doi:10.1176/ajp.157.1.115 · Cited by 1,670 · see citing works
Raison, C. L., Rutherford, R. E., Woolwine, B. J., Shuo, C., Schettler, P., Drake, D. F., Haroon, E., & Miller, A. H. (2013) · JAMA Psychiatry · doi:10.1001/2013.jamapsychiatry.4 · Cited by 1,617 · see citing works
Inflammation is detrimental for neurogenesis in adult brain
Ekdahl, C. T., Claasen, J.-H., Bonde, S., Kokaia, Z., & Lindvall, O. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2234031100 · Cited by 1,559 · see citing works
Immune modulation of learning, memory, neural plasticity and neurogenesis
Yirmiya, R., & Goshen, I. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.10.015 · Cited by 1,483 · see citing works
Self-citationCytokine-Associated Emotional and Cognitive Disturbances in Humans
Reichenberg, A., Yirmiya, R., Schuld, A., Kraus, T., Haack, M., Morag, A., & Pollmächer, T. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.5.445 · Cited by 1,365 · see citing works
Self-citationZiv, Y., Ron, N., Butovsky, O., Landa, G., Sudai, E., Greenberg, N., Cohen, H., Kipnis, J., & Schwartz, M. (2006) · Nature Neuroscience · doi:10.1038/nn1629 · Cited by 1,209 · see citing works
Adult hippocampal neurogenesis in depression
Sahay, A., & Hen, R. (2007) · Nature Neuroscience · doi:10.1038/nn1969 · Cited by 1,206 · see citing works
The cellular neurobiology of depression
Manji, H. K., Drevets, W. C., & Charney, D. S. (2001) · Nature Medicine · doi:10.1038/87865 · Cited by 1,182 · see citing works
Mood disorders in the medically ill: scientific review and recommendations
Evans, D. L., Charney, D. S., Lewis, L., Golden, R. N., Gorman, J. M., Krishnan, K. R. R., Nemeroff, C. B., Bremner, J. D., Carney, R. M., Coyne, J. C., et al. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.05.001 · Cited by 1,071 · see citing works
The Role of Microglia in the Healthy Brain: Figure 1.
Tremblay, M.-È., Stevens, B., Sierra, A., Wake, H., Bessis, A., & Nimmerjahn, A. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4158-11.2011 · Cited by 992 · see citing works
Adult brain neurogenesis and psychiatry: a novel theory of depression
Jacobs, B. L., van Praag, H., & Gage, F. H. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000712 · Cited by 964 · see citing works
Hannestad, J., DellaGioia, N., & Bloch, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.132 · Cited by 914 · see citing works
Maes, M., Yirmyia, R., Noraberg, J., Brene, S., Hibbeln, J., Perini, G., Kubera, M., Bob, P., Lerer, B., & Maj, M. (2009) · Metabolic Brain Disease · doi:10.1007/s11011-008-9118-1 · Cited by 894 · see citing works
Self-citationSelective Ablation of Proliferating Microglial Cells Exacerbates Ischemic Injury in the Brain
Lalancette-Hébert, M., Gowing, G., Simard, A., Weng, Y. C., & Kriz, J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5360-06.2007 · Cited by 874 · see citing works
IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress
Koo, J. W., & Duman, R. S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708092105 · Cited by 862 · see citing works
Brain inflammation and adult neurogenesis: The dual role of microglia
Ekdahl, C. T., Kokaia, Z., & Lindvall, O. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2008.06.052 · Cited by 801 · see citing works
Steiner, J., Bielau, H., Brisch, R., Danos, P., Ullrich, O., Mawrin, C., Bernstein, H.-G., & Bogerts, B. (2008) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2006.10.013 · Cited by 791 · see citing works
Cotter, D., Mackay, D., Landau, S., Kerwin, R., & Everall, I. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.6.545 · Cited by 766 · see citing works
Goshen, I., Kreisel, T., Ben-Menachem-Zidon, O., Licht, T., Weidenfeld, J., Ben-Hur, T., & Yirmiya, R. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002055 · Cited by 762 · see citing works
Self-citationEvidence for a cytokine model of cognitive function
McAfoose, J., & Baune, B. T. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.10.005 · Cited by 760 · see citing works
Wohleb, E. S., Hanke, M. L., Corona, A. W., Powell, N. D., Stiner, L. M., Bailey, M. T., Nelson, R. J., Godbout, J. P., & Sheridan, J. F. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.0450-11.2011 · Cited by 638 · see citing works
Gliogenesis and Glial Pathology in Depression
Rajkowska, G., & Miguel-Hidalgo, J. J. (2007) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152707780619326 · Cited by 612 · see citing works
Glial Loss in the Prefrontal Cortex Is Sufficient to Induce Depressive-like Behaviors
Banasr, M., & Duman, R. S. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.06.008 · Cited by 606 · see citing works
Endotoxin produces a depressive-like episode in rats
Yirmiya, R. (1996) · Brain Research · doi:10.1016/0006-8993(95)01415-2 · Cited by 604 · see citing works
Self-citationCaspase signalling controls microglia activation and neurotoxicity
Burguillos, M. A., Deierborg, T., Kavanagh, E., Persson, A., Hajji, N., Garcia-Quintanilla, A., Cano, J., Brundin, P., Englund, E., Venero, J. L., et al. (2011) · Nature · doi:10.1038/nature09788 · Cited by 585 · see citing works
Frank, M. G., Baratta, M. V., Sprunger, D. B., Watkins, L. R., & Maier, S. F. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2006.03.005 · Cited by 578 · see citing works
Self-citationTynan, R. J., Naicker, S., Hinwood, M., Nalivaiko, E., Buller, K. M., Pow, D. V., Day, T. A., & Walker, F. R. (2010) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2010.02.001 · Cited by 531 · see citing works
Hinwood, M., Morandini, J., Day, T. A., & Walker, F. R. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr229 · Cited by 420 · see citing works
Interleukin-1 (IL-1): A central regulator of stress responses
Goshen, I., & Yirmiya, R. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.10.001 · Cited by 399 · see citing works
Self-citationNair, A., & Bonneau, R. H. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2005.09.012 · Cited by 392 · see citing works
Tynan, R. J., Weidenhofer, J., Hinwood, M., Cairns, M. J., Day, T. A., & Walker, F. R. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.12.011 · Cited by 382 · see citing works
Thored, P., Heldmann, U., Gomes‐Leal, W., Gisler, R., Darsalia, V., Taneera, J., Nygren, J. M., Jacobsen, S. W., Ekdahl, C. T., Kokaia, Z., et al. (2009) · Glia · doi:10.1002/glia.20810 · Cited by 378 · see citing works
Chronic stress, acute stress, and depressive symptoms
Mcgonagle, K. A., & Kessler, R. C. (1990) · American Journal of Community Psychology · doi:10.1007/bf00931237 · Cited by 365 · see citing works
Hinwood, M., Tynan, R. J., Charnley, J. L., Beynon, S. B., Day, T. A., & Walker, F. R. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs151 · Cited by 325 · see citing works
Evidence for activation of microglia in patients with psychiatric illnesses
Bayer, T. A., Buslei, R., Havas, L., & Falkai, P. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00545-5 · Cited by 323 · see citing works
Colony-stimulating factors as promoters of ameboid microglia
Giulian, D., & Ingeman, J. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-12-04707.1988 · Cited by 323 · see citing works
Warner-Schmidt, J. L., Vanover, K. E., Chen, E. Y., Marshall, J. J., & Greengard, P. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104836108 · Cited by 291 · see citing works
Molecular consequences of activated microglia in the brain: overactivation induces apoptosis
Liu, B., Wang, K., Gao, H.-M., Mandavilli, B., Wang, J.-Y., & Hong, J.-S. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.t01-1-00216.x · Cited by 286 · see citing works
Yirmiya, R. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00226-8 · Cited by 224 · see citing works
Self-citationBoissonneault, V., Filali, M., Lessard, M., Relton, J., Wong, G., & Rivest, S. (2008) · Brain · doi:10.1093/brain/awn331 · Cited by 221 · see citing works
Sugama, S., Fujita, M., Hashimoto, M., & Conti, B. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.02.043 · Cited by 216 · see citing works
Effects of colony stimulating factors on isolated microglia in vitro
Suzumura, A., Sawada, M., Yamamoto, H., & Marunouchi, T. (1990) · Journal of Neuroimmunology · doi:10.1016/0165-5728(90)90094-4 · Cited by 216 · see citing works
Antidepressants inhibit interferon-γ-induced microglial production of IL-6 and nitric oxide
Hashioka, S., Klegeris, A., Monji, A., Kato, T., Sawada, M., McGeer, P. L., & Kanba, S. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.03.022 · Cited by 198 · see citing works
Low-dose endotoxemia and human neuropsychological functions
Krabbe, K. S., Reichenberg, A., Yirmiya, R., Smed, A., Pedersen, B. K., & Bruunsgaard, H. (2005) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2005.04.010 · Cited by 189 · see citing works
Self-citationKohman, R. A., DeYoung, E. K., Bhattacharya, T. K., Peterson, L. N., & Rhodes, J. S. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.10.006 · Cited by 176 · see citing works
Walker, F. R. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.10.002 · Cited by 175 · see citing works
Blandino, 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
Frank, M. G., Wieseler‐Frank, J., Watkins, L. R., & Maier, S. F. (2005) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2005.06.026 · Cited by 164 · see citing works
Self-citationLai, A. Y., & Todd, K. G. (2007) · Glia · doi:10.1002/glia.20610 · Cited by 145 · see citing works
Effects of antidepressants on cytokine production and actions
Castanon, N., Leonard, B. E., Neveu, P. J., & Yirmiya, R. (2002) · Brain Behavior and Immunity · doi:10.1016/s0889-1591(02)00008-9 · Cited by 143 · see citing works
Self-citationKempermann, G., & Neumann, H. (2003) · Science · doi:10.1126/science.1092864 · Cited by 139 · see citing works
Blandino, P., Barnum, C. J., Solomon, L. G., Larish, Y., Lankow, B. S., & Deak, T. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.04.013 · Cited by 137 · see citing works
Bouhy, D., Malgrange, B., Multon, S., Poirrier, A., Scholtes, F., Schoenen, J. E., & Franzen, R. (2006) · The FASEB Journal · doi:10.1096/fj.05-4382fje · Cited by 112 · see citing works
Fields, C., Drye, L., Vaidya, V., & Lyketsos, C. (2012) · The American Journal of Geriatric Psychiatry · doi:10.1097/jgp.0b013e318227f4da · Cited by 96 · see citing works
Chronic psychosocial stress down-regulates central cytokines mRNA
Bartolomucci, A., Palanza, P., Parmigiani, S., Pederzani, T., Merlot, É., Neveu, P. J., & Dantzer, R. (2003) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2003.09.009 · Cited by 94 · see citing works
Plata‐Saláman, C. R., Ilyin, S. E., Turrin, N. P., Gayle, D. A., Flynn, M. C., Bedard, T., Merali, Z., & Anisman, H. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00204-x · Cited by 84 · see citing works
Gallagher, P., Castro, V. M., D, M. F. M., Weilburg, J. B., Murphy, S. N., Gainer, V. S., Churchill, S. E., Kohane, I. S., Iosifescu, D. V., Smoller, J. W., et al. (2012) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2012.11091325 · Cited by 79 · see citing works
Early responses to deep brain stimulation in depression are modulated by anti-inflammatory drugs
Pérez-Caballero, L., Pérez‐Egea, R., Romero‐Grimaldi, C., Puigdemont, D., Molet, J., Caso, J. R., Micó, J. A., Pérez, V., Leza, J. C., & Berrocoso, E. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.63 · Cited by 78 · see citing works
Central IL-1 receptor signaling regulates bone growth and mass
Bajayo, A., Goshen, I., Feldman, S., CSERNUS, V. J., Iverfeldt, K., Shohami, E., Yirmiya, R., & Bab, I. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502562102 · Cited by 78 · see citing works
Self-citationChronic intermittent cold stress sensitizes neuro-immune reactivity in the rat brain
Girotti, M., Donegan, J. J., & Morilak, D. A. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.02.008 · Cited by 71 · see citing works
Bauer, J., Hohagen, F., Gimmel, E., Bruns, F., Lis, S., Krieger, S., Ambach, W., Guthmann, A., Grunze, H., Fritsch-Montero, R., et al. (1995) · Biological Psychiatry · doi:10.1016/0006-3223(95)00374-x · Cited by 68 · see citing works
Acute-phase responses in transgenic mice with CNS overexpression of IL-1 receptor antagonist
Lundkvist, J., Sundgren‐Andersson, A. K., Tingsborg, S., Östlund, P., Engfors, C., Alheim, K., Bartfai, T., Iverfeldt, K., & Schultzberg, M. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.276.3.r644 · Cited by 57 · see citing works
Mormède, C., Castanon, N., Medina, C. F., Moze, E., Lestage, J., Neveu, P. J., & Dantzer, R. (2002) · NeuroImmunoModulation · doi:10.1159/000071477 · Cited by 52 · see citing works
Tanebe, Nishijo, Muraguchi, & Ono, O. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00414.x · Cited by 39 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The chronic mild stress (CMS) model of depression: History, evaluation and usage
Willner, P. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.08.002 · Cited by 959 · see citing works
Depression as a Microglial Disease
Yirmiya, R., Rimmerman, N., & Reshef, R. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.08.001 · Cited by 944 · see citing works
Self-citationCalcia, M., Bonsall, D. R., Bloomfield, P. S., Selvaraj, S., Barichello, T., & Howes, O. D. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4218-9 · Cited by 710 · see citing works
Integrating neuroimmune systems in the neurobiology of depression
Wohleb, E. S., Franklin, T., Iwata, M., & Duman, R. S. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.69 · Cited by 668 · see citing works
Norden, D. M., Trojanowski, P. J., Villanueva, E., Navarro, E., & Godbout, J. P. (2015) · Glia · doi:10.1002/glia.22930 · Cited by 596 · see citing works
Microglia in depression: an overview of microglia in the pathogenesis and treatment of depression
Wang, H., He, Y., Sun, Z., Ren, S., Liu, M., Wang, G., & Yang, J. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02492-0 · Cited by 591 · see citing works
Microglial regional heterogeneity and its role in the brain
Tan, Y.-L., Yuan, Y., & Tian, L. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0609-8 · Cited by 571 · see citing works
Tay, T. L., Savage, J. C., Hui, C. W., Bisht, K., & Tremblay, M. (2017) · The Journal of Physiology · doi:10.1113/jp272134 · Cited by 562 · see citing works
The microbiome: a key regulator of stress and neuroinflammation
Rea, K., Dinan, T. G., & Cryan, J. F. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.03.001 · Cited by 508 · see citing works
Deficient autophagy in microglia impairs synaptic pruning and causes social behavioral defects
Kim, H.-J., Cho, M.-H., Shim, W. H., Kim, J. K., Jeon, E.-Y., Kim, D.-H., & Yoon, S.-Y. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.103 · Cited by 475 · see citing works
Sex differences in depression: Insights from clinical and preclinical studies
Eid, R. S., Gobinath, A. R., & Galea, L. A. M. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.01.006 · Cited by 458 · see citing works
Bidirectional Microglia–Neuron Communication in Health and Disease
Szepesi, Z., Manouchehrian, O., Bachiller, S., & Deierborg, T. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00323 · Cited by 459 · see citing works
Wohleb, E. S., McKim, D. B., Sheridan, J. F., & Godbout, J. P. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00447 · Cited by 420 · see citing works
Microglia Priming with Aging and Stress
Niraula, A., Sheridan, J. F., & Godbout, J. P. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.185 · Cited by 398 · see citing works
Immune and neuroendocrine mechanisms of stress vulnerability and resilience
Ménard, C., Pfau, M. L., Hodes, G. E., & Russo, S. J. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.90 · Cited by 374 · see citing works
NLRP3 inflammasome-driven pathways in depression: clinical and preclinical findings
Kaufmann, F. N., Costa, A. P., Ghisleni, G., Diaz, A. P., Rodrigues, A. L. S., Peluffo, H., & Kaster, M. P. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.03.002 · Cited by 370 · see citing works
McKim, D. B., Weber, M. D., Niraula, A., Sawicki, C. M., Liu, X., Jarrett, B. L., Ramirez-Chan, K., Wang, Y., Roeth, R. M., Sucaldito, A. D., et al. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.64 · Cited by 365 · see citing works
Cao, P., Chen, C., Liu, A., Shan, Q., Zhu, X., Jia, C.-H., Peng, X., Zhang, M., Farzinpour, Z., Zhou, W., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.06.012 · Cited by 346 · see citing works
Nie, X., Kitaoka, S., Tanaka, K., Segi‐Nishida, E., Imoto, Y., Ogawa, A., Nakano, F., Tomohiro, A., Nakayama, K., Taniguchi, M., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.035 · Cited by 318 · see citing works
The role of neuroimmune signaling in alcoholism
Crews, F. T., Lawrimore, C. J., Walter, T. J., & Coleman, L. G. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.01.031 · Cited by 321 · see citing works
Depression's Unholy Trinity: Dysregulated Stress, Immunity, and the Microbiome
Cruz-Pereira, J. S., Rea, K., Nolan, Y. M., O'Leary, O. F., Dinan, T. G., & Cryan, J. F. (2020) · Annual Review of Psychology · doi:10.1146/annurev-psych-122216-011613 · Cited by 320 · see citing works
Microglia, Lifestyle Stress, and Neurodegeneration
Madore, C., Yin, Z., Leibowitz, J. A., & Butovsky, O. (2020) · Immunity · doi:10.1016/j.immuni.2019.12.003 · Cited by 310 · see citing works
Neurobiology of Resilience: Interface Between Mind and Body
Cathomas, F., Murrough, J. W., Nestler, E. J., Han, M.-H., & Russo, S. J. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.04.011 · Cited by 296 · see citing works
IL4-driven microglia modulate stress resilience through BDNF-dependent neurogenesis
Zhang, J., Rong, P., Zhang, L., He, H., Zhou, T., Fan, Y., Mo, L., Zhao, Q., Han, Y., Li, S., et al. (2021) · Science Advances · doi:10.1126/sciadv.abb9888 · Cited by 287 · see citing works
Du Preez, A., Onorato, D., Eiben, I., Musaelyan, K., Egeland, M., Zunszain, P. A., Fernandes, C., Thuret, S., & Pariante, C. M. (2021) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.07.015 · Cited by 285 · see citing works
Microglia in depression: current perspectives
Jia, X., Gao, Z., & Hu, H. (2020) · Science China Life Sciences · doi:10.1007/s11427-020-1815-6 · Cited by 283 · 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
Hippocampal neurogenesis: Learning to remember
Lazarov, O., & Hollands, C. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.12.006 · Cited by 281 · see citing works
Kopschina Feltes, P., Doorduin, J., Klein, H. C., Juárez-Orozco, L. E., Dierckx, R. A., Moriguchi-Jeckel, C. M., & de Vries, E. F. (2017) · Journal of Psychopharmacology · doi:10.1177/0269881117711708 · Cited by 279 · see citing works
Brain microglia in psychiatric disorders
Mondelli, V., Vernon, A. C., Turkheimer, F., Dazzan, P., & Pariante, C. M. (2017) · The Lancet Psychiatry · doi:10.1016/s2215-0366(17)30101-3 · Cited by 262 · see citing works
Microbes, immunity, and behavior: psychoneuroimmunology meets the microbiome
Dinan, T. G., & Cryan, J. F. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.103 · Cited by 246 · see citing works
Hellwig, S., Brioschi, S., Dieni, S., Frings, L., Masuch, A., Blank, T., & Biber, K. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.11.008 · Cited by 252 · see citing works
Microglia: An Interface between the Loss of Neuroplasticity and Depression
Singhal, G., & Baune, B. T. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00270 · Cited by 252 · see citing works
Fractalkine receptor deficiency impairs microglial and neuronal responsiveness to chronic stress
Milior, G., Lecours, C., Samson, L., Bisht, K., Poggini, S., Pagani, F., Deflorio, C., Lauro, C., Alboni, S., Limatola, C., et al. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.07.024 · Cited by 247 · see citing works
Microglial TNF-α Suppresses Cocaine-Induced Plasticity and Behavioral Sensitization
Lewitus, G. M., Konefal, S., Greenhalgh, A. D., Pribiag, H., Augereau, K., & Stellwagen, D. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.030 · Cited by 244 · see citing works
Adult neurogenesis, glia, and the extracellular matrix
Cope, E. C., & Gould, E. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.03.023 · Cited by 236 · see citing works
Paolicelli, R. C., & Ferretti, M. T. (2017) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2017.00009 · Cited by 235 · see citing works
The molecular and cellular mechanisms of depression: a focus on reward circuitry
Fox, M. E., & Lobo, M. K. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0415-3 · Cited by 232 · see citing works
A Narrative Review of Cancer-Related Fatigue (CRF) and Its Possible Pathogenesis
Yang, S., Chu, S., Gao, Y., Ai, Q., Liu, Y., Li, X., & Chen, N. (2019) · Cells · doi:10.3390/cells8070738 · Cited by 237 · see citing works
An astroglial basis of major depressive disorder? An overview
Wang, Q., Jie, W., Liu, J., Yang, J., & Gao, T. (2017) · Glia · doi:10.1002/glia.23143 · Cited by 222 · see citing works
Bollinger, J. L., Burns, C. M. B., & Wellman, C. L. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.10.003 · Cited by 216 · see citing works
Bassett, B., Subramaniyam, S., Yang, F., Varney, S., Pan, H., Carneiro, A. M. D., & Chung, C. Y. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.11.009 · Cited by 217 · see citing works
Microglia Gone Rogue: Impacts on Psychiatric Disorders across the Lifespan
Tay, T. L., Béchade, C., D’Andrea, I., St‐Pierre, M., Henry, M. S., Roumier, A., & Tremblay, M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00421 · Cited by 211 · see citing works
NLRP3 gene knockout blocks NF-κB and MAPK signaling pathway in CUMS-induced depression mouse model
Su, W., Zhang, Y., Chen, Y., Gong, H., Lian, Y., Wei, P., Liu, Y., Wang, Y., You, Z., Feng, S.-J., et al. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.01.018 · Cited by 214 · see citing works
Neuroinflammation in bipolar disorder – A [11C]-(R)-PK11195 positron emission tomography study
Haarman, B. C. M., der Lek, R. F. R., de Groot, J. C., Ruhé, H. G., Klein, H. C., Zandstra, T. E., Burger, H., Schoevers, R. A., de Vries, E. F. J., Drexhage, H. A., et al. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2014.03.016 · Cited by 213 · see citing works
Microglia and CNS Interleukin-1: Beyond Immunological Concepts
Liu, X., & Quan, N. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00008 · Cited by 214 · see citing works
Depression and sterile inflammation: essential role of danger associated molecular patterns
Franklin, T. C., Xu, C., & Duman, R. S. (2018) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.10.025 · Cited by 204 · see citing works
Neuroinflammatory 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
Adult neurogenesis: a substrate for experience-dependent change
Opendak, M., & Gould, E. (2015) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.01.001 · Cited by 200 · see citing works
Khan, A. A., Plana‐Ripoll, O., Antonsen, S., Brandt, J. G., Geels, C., Landecker, H. L., Sullivan, P. F., Pedersen, C. B., & Rzhetsky, A. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000353 · Cited by 199 · see citing works
Suicide and Microglia: Recent Findings and Future Perspectives Based on Human Studies
Suzuki, H., Ohgidani, M., Kuwano, N., Chrétien, F., Lorin de la Grandmaison, G., Onaya, M., Tominaga, I., Setoyama, D., Kang, D., Mimura, M., et al. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00031 · Cited by 198 · see citing works
Zhang, Y., Du, L., Bai, Y., Han, B., He, C., Gong, L., Huang, R., Shen, L., Chao, J., Liu, P., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-018-0285-0 · Cited by 184 · see citing works
Depression as a Glial-Based Synaptic Dysfunction
Rial, D., Lemos, C., Pinheiro, H., Duarte, J. M., Gonçalves, F. Q., Real, J. I., Prediger, R. D., Gonçalves, N., Gomes, C. A., Canas, P. M., et al. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00521 · Cited by 182 · see citing works
Central pathways causing fatigue in neuro-inflammatory and autoimmune illnesses
Morris, G., Berk, M., Walder, K. R., & Maes, M. H. J. (2015) · BMC Medicine · doi:10.1186/s12916-014-0259-2 · Cited by 179 · see citing works
Franklin, T., Wohleb, E. S., Zhang, Y., Fogaça, M. V., Hare, B. D., & Duman, R. S. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.06.034 · Cited by 173 · see citing works
Shemer, A., Scheyltjens, I., Frumer, G. R., Kim, J.-S., Grozovski, J., Ayanaw, S., Dassa, B., Van Hove, H., Chappell-Maor, L., Boura-Halfon, S., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.09.018 · Cited by 175 · see citing works
Haase, J. K., & Brown, E. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.10.002 · Cited by 173 · see citing works
Cheng, Y., Pardo, M., Armini, R. D. S., Martinez, A., Mouhsine, H., Zagury, J.-F., Jope, R. S., & Beurel, E. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.12.012 · Cited by 174 · see citing works
Stress-Induced Depressive Behaviors Require a Functional NLRP3 Inflammasome
Alcocer-Gómez, E., Ulecia-Morón, C., Marín-Aguilar, F., Rybkina, T., Casas-Barquero, N., Ruiz-Cabello, J., Ryffel, B., Apetoh, L., Ghiringhelli, F., Bullón, P., et al. (2016) · Molecular Neurobiology · doi:10.1007/s12035-015-9408-7 · Cited by 172 · see citing works
Zhang, C., Zhang, Y.-P., Li, Y.-Y., Liu, B.-P., Wang, H.-Y., Li, K.-W., Zhao, S., & Song, C. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.07.001 · Cited by 172 · see citing works
Klawonn, A. M., Fritz, M., Castany, S., Pignatelli, M., Canal, C., Similä, F., Tejeda, H. A., Levinsson, J., Jaarola, M., Jakobsson, J., et al. (2021) · Immunity · doi:10.1016/j.immuni.2020.12.016 · Cited by 161 · see citing works
Lucassen, P. J., Oomen, C. A., Naninck, E. F. G., Fitzsimons, C. P., van Dam, A.-M., Czeh, B., & Korosi, A. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021303 · Cited by 166 · see citing works
Kraynak, T. E., Marsland, A. L., Wager, T. D., & Gianaros, P. J. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.013 · Cited by 165 · see citing works
Inflammation Models of Depression in Rodents: Relevance to Psychotropic Drug Discovery
Remus, J. L., & Dantzer, R. (2016) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyw028 · Cited by 166 · see citing works
Neuron–Microglia Interactions in Mental Health Disorders: “For Better, and For Worse”
Wohleb, E. S. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00544 · Cited by 164 · see citing works
Microglia: Neuroimmune-sensors of stress
Frank, M. G., Fonken, L. K., Watkins, L. R., & Maier, S. F. (2019) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2019.01.001 · Cited by 160 · see citing works
Self-citationZhang, J., Xie, X., Tang, M., Zhang, J., Zhang, B., Zhao, Q., Han, Y., Yan, W., Peng, C., & You, Z. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.07.012 · Cited by 150 · see citing works
Toll-like receptor signaling and stages of addiction
Crews, F. T., Walter, T. J., Coleman, L. G., & Vetreno, R. P. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4560-6 · Cited by 159 · see citing works
Microglia in neuronal plasticity: Influence of stress
Delpech, J.-C., Madore, C., Nadjar, A., Joffre, C., Wohleb, E. S., & Layé, S. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.12.034 · Cited by 157 · see citing works
Liu, W., Wang, J., Xie, Z.-M., Xu, N., Zhang, G.-F., Jia, M., Zhou, Z., Hashimoto, K., & Yang, J. (2015) · Psychopharmacology · doi:10.1007/s00213-015-4128-2 · Cited by 154 · see citing works
Ullrich (2018) · doi:10.1038/mp.2017.188 · Cited by 145 · see citing works
Minocycline alters behavior, microglia and the gut microbiome in a trait-anxiety-dependent manner
Schmidtner, A. K., Slattery, D. A., Gläsner, J., Hiergeist, A., Gryksa, K., Malik, V. A., Hellmann-Regen, J., Heuser, I., Baghai, T. C., Gessner, A., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0556-9 · Cited by 153 · see citing works
Microglial dysfunction connects depression and Alzheimer’s disease
Santos, L. E., Beckman, D., & Ferreira, S. T. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.11.011 · Cited by 119 · see citing works
Role of GABAB receptors in learning and memory and neurological disorders
Heaney, C. F., & Kinney, J. W. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.01.007 · Cited by 154 · see citing works
Inflammation and neuronal plasticity: a link between childhood trauma and depression pathogenesis
Cattaneo, A., Macchi, F., Plazzotta, G., Veronica, B., Bocchio-Chiavetto, L., Riva, M. A., & Pariante, C. M. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00040 · Cited by 152 · see citing works
Therapeutic Implications of Brain–Immune Interactions: Treatment in Translation
Miller, A. H., Haroon, E., & Felger, J. C. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.167 · Cited by 152 · see citing works
Huang, C., Wang, P., Xu, X., Zhang, Y., Gong, Y. L., Hu, W., Gao, M., Wu, Y. H., Ling, Y., Zhao, X., et al. (2017) · Glia · doi:10.1002/glia.23241 · Cited by 149 · see citing works
Haapakoski, R., Ebmeier, K. P., Alenius, H., & Kivimäki, M. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.11.012 · Cited by 137 · see citing works
Li, W., Ali, T., Zheng, C., Liu, Z., He, K., Shah, F. A., Ren, Q., Rahman, S. U., Li, N., Yu, Z., et al. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02091-5 · Cited by 147 · see citing works
Zhuang, H., Yao, X., Li, H., Li, Q., Yang, C., Wang, C., Xu, D., Xiao, Y., Gao, Y. J., Gao, J., et al. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.11.018 · Cited by 147 · see citing works
Chronic mild stress paradigm as a rat model of depression: facts, artifacts, and future perspectives
Strekalova, T. V., Liu, Y., Kiselev, D., Khairuddin, S., Chiu, J. L. Y., Lam, J., Chan, Y., Pavlov, D., Proshin, A. T., Lesch, K., et al. (2022) · Psychopharmacology · doi:10.1007/s00213-021-05982-w · Cited by 146 · see citing works
Stress induced microglial activation contributes to depression
Li, B., Yang, W., Ge, T., Wang, Y., & Cui, R. (2022) · Pharmacological Research · doi:10.1016/j.phrs.2022.106145 · Cited by 147 · see citing works
Bortolato, B., F. Carvalho, A., K. Soczynska, J., I. Perini, G., & S. McIntyre, R. (2015) · Current Neuropharmacology · doi:10.2174/1570159x13666150630171433 · Cited by 142 · see citing works
Giovanoli, S., Weber‐Stadlbauer, U., Schedlowski, M., Meyer, U., & Engler, H. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.09.015 · Cited by 139 · see citing works
Microglial depletion alters the brain neuroimmune response to acute binge ethanol withdrawal
Walter, T. J., & Crews, F. T. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0856-z · Cited by 141 · see citing works
Stein, 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
Wang, B., Huang, X., Pan, X., Zhang, T., Hou, C., Su, W., Liu, L.-L., Li, J., & Wang, Y. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.06.019 · Cited by 134 · see citing works
Yin, N., Zhao, Y., Liu, C., Yang, Y., Wang, Z., Yu, W., Zhang, K., Zhang, Z., Liu, J., Zhang, Y., et al. (2022) · Advanced Materials · doi:10.1002/adma.202201322 · Cited by 136 · see citing works
Neuroendocrine Regulation of Brain Cytokines After Psychological Stress
Johnson, J. D., Barnard, D. F., Kulp, A. C., & Mehta, D. M. (2019) · Journal of the Endocrine Society · doi:10.1210/js.2019-00053 · Cited by 135 · see citing works
Zhu, W., Cao, F.-S., Feng, J., Chen, H.-W., Wan, J.-R., Lu, Q., & Wang, J. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2016.11.037 · Cited by 134 · see citing works
Lehmann, M. L., Cooper, H. A., Maric, D., & Herkenham, M. A. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0672-x · Cited by 133 · see citing works
The Immune System and the Role of Inflammation in Perinatal Depression
Leff, P., Mancilla‐Herrera, I., Flores‐Ramos, M., Cruz-Fuentes, C. S., Reyes‐Grajeda, J. P., García-Cuétara, M. D. P., Bugnot-Pérez, M. D., & Pulido-Ascencio, D. E. (2016) · Neuroscience Bulletin · doi:10.1007/s12264-016-0048-3 · Cited by 132 · see citing works
Piirainen, S., Youssef, A. M., Song, C., Kalueff, A. V., Landreth, G. E., Malm, T., & Tian, L. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.046 · Cited by 125 · see citing works
Unfolding the Role of BDNF as a Biomarker for Treatment of Depression
Rana, T., Behl, T., Sehgal, A., Srivastava, P., & BUNGAU, S. G. (2020) · Journal of Molecular Neuroscience · doi:10.1007/s12031-020-01754-x · Cited by 127 · see citing works
Dynamic microglial modulation of spatial learning and social behavior
Torres, L., Danver, J., Ji, K., Miyauchi, J. T., Chen, D., Anderson, M. E., West, B. L., Robinson, J. K., & Tsirka, S. E. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.09.001 · Cited by 126 · see citing works
Hu, P., Lü, Y., Pan, B., & Zhang, W. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231911076 · Cited by 134 · see citing works
Neuroimmunology of Behavioral Comorbidities Associated With Cancer and Cancer Treatments
dos Santos, J. C., & Pyter, L. M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01195 · Cited by 123 · see citing works
The neuroimmune response during stress: A physiological perspective
Haykin, H., & Rolls, A. (2021) · Immunity · doi:10.1016/j.immuni.2021.08.023 · Cited by 128 · see citing works
Wang, H.-T., Huang, F., Hu, Z., Zhang, W., Qiao, X., Huang, Y., Dai, R., Li, F., & Li, C.-Q. (2017) · Neurotoxicity Research · doi:10.1007/s12640-016-9696-3 · Cited by 121 · see citing works
Liu, J., Buisman-Pijlman, F., & Hutchinson, M. R. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00309 · Cited by 119 · see citing works
- Authors
- Kreisel, T., Frank, M. G., Licht, T., Reshef, R., Ben-Menachem-Zidon, O., Baratta, M. V., Maier, S. F., & Yirmiya, R.
- Affiliations
- Hebrew University of Jerusalem (IL)
- University of Colorado Boulder (US)
- Corresponding author
- Yirmiya, R
- Venue
- Molecular Psychiatry
- Published
- 2013-12-17
- Volume
- 19
- Issue
- 6
- Pages
- 699-709
- ISSN
- 1359-4184 (ISSN-L)
- 1476-5578
- OpenAlex
- W2051359369
- Cited by
- 663
- References
- 85
- Citations by year
- 2026: 30 · 2025: 40 · 2024: 48 · 2023: 70 · 2022: 64 · 2021: 73 · 2020: 62 · 2019: 58 · 2018: 53 · 2017: 55 · 2016: 51 · 2015: 43 · 2014: 14 · 2013: 1
- FWCI
- 20.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- microglia, chronic unpredictable mild stress, depression, depression-like behavior, hippocampal neurogenesis, microglial apoptosis, microglial activation, minocycline, interleukin-1 receptor antagonist, imipramine, endotoxin, macrophage colony-stimulating factor, GM-CSF, neuroinflammation
- MeSH terms
- Animals, Behavior, Animal, Brain, Chronic Disease, Depressive Disorder, Hippocampus, Male, Mice, Transgenic, Stress, Psychological, Apoptosis, Microglia, Uncertainty, Cell Proliferation, Mice, Rats, Neurogenesis
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
