Chronic foot‐shock stress potentiates the influx of bone marrow‐derived microglia into hippocampus
Abstract
For several years, a new population of microglia derived from bone marrow has been described in multiple settings such as infection, trauma, and neurodegenerative disease. The aim of this study was to investigate the migration of bone marrow‐derived cells to the brain parenchyma after stress exposure. Stress exposure was performed in mice that had received bone marrow transplantation from GFP mice, allowing identification of blood‐derived elements within the brain. Electric foot‐shock exposure was chosen because of its ability to serve as fundamental and physical stress in mice. Bone marrow‐derived GFP+ cells migrated to the ventral part of the hippocampus and acquired a ramified microglia‐like morphology. Microglia marker Iba1 was expressed by 100% of the ramified cells, whereas ramified cells were negative for the astrocyte marker GFAP. Compared with the case in the control group, ramified cells significantly increased after chronic exposure to stress (5 days). One month after 5 days of stress exposure, ramified cells significantly decreased in ventral hippocampus compared with the group examined immediately after the last stress exposure. We report for the first time the migration of bone marrow‐derived cells to the ventral hippocampus after stress exposure. These cells have the characteristics of microglia. Mechanisms responsible for this migration and their roles in the brain remain to be determined. © 2010 Wiley‐Liss, Inc.
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Chronic stress promotes trafficking of BM-derived monocytes to the brain.
“The first evidence that chronic stress promotes trafficking of BM-derived monocytes was by Brevet et al (2010).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as Brevet et al, 2010
Stress exposure causes trafficking of peripheral monocytes into the brain parenchyma.
“First evidence that stress exposure causes trafficking of peripehral monocytes into the brain parenchyma.”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as [17]
Cites
Simard, A. R., Soulet, D., Gowing, G., Julien, J.-P., & Rivest, S. (2006) · Neuron · doi:10.1016/j.neuron.2006.01.022 · Cited by 1,265 · 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
Chronic pain, chronic stress and depression: Coincidence or consequence?
Blackburn‐Munro, G., & Blackburn‐Munro, R. E. (2001) · Journal of Neuroendocrinology · doi:10.1046/j.0007-1331.2001.00727.x · Cited by 493 · see citing works
Zhang, J., Shi, X., Echeverry, S., Mogil, J. S., Koninck, Y. D., & Rivest, S. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3016-07.2007 · Cited by 421 · see citing works
Nair, A., & Bonneau, R. H. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2005.09.012 · Cited by 392 · see citing works
Simard, A. R., & Rivest, S. (2004) · The FASEB Journal · doi:10.1096/fj.04-1517fje · Cited by 354 · see citing works
Murray, F., Smith, D., & Hutson, P. H. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.01.014 · Cited by 334 · see citing works
Depression, antidepressants, and the shrinking hippocampus
Sapolsky, R. M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.231475998 · Cited by 327 · see citing works
Peripheral and central proinflammatory cytokine response to a severe acute stressor
O'Connor, K. A., Johnson, J. D., Hansen, M. K., Wieseler Frank, J. L., Maksimova, E., Watkins, L. R., & Maier, S. F. (2003) · Brain Research · doi:10.1016/j.brainres.2003.08.006 · Cited by 247 · 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
Conrad, C. D. (2006) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582306289043 · Cited by 211 · see citing works
Djukic, M. (2006) · Brain · doi:10.1093/brain/awl206 · Cited by 186 · see citing works
Hayashi, Y., Yoshida, M., Yamato, M., Ide, T., Wu, Z., Ochi-Shindou, M., Kanki, T., Kang, D., Sunagawa, K., Tsutsui, H., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1957-08.2008 · Cited by 180 · see citing works
From bone marrow to microglia: barriers and avenues
Davoust, N., Vuaillat, C., Androdias, G., & Nataf, S. (2008) · Trends in Immunology · doi:10.1016/j.it.2008.01.010 · Cited by 173 · see citing works
Differential contributions of dorsal vs. ventral hippocampus to auditory trace fear conditioning
Yoon, T., & Otto, T. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.12.006 · Cited by 122 · see citing works
Bechmann, I., Goldmann, J., Kovac, A. D., Kwidzinski, E., Simbürger, E., Naftolin, F. N., Dirnagl, U., Nitsch, R., & Priller, J. (2005) · The FASEB Journal · doi:10.1096/fj.04-2599fje · Cited by 117 · see citing works
Early and Rapid Engraftment of Bone Marrow-Derived Microglia in Scrapie
Priller, J., Prinz, M., Heikenwälder, M. F., Zeller, N., Schwarz, P., Heppner, F. L., & Aguzzi, A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2275-06.2006 · Cited by 89 · see citing works
Age-dependent spatial memory loss can be partially restored by immune activation
Ron-Harel, N., Segev, Y., Lewitus, G. M., Cardon, M., Ziv, Y., Netanely, D., Jacob-Hirsch, J., Amariglio, N., Rechavi, G., Domany, E., et al. (2008) · Rejuvenation Research · doi:10.1089/rej.2008.0755 · Cited by 73 · see citing works
Wu, Y.-P., McMahon, E., Kraine, M. R., Tisch, R., Meyers, A. A., Frelinger, J., Matsushima, G. K., & Suzuki, K. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65058-4 · Cited by 69 · see citing works
Rodrı́guez, M., Alvarez‐Erviti, L., Blesa, F. J., Rodríguez‐Oroz, M., Arina, A., Melero, I., Ramos, L. I., & Obeso, J. A. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2007.07.024 · Cited by 67 · see citing works
Trentani, A., Kuipers, S. D., Meerman, G. J. T., Beekman, J. M., Horst, G. J. T., & den Boer, J. A. (2003) · Neurobiology of Disease · doi:10.1016/j.nbd.2003.08.006 · Cited by 40 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
“Finally, intense stress can induce the infiltration into the brain of bone marrow-derived monocytes which can themselves become microglia-like or alter the functioning of existing microglia [54–56].”
BackgroundMethodCalcia, 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
“…et al. (2011), Yoo et al. (2011),a Diz-Chaves et al. (2012, 2013) Varying unpredictable stress, occlusal disharmony, foot shock ↑ Rat, adult/peripubertal mouse Brevet et al. (2010), Kojo et al. (2010), Giovanoli et al. (2013), Kreisel et al.(2014) Chronic varying unpredictable stress ↓ Rat,…”
BackgroundMethodInfluentialWohleb, E. S., Powell, N. D., Godbout, J. P., & Sheridan, J. F. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1671-13.2013 · Cited by 563 · see citing works
“Moreover, recent findings using chronic footshock indicated that BMderived microglia were present in the hippocampus after stress (Brevet et al., 2010).”
BackgroundImmune 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
“Indeed, previous preclinical studies have shown that psychological stress induces the infiltration of peripheral monocytes into the brain, where they alter behavior and promote microglial reactivity (Brevet et al., 2010; Wohleb et al., 2013; Ataka et al., 2013; Wohleb et al., 2015).”
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
Sex differences in the neuro-immune consequences of stress: Focus on depression and anxiety
Bekhbat, M., & Neigh, G. N. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.02.006 · Cited by 359 · see citing works
“While this particular social defeat paradigm has not been performed in female mice, similar demonstration of increased leukocyte trafficking has been reported in female mice that have been subjected to footshock stress (Brevet et al 2010).”
BackgroundWohleb, E. S., McKim, D. B., Shea, D. T., Powell, N. D., Tarr, A. J., Sheridan, J. F., & Godbout, J. P. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.11.029 · Cited by 300 · see citing works
“infiltrating GFP macrophages were reduced in the brain or spinal cord after 1 month (34,35).”
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
“1-mediated potassium buffering and regulation of neuronal burst firing in the LHb (Cui et al., 2018).”
BackgroundInfluentialRepeated 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
“After day 5 of footshock, there was a significant increase of GFP+ cells (ie, BM-derived cells) in the hippocampus (Brevet et al, 2010).”
BackgroundWohleb, 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
“Previous studies demonstrate that exposure to psychological stress elicited monocyte trafficking to the brain (Brevet et al., 2010; Wohleb et al., 2011, 2013, 2014a,b; Ataka et al., 2013; Sawada et al., 2014).”
BackgroundResultInfluentialBassett, 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
Reader, B. F., Jarrett, B. L., McKim, D. B., Wohleb, E. S., Godbout, J. P., & Sheridan, J. F. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.01.001 · Cited by 179 · 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).”
BackgroundResultInfluentialMoylan, S., Eyre, H. A., Maes, M., Baune, B. T., Jacka, F. N., & Berk, M. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.02.003 · Cited by 155 · see citing works
Wager‐Smith, K., & Markou, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.010 · Cited by 150 · see citing works
“There is even one report of recruitment of bone-marrow derived cells into the hippocampus during stress (Brevet et al. 2010), suggesting that stress may trigger full blown neuroinflammation rather than merely activating brain cytokine signaling.”
BackgroundLehmann, 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
“Thus, degradation of the blood-brain barrier may underlie the observed monocyte infiltration and engraftment in stress studies employing irradiation [9, 11, 59] or busulfan treatment [10].”
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
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
“Stress factors were found to induce microglial activation primarily in the brain hippocampus (Brevet et al. 2010; Kreisel et al. 2014; Tynan et al. 2010).”
BackgroundLiu, J., Buisman-Pijlman, F., & Hutchinson, M. R. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00309 · Cited by 119 · 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
“Following 5 days of foot shock stress, BM-derived monocytes trafficked to the ventral HPC and demonstrated a ramified microglia-like morphological phenotype [70].”
BackgroundPreclinical experimental stress studies: Protocols, assessment and comparison
Bali, A., & Jaggi, A. S. (2014) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.10.017 · Cited by 103 · see citing works
Whole Brain Radiation-Induced Vascular Cognitive Impairment: Mechanisms and Implications
Warrington, J. P., Ashpole, N. M., Csiszár, A., Lee, Y. W., Ungvari, Z. I., & Sonntag, W. E. (2013) · Journal of Vascular Research · doi:10.1159/000354227 · Cited by 98 · see citing works
Sex differences in the stress response in SD rats
Lü, J., Wu, X., Zhu, Q., Li, J., Shi, L., Wu, J., Zhang, Q., Huang, M., & Bao, A. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.02.009 · Cited by 95 · see citing works
Ataka, 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 · see citing works
“We recently reported that chronically repeated footshock stress induced a massive infiltration of bone marrowderived cells into the ventral hippocampus in mice [10].”
BackgroundSelf-citationSawada, A., Niiyama, Y., Ataka, K., Nagaishi, K., Yamakage, M., & Fujimiya, M. (2014) · Pain · doi:10.1016/j.pain.2014.05.031 · Cited by 86 · see citing works
“In the C57BL/6 strain of mice, we previously showed a relationship between the infiltration of BM-derived microglia into the paraventricular nucleus of the hypothalamus and anxiety-like behavior via chronic psychological stress produced by the communication box procedure [5], and the infiltration of BM-derived microgl…”
BackgroundSelf-citationRéus, G. Z., Fernandes, G. C., de Moura, A. B., da Silva, R. H., Darabas, A. C., de Souza, T. G., Abelaira, H. M., Carneiro, C., Wendhausen, D. L., Michels, M., et al. (2017) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2017.08.020 · Cited by 83 · see citing works
“…release chemokine ligand 2 (CCL2) in the blood, which, in turn, can bind to chemokine receptor type 2 (CCR2) in monocytes, cross the BBB, penetrate into the brain areas involved in stress and MDD, and increase the expression of cytokines, such as IL-1β (Brevet et al., 2010; Ménard et al., 2016).”
BackgroundPicard, 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
Sun, N., Hu, H., Wang, F., Li, L., Zhu, W., Shen, Y., Xiu, J., & Xu, Q. (2021) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.11.032 · Cited by 75 · see citing works
Jones, M., Lebonville, C. L., Paniccia, J. E., Balentine, M. E., Reissner, K. J., & Lysle, D. T. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.09.016 · Cited by 74 · see citing works
Herbal Medicine Ninjin'yoeito in the Treatment of Sarcopenia and Frailty
Uto, N. S., Amitani, H., Atobe, Y., Sameshima, Y., Sakaki, M., Rokot, N. T., Ataka, K., Amitani, M. S., & Inui, A. (2018) · Frontiers in Nutrition · doi:10.3389/fnut.2018.00126 · Cited by 67 · see citing works
Self-citationInteractions of neuroimmune signaling and glutamate plasticity in addiction
Gipson, C. D., Rawls, S. M., Scofield, M. D., Siemsen, B. M., Bondy, E. O., & Maher, E. E. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02072-8 · Cited by 67 · see citing works
“One preclinical example of this is a study which found that bone marrow-derived microglia infiltrate the hippocampus of mice following chronic foot-shock stress [45].”
BackgroundInfluentialWhy dyspepsia can occur without organic disease: pathogenesis and management of functional dyspepsia
Miwa, H. (2012) · Journal of Gastroenterology · doi:10.1007/s00535-012-0625-9 · Cited by 55 · see citing works
Inflammatory Pathways in Psychiatric Disorders: the Case of Schizophrenia and Depression
Feng, T., Tripathi, A., & Pillai, A. (2020) · Current Behavioral Neuroscience Reports · doi:10.1007/s40473-020-00207-4 · Cited by 50 · see citing works
Molecular insights into the therapeutic promise of targeting HMGB1 in depression
Rana, T., Behl, T., Mehta, V., Uddin, M. S., & BUNGAU, S. G. (2020) · Pharmacological Reports · doi:10.1007/s43440-020-00163-6 · Cited by 49 · see citing works
Interoception and Inflammation in Psychiatric Disorders
Savitz, J., & Harrison, N. A. (2018) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2017.12.011 · Cited by 126 · see citing works
“sensitization, whereby previously stressed animals show a heightened propensity to maladaptive stress responses to later subthreshold stressors (12,40) (Figure 3).”
Niu, L., Luo, S. S., Xu, Y., Wang, Z., Luo, D., Yang, H., Li, W., He, J., Zhong, X. L., Liu, Z. H., et al. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107301 · Cited by 39 · see citing works
An emerging role for microglia in stress‐effects on memory
Sanguino‐Gómez, J., Buurstede, J. C., Abiega, O., Fitzsimons, C. P., Lucassen, P. J., Eggen, B. J. L., Lesuis, S. L., Meijer, O. C., & Krugers, H. J. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15188 · Cited by 42 · see citing works
“Chronic stress exposure, e.g., potentiates the influx of bone marrow– derived cells by extravasation into the brain parenchyma of the ventral hippocampus and differentiation into microglia (Brevet et al., 2010).”
BackgroundHaematopoietic cells produce BDNF and regulate appetite upon migration to the hypothalamus
Urabe, H., Kojima, H., Chan, L., Terashima, T., Ogawa, N., Katagi, M., Fujino, K., Kumagai, A., Kawai, H., Asakawa, A., et al. (2013) · Nature Communications · doi:10.1038/ncomms2536 · Cited by 41 · see citing works
Self-citationLi, W.-Y., Zhu, Q., Jin, L.-Y., Yang, Y., Xu, X.-Y., & Hu, X.-Y. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.308665 · Cited by 37 · see citing works
“The mRNA level of the target gene was determined using methods described elsewhere (Wang et al., 2008; Brevet et al., 2010).”
MethodZhao, Y., Suo, Y., Yang, Z.-B., Hao, Y., Li, W., Su, Y., Shi, Y., Gao, Y., Song, L., Yin, X., et al. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.10.009 · Cited by 23 · see citing works
Microglial Dysregulation and Suicidality: A Stress-Diathesis Perspective
Baharikhoob, P., & Kolla, N. J. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00781 · Cited by 37 · see citing works
Yagi, T., Asakawa, A., Ueda, H., Miyawaki, S., & Inui, A. (2013) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2013.1418 · Cited by 34 · see citing works
“When repeated doses of strong electric shock were administered to neonatal mice, their hippocampal glial cells became necrotic and this incuded the migration of stem cells from the bone marrow to the hippocampus (60).”
Self-citationBekhbat, M., Mukhara, D., Dozmorov, M. G., Stansfield, J. C., Benusa, S. D., Hyer, M. M., Rowson, S. A., Kelly, S. D., Qin, Z. S., Dupree, J. L., et al. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-00970-2 · Cited by 34 · see citing works
Xiao, X., Zhang, H., Ning, W., Yang, Z. R., Wang, Y., & Zhang, T. (2022) · Experimental Neurology · doi:10.1016/j.expneurol.2022.114060 · Cited by 29 · see citing works
Hu, H., Xue, Y., He, Y., Duan, C., & Sun, N. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02569-w · Cited by 20 · see citing works
Terashima, T., Kojima, H., Urabe, H., Yamakawa, I., Ogawa, N., Kawai, H., Chan, L., & Maegawa, H. (2014) · Journal of Neuroscience Research · doi:10.1002/jnr.23368 · Cited by 23 · see citing works
“For BMT, 8-week-old female nontransgenic littermates (on a C57BL/6 background; WT) or SOD1-tg mice (on a C57BL/6 background) were irradiated (9 Gy) and injected with 4 million BM cells isolated from male WT (nontransgenic littermates on C57BL/6 background), SOD1-tg (on C57BL/6 background), or GFP mice (on C57BL/6 back…”
MethodSelf-citationMicroglia as a Hub for Suicide Neuropathology: Future Investigation and Prevention Targets
de Andrade, E. G., Ibáñez, F. G., & Tremblay, M. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.839396 · Cited by 22 · see citing works
Role of high mobility group box protein 1 in depression: A mechanistic and therapeutic perspective
Wang, S., Guan, Y., Zhu, Y., & Wang, M. (2022) · World Journal of Psychiatry · doi:10.5498/wjp.v12.i6.779 · Cited by 20 · see citing works
Reddaway, J., & Brydges, N. M. (2020) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2020.103567 · Cited by 14 · see citing works
Mawson, E. R., & MORRIS, B. J. (2023) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2023.110773 · Cited by 13 · see citing works
“Stress has been linked with increased microglial activity in numerous brain regions (Calcia et al., 2016), particularly HC (Brevet et al., 2010; Delpech et al., 2016; Espinosa-Oliva et al., 2011), PFC (Bollinger et al., 2020, 2016; Hinwood et al., 2013, 2012; Kopp et al., 2013) and NAc (McGrath and…”
Shen, C., Hassan, T., Presto, P., Payberah, D., Devega, R., Wakefield, S. M., Dunn, D. M., & Neugebauer, V. (2025) · Journal of Nutrition · doi:10.1016/j.tjnut.2025.04.006 · Cited by 8 · see citing works
Zebrafish models: Charting promising platform and illuminating the depths of depression
Yang, B., Han, Y., Yang, Y., Li, Y., & Zhu, X. (2025) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2025.174097 · Cited by 5 · see citing works
Nowak, D. B., Taborda-Bejarano, J. P., Chaure, F. J., Mantsch, J. R., & García‐Keller, C. (2025) · Cells · doi:10.3390/cells14131014 · Cited by 4 · see citing works
“Trafficked monocytes exhibit spatial selectivity, arriving in stress-activated brain structures, including the hippocampus [59].”
Liu, L., Zhao, Z., Lu, L., Liu, J., Wu, X. F., Sun, J., Wei, Y., & Dong, J. (2018) · Traditional Medicine and Modern Medicine · doi:10.1142/s2575900018300035 · Cited by 4 · see citing works
Yirmiya, D., Rimmerman, N., & Reshef, R. (2015) · Cited by 1 · see citing works
Weber, M. D. (2015) · CU Scholar (University of Colorado Boulder)
Yusta, G., Díaz-Peláez, E., & Muriel, C. (2007) · PubMed
Miwa, H. (2017) · Nihon Naika Gakkai Zasshi · doi:10.2169/naika.106.39
Jones, M. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/7rx3-qr60
Immune Mechanisms of Depression
Ménard, C., Pfau, M. L., Hodes, G. E., & Russo, S. J. (2017) · Oxford University Press eBooks · doi:10.1093/med/9780190681425.003.0028
The Role Of Microglia In The Effects of Stress On Learning And Memory
Nazari-Serenjeh, F., Mohsenipour, S., Babaki, Z., & Ghasemzadeh, Z. (2024) · Cell and Tissue Journal · doi:10.61186/jct.15.2.155
The effect of neuroimmune signalling on drug addiction
Chen, Q., Chi, H., Liu, S. J., & Zhou, Y. (2026) · Frontiers in Pharmacology · doi:10.3389/fphar.2026.1830998
“One preclinical study revealed that after prolonged foot shock stress, murine hippocampal bone marrow-derived monocytes infiltrate the brain (Brevet et al., 2010).”
- Authors
- Brevet, M., Kojima, H., Asakawa, A., Atsuchi, K., Ushikai, M., Ataka, K., Inui, A., Kimura, H., Sevestre, H., & Fujimiya, M.
- Affiliations
- Shiga University of Medical Science (JP)
- Kagoshima University (JP)
- Sapporo Medical University (JP)
- Centre Hospitalier Universitaire Amiens-Picardie (FR)
- Corresponding author
- Brevet, Marie
- Venue
- Journal of Neuroscience Research
- Publisher
- Wiley
- Published
- 2010-02-12
- Volume
- 88
- Issue
- 9
- Pages
- 1890-1897
- ISSN
- 0360-4012 (ISSN-L)
- 1097-4547
- OpenAlex
- W2166429487
- Cited by
- 62
- References
- 21
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 1 · 2023: 1 · 2022: 4 · 2021: 6 · 2020: 9 · 2019: 1 · 2018: 3 · 2017: 7 · 2016: 6 · 2015: 6 · 2014: 4 · 2013: 7 · 2012: 1
- FWCI
- 1.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroscience Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- hippocampus, microglial migration, bone marrow transplantation, Iba1, ramified microglia, ventral hippocampus, stress exposure, neuroinflammation
- MeSH terms
- Acute Disease, Animals, Bone Marrow Cells, Calcium-Binding Proteins, Cell Movement, Chronic Disease, Electroshock, Female, Glial Fibrillary Acidic Protein, Hippocampus, Immunohistochemistry, Mice, Inbred C57BL, Mice, Transgenic, Microfilament Proteins, Nerve Tissue Proteins, Random Allocation, Stress, Psychological, Time Factors, Bone Marrow Transplantation, Microglia, Green Fluorescent Proteins, Mice
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 ›
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