Early life stress perturbs the maturation of microglia in the developing hippocampus
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Children exposed to abuse or neglect show abnormal hippocampal development and similar findings have been reported in rodent models. Using brief daily separation (BDS), a mouse model of early life stress, we previously showed that exposure to BDS impairs hippocampal function in adulthood and perturbs synaptic maturation, synaptic pruning, axonal growth and myelination in the developing hippocampus. Given that microglia are involved in these developmental processes, we tested whether BDS impairs microglial activity in the hippocampus of 14 (during BDS) and 28-day old mice (one week after BDS). We found that BDS increased the density and altered the morphology of microglia in the hippocampus of 14-day old pups, effects that were no longer present on postnatal day (PND) 28. Despite the normal cell number and morphology seen at PND28, the molecular signature of hippocampal microglia, assessed using the NanoString immune panel, was altered at both ages. We showed that during normal hippocampal development, microglia undergo significant changes between PND14 and PND28, including reduced cell density, decreased ex vivo phagocytic activity, and an increase in the expression of genes involved in inflammation and cell migration. However, microglia harvested from the hippocampus of 28-day old BDS mice showed an increase in phagocytic activity and reduced expression of genes that normally increase across development. Promoter analysis indicated that alteration in the transcriptional activity of PU.1, Creb1, Sp1, and RelA accounted for most of the transcriptional changes seen during normal microglia development and for most of the BDS-induced changes at PND14 and PND28. These findings are the first to demonstrate that early life stress dysregulates microglial function in the developing hippocampus and to identify key transcription factors that are likely to mediate these changes.
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In animal models, long-lasting effects of early life stress have been documented.
“In animal models, long-lasting effects of ELS have been documented.202–207”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [205]
Early life stress from maternal separation can induce a pro-inflammatory microglia phenotype in offspring and reduce PU.1 transcriptional activity.
“Early life stress caused by maternal separation can induce pro-inflammatory microglia phenotype in offspring and reduced PU.1 transcriptional activity [64].”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [64]
Early life stress may affect microglia development.
“Other environmental factors such as early life stress may also affect microglia development.”
From Transcriptional and Epigenetic Regulation of Microglia in Health and Disease (2019) · cites this paper as [64]
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A new mathematical model for relative quantification in real-time RT-PCR
Pfaffl, M. W. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.9.e45 · Cited by 34,610 · see citing works
Polazzi, E., Mengoni, I., Caprini, M., Peña‐Altamira, E., Kurtys, E., & Monti, B. (2012) · Neurosignals · doi:10.1159/000337115 · Cited by 9,023 · see citing works
Synaptic Pruning by Microglia Is Necessary for Normal Brain Development
Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T. A., Guiducci, E., Dumas, L., et al. (2011) · Science · doi:10.1126/science.1202529 · Cited by 4,244 · see citing works
Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner
Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., Ransohoff, R. M., Greenberg, M. E., Barres, B. A., & Stevens, B. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.026 · Cited by 4,089 · see citing works
Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor
Parkhurst, C. N., Yang, G., Ninan, I., Savas, J. N., Yates, J. R., Lafaille, J. J., Hempstead, B. L., Littman, D. R., & Gan, W.-B. (2013) · Cell · doi:10.1016/j.cell.2013.11.030 · Cited by 2,599 · see citing works
Identification of a unique TGF-β–dependent molecular and functional signature in microglia
Butovsky, O., Jedrychowski, M. P., Moore, C. S., Cialic, R., Lanser, A. J., Gabriely, G., Koeglsperger, T., Dake, B., Wu, P. M., Doykan, C. E., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3599 · Cited by 2,543 · see citing works
Self-citationM2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination
Miron, V. E., Boyd, A., Zhao, J.-W., Yuen, T. J., Ruckh, J. M., Shadrach, J. L., van Wijngaarden, P., Wagers, A. J., Williams, A., Franklin, R. J. M., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3469 · Cited by 1,788 · see citing works
Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways
Kierdorf, K., Erny, D., Goldmann, T., Sander, V., Schulz, C., Perdiguero, E. G., Wieghofer, P., Heinrich, A., Riemke, P., Hölscher, C., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3318 · Cited by 1,457 · see citing works
Maternal care, hippocampal synaptogenesis and cognitive development in rats
Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000) · Nature Neuroscience · doi:10.1038/77702 · Cited by 1,195 · see citing works
Microglia Regulate the Number of Neural Precursor Cells in the Developing Cerebral Cortex
Cunningham, C. L., Martínez-Cerdeño, V., & Noctor, S. C. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3441-12.2013 · Cited by 976 · see citing works
Butovsky, O., Ziv, Y., Schwartz, A., Landa, G., Talpalar, A. E., Pluchino, S., Martino, G., & Schwartz, M. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.10.006 · Cited by 923 · see citing works
Self-citationThe Role of the Transcription Factor CREB in Immune Function
Wen, A. Y., Sakamoto, K. M., & Miller, L. S. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001829 · Cited by 865 · see citing works
Layer V cortical neurons require microglial support for survival during postnatal development
Ueno, M., Fujita, Y., Tanaka, T., Nakamura, Y., Kikuta, J., Ishii, M., & Yamashita, T. (2013) · Nature Neuroscience · doi:10.1038/nn.3358 · Cited by 781 · see citing works
Hodes, G. E., Pfau, M. L., Leboeuf, M., Golden, S. A., Christoffel, D. J., Bregman, D., Rebusi, N., Heshmati, M., Aleyasin, H., Warren, B. L., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1415191111 · Cited by 692 · see citing works
Paresce, D. M., Ghosh, R. N., & Maxfield, F. R. (1996) · Neuron · doi:10.1016/s0896-6273(00)80187-7 · Cited by 663 · see citing works
Champagne, D. L., Bagot, R. C., van Hasselt, F., Ramakers, G., Meaney, M. J., de Kloet, E. R., Joels, M., & Krugers, H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0526-08.2008 · Cited by 661 · see citing works
Erblich, B., Zhu, L., Etgen, A. M., Dobrenis, K., & Pollard, J. W. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026317 · Cited by 649 · 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
Chugani, H. T., Behen, M. E., Muzik, O., Juhász, C., Nagy, F. T., & Chugani, D. C. (2001) · NeuroImage · doi:10.1006/nimg.2001.0917 · Cited by 577 · see citing works
Wohleb, 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
Physiological and behavioral effects of infantile stimulation
Levine, S., Haltmeyer, G. C., Karas, G. G., & Denenberg, V. H. (1967) · Physiology & Behavior · doi:10.1016/0031-9384(67)90011-x · Cited by 545 · see citing works
Microglia Are Essential to Masculinization of Brain and Behavior
Lenz, K. M., Nugent, B. M., Haliyur, R., & McCarthy, M. M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.1268-12.2013 · Cited by 526 · see citing works
Meaney, M. J., Aitken, D. H., Viau, V., Sharma, S., & Sarrieau, A. (2008) · Neuroendocrinology · doi:10.1159/000125287 · Cited by 457 · see citing works
Childhood maltreatment and inflammatory markers: a systematic review.
Coelho, R., Viola, T. W., Walss‐Bass, C., Brietzke, E., & Grassi‐Oliveira, R. (2014) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.12217 · Cited by 426 · see citing works
Herringa, R. J., Birn, R. M., Ruttle, P. L., Burghy, C. A., Stodola, D. E., Davidson, R. J., & Essex, M. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310766110 · Cited by 426 · see citing works
Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines
Johnson, J. D., Campisi, J., Sharkey, C. M., Kennedy, S. L., Nickerson, M., Greenwood, B. N., & Fleshner, M. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.06.090 · Cited by 424 · see citing works
The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain
Bellavance, M.-A., & Rivest, S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00136 · Cited by 419 · see citing works
Total protein analysis as a reliable loading control for quantitative fluorescent Western blotting
Eaton, S. L., Roche, S. L., Llavero Hurtado, M., Oldknow, K. J., Farquharson, C., Gillingwater, T. H., & Wishart, T. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072457 · Cited by 403 · see citing works
Ivy, A. S., Rex, C. S., Chen, Y., Dubé, C., Maras, P. M., Grigoriadis, D. E., Gall, C. M., Lynch, G., & Baram, T. Z. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1784-10.2010 · Cited by 402 · see citing works
Wakselman, S., Béchade, C., Roumier, A., Bernard, D., Triller, A., & Bessis, A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1006-08.2008 · Cited by 351 · see citing works
PU.1 and C/EBPα/β convert fibroblasts into macrophage-like cells
Feng, R., Desbordes, S. C., Xie, H., Tillo, E. S., Pixley, F., Stanley, E. R., & Graf, T. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711961105 · Cited by 348 · see citing works
Hao, S., Dey, A., Yu, X., & Stranahan, A. M. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.08.023 · Cited by 302 · see citing works
Self-citationWohleb, 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
A Starring Role for Microglia in Brain Sex Differences
Lenz, K. M., & McCarthy, M. M. (2015) · The Neuroscientist · doi:10.1177/1073858414536468 · Cited by 281 · see citing works
Rice, R. A., Spangenberg, E. E., Yamate-Morgan, H., Lee, R. J., Arora, R. P. S., Hernandez, M. X., Tenner, A. J., West, B. L., & Green, K. N. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0336-15.2015 · Cited by 270 · see citing works
Diz-Chaves, Y., Pernía, O., Carrero, P., & García‐Segura, L. M. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-71 · Cited by 233 · see citing works
Up-regulation of Microglial CD11b Expression by Nitric Oxide
Roy, A., Fung, Y. K., Liu, X., & Pahan, K. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m600236200 · Cited by 214 · see citing works
Maheu, F., Dozier, M. E., Guyer, A., Mandell, D., Peloso, E., Poeth, K., Jenness, J., Lau, J. Y. F., Ackerman, J., Pine, D., et al. (2010) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.10.1.34 · Cited by 208 · see citing works
Maternal care influences neuronal survival in the hippocampus of the rat
Bredy, T. W., Grant, R. J., Champagne, D. L., & Meaney, M. J. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.02965.x · Cited by 208 · see citing works
Garofalo, R. P. (2010) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2009.11.019 · Cited by 205 · see citing works
Maternal Stress and Effects of Prenatal Air Pollution on Offspring Mental Health Outcomes in Mice
Bolton, J. L., Huff, N. C., Smith, S. H., Mason, S. N., Foster, W. M., Auten, R. L., & Bilbo, S. D. (2013) · Environmental Health Perspectives · doi:10.1289/ehp.1306560 · Cited by 192 · see citing works
Roque, A., Ochoa‐Zarzosa, A., & Torner, L. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.09.017 · Cited by 190 · see citing works
Pace, T. W. W., Wingenfeld, K., Schmidt, I., Meinlschmidt, G., Hellhammer, D. H., & Heim, C. M. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2011.07.232 · Cited by 184 · see citing works
Diz-Chaves, Y., Astiz, M., Bellini, M. J., & García‐Segura, L. M. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.11.013 · Cited by 178 · see citing works
Reduced hippocampal activity in youth with posttraumatic stress symptoms: an FMRI study.
Carrion, V., Haas, B. W., Garrett, A., Song, S.-Z. J., & Reiss, A. (2010) · Journal of Pediatric Psychology · doi:10.1093/jpepsy/jsp112 · Cited by 169 · see citing works
Modification of the corticosterone response curve as a function of handling in infancy
Hess, J. L., Denenberg, V. H., ZARROW, M. X., & Pfeifer, W. (1969) · Physiology & Behavior · doi:10.1016/0031-9384(69)90023-7 · Cited by 160 · see citing works
Brain macrophages stimulate neurite growth and regeneration by secreting thrombospondin
Chamak, B., Morandi, V., & Mallat, M. (1994) · Journal of Neuroscience Research · doi:10.1002/jnr.490380213 · Cited by 155 · see citing works
Nectin-3 links CRHR1 signaling to stress-induced memory deficits and spine loss
Wang, X., Su, Y., Wagner, K. V., Avrabos, C., Scharf, S. H., Hartmann, J., Wolf, M., Liebl, C., Kühne, C., Wurst, W., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3395 · Cited by 142 · see citing works
The transcription factor PU.1 is critical for viability and function of human brain microglia
Smith, A. M., Gibbons, H. M., Oldfield, R. L., Bergin, P. M., Mee, E. W., Faull, R. L. M., & Dragunow, M. (2013) · Glia · doi:10.1002/glia.22486 · Cited by 141 · see citing works
Garrett, A. S., Carrion, V., Kletter, H., Karchemskiy, A., Weems, C. F., & Reiss, A. (2012) · Depression and Anxiety · doi:10.1002/da.21892 · Cited by 131 · see citing works
Takenouchi, T., Nakai, M., Iwamaru, Y., Sugama, S., Tsukimoto, M., Fujita, M., Wei, J., Sekigawa, A., Sato, M., Kojima, S., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0802577 · Cited by 126 · see citing works
Development of microglia in the postnatal rat hippocampus
Dalmau, I., Finsen, B. R., Zimmer, J., Gonz�lez, B., & Castellano, B. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1998)8:5 · Cited by 124 · see citing works
C/EBPα binds and activates the PU.1 distal enhancer to induce monocyte lineage commitment
Yeamans, C., Wang, D., Paz-Priel, I., Torbett, B. E., Tenen, D. G., & Friedman, A. D. (2007) · Blood · doi:10.1182/blood-2007-03-080291 · Cited by 118 · see citing works
Frank, M. G., Watkins, L. R., & Maier, S. F. (2011) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2011.01.005 · Cited by 116 · see citing works
Postnatal maturation of human GABAA receptors measured with positron emission tomography
Chugani, D. C., Muzik, O., Juhász, C., Janisse, J. J., Ager, J. W., & Chugani, H. T. (2001) · Annals of Neurology · doi:10.1002/ana.1003.abs · Cited by 116 · see citing works
Steward, O., & Falk, P. M. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903140311 · Cited by 114 · see citing works
Effects of early-life stress on cognitive function and hippocampal structure in female rodents.
Loi, M., Mossink, J. C. L., Meerhoff, G. F., Den Blaauwen, J. L., Lucassen, P. J., & Joëls, M. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2015.08.024 · Cited by 109 · see citing works
Poeggel, G., Helmeke, C., Abraham, A., Schwabe, T., Friedrich, P., & Braun, K. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2434663100 · Cited by 107 · see citing works
Helmeke, C. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.8.717 · Cited by 106 · see citing works
Jackowski, A. P., Perera, T. D., Abdallah, C. G., Garrido, G. J., Tang, C. Y., Martínez, J. A. B., Mathew, S. J., Gorman, J. M., Rosenblum, L. A., Smith, E. L., et al. (2011) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2010.11.006 · Cited by 89 · see citing works
Self-citationBilbo, S. D., Newsum, N. J., Sprunger, D. B., Watkins, L. R., Rudy, J. W., & Maier, S. F. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2006.10.005 · Cited by 88 · see citing works
Prenatal stress alters microglial development and distribution in postnatal rat brain
Gómez‐González, B., & Escobar, A. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0590-4 · Cited by 86 · see citing works
Affiliative Behavior Requires Juvenile, But Not Adult Neurogenesis
Wei, L., Meaney, M. J., Duman, R. S., & Kaffman, A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1333-11.2011 · Cited by 83 · see citing works
Self-citationSpinelli, S., Chefer, S. I., Carson, R. E., Jagoda, E. M., Lang, L., Heilig, M. A., Barr, C. S., Suomi, S. J., Higley, J. D., & Stein, E. A. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.12.030 · Cited by 77 · see citing works
McNamee, E. N., Griffin, É. W., Ryan, K. M., Ryan, K. J., Heffernan, S., Harkin, A., & Connor, T. J. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.03.014 · Cited by 74 · see citing works
Wei, L., David, A., Duman, R. S., Anisman, H., & Kaffman, A. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.01.007 · Cited by 72 · see citing works
Self-citationEarly life stress inhibits expression of a novel innate immune pathway in the developing hippocampus
Wei, L., Simen, A., Mane, S., & Kaffman, A. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.239 · Cited by 71 · see citing works
Self-citationNew Frontiers in Animal Research of Psychiatric Illness
Kaffman, A., & Krystal, J. J. (2012) · Methods in Molecular Biology · doi:10.1007/978-1-61779-458-2_1 · Cited by 59 · see citing works
Self-citationStress Granules Modulate SYK to Cause Microglial Cell Dysfunction in Alzheimer's Disease
Ghosh, S., & Geahlen, R. L. (2015) · EBioMedicine · doi:10.1016/j.ebiom.2015.09.053 · Cited by 59 · see citing works
Early-life stress increases the motility of microglia in adulthood
Takatsuru, Y., Nabekura, J., Ishikawa, T., Kohsaka, S., & Koibuchi, N. (2015) · The Journal of Physiological Sciences · doi:10.1007/s12576-015-0361-z · Cited by 55 · see citing works
Stevens, S. L., Shaw, T., Dykhuizen, E. C., et al. (2003) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/01.wcb.0000086957.72078.d4 · Cited by 52 · see citing works
Early-Life Stress Perturbs Key Cellular Programs in the Developing Mouse Hippocampus
Wei, L., Jin, H., Lacher, R. K., Abbott, T. B., Chung, L. M., Colangelo, C. M., & Kaffman, A. (2015) · Developmental Neuroscience · doi:10.1159/000430861 · Cited by 50 · see citing works
Self-citationCorticotropin-Releasing Hormone, Microglia and Mental Disorders
Kritas, S. K., Saggini, A., Cerulli, G. G., Caraffa, A., Antinolfi, P., Pantalone, A., Rosati, M., Tei, M. M., Speziali, A., Saggini, R., et al. (2014) · International Journal of Immunopathology and Pharmacology · doi:10.1177/039463201402700203 · Cited by 45 · see citing works
The Effects of Subcutaneous Injections of Glucocorticoids on Amoeboid Microglia in Postnatal Rats.
Kaur, C., Wu, C., WEN, C. Y., & Ling, E. A. (1994) · Archivum histologicum japonicum · doi:10.1679/aohc.57.449 · Cited by 36 · see citing works
Induction of microglial apoptosis by corticotropin‐releasing hormone
Ock, J., Lee, H., Kim, S., Lee, W., Choi, D., Park, E. J., Kim, S., Kim, I. K., & Suk, K. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03933.x · Cited by 35 · see citing works
Strategies for myelin regeneration: lessons learned from development
Pang, Y., Bhatt, A., & Fan, L. (2014) · Neural Regeneration Research · doi:10.4103/1673-5374.137586 · Cited by 32 · see citing works
Axon Pruning in the Developing Vertebrate Hippocampus
Faulkner, R. L., Low, L. K., & Cheng, H.-J. (2006) · Developmental Neuroscience · doi:10.1159/000096207 · Cited by 28 · see citing works
Intranuclear interactomic inhibition of NF-κB suppresses LPS-induced severe sepsis
Park, S.-D., Cheon, S. Y., Park, T. Y., Shin, B.-Y., Oh, H.-J., Ghosh, S., Koo, B., & Lee, S. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.07.008 · Cited by 24 · see citing works
Wu, C., Chien, H., Chang, C., et al. (2001) · Neuroscience Research · doi:10.1016/s0168-0102(01)00231-0 · Cited by 16 · see citing works
Early Life Stress Inhibits Expression of Ribosomal RNA in the Developing Hippocampus
Wei, L., Jin, H., & Kaffman, A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0115283 · Cited by 11 · see citing works
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Inflammation and the neural diathesis-stress hypothesis of schizophrenia: a reconceptualization
Howes, O. D., & McCutcheon, R. (2017) · Translational Psychiatry · doi:10.1038/tp.2016.278 · Cited by 288 · see citing works
Gut microbiota–brain axis in depression: the role of neuroinflammation
Carlessi, A. S., Borba, L. A., Zugno, A. I., Quevedo, J., & Réus, G. Z. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.14631 · Cited by 243 · see citing works
Yuan, M., Yang, B., Rothschild, G., Mann, J. J., Sanford, L. D., Tang, X., Huang, C., Wang, C., & Zhang, W. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01519-z · Cited by 246 · see citing works
Transcriptional and Epigenetic Regulation of Microglia in Health and Disease
Yeh, H., & Ikezu, T. (2019) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2018.11.004 · Cited by 135 · see citing works
Pinto, B., Morelli, G., Rastogi, M., Savardi, A., Fumagalli, A., Petretto, A., Bartolucci, M., Varea, E., Catelani, T., Contestabile, A., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.09.010 · Cited by 135 · see citing works
Environment matters: microglia function and dysfunction in a changing world
Hanamsagar, R., & Bilbo, S. D. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.10.007 · Cited by 122 · see citing works
Kronman, H., Torres-Berrío, A., Sidoli, S., Issler, O., Godino, A., Ramakrishnan, A., Mews, P., Lardner, C. K., Parise, E. M., Walker, D. M., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00814-8 · Cited by 108 · see citing works
Simon, E., Obst, J., & Gomez-Nicola, D. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2018.01.059 · Cited by 83 · see citing works
Lehtola, S. J., Tuulari, J. J., Scheinin, N. M., Karlsson, L., Parkkola, R., Merisaari, H., Lewis, J. D., Fonov, V. S., Louis Collins, D., Evans, A., et al. (2020) · NeuroImage: Clinical · doi:10.1016/j.nicl.2020.102380 · Cited by 51 · see citing works
Gildawie, K. R., Orso, R., Peterzell, S., Thompson, V., & Brenhouse, H. C. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135381 · Cited by 46 · see citing works
- Authors
- Delpech, J.-C., Wei, L., Hao, J., Yu, X., Madore, C., Butovsky, O., & Kaffman, A.
- Affiliations
- Yale University (US)
- Brigham and Women's Hospital (US)
- Corresponding author
- Kaffman, Arie
- Venue
- Brain Behavior and Immunity
- Publisher
- Elsevier BV
- Published
- 2016-10
- Volume
- 57
- Pages
- 79-93
- ISSN
- 0889-1591 (ISSN-L)
- PMC
- PMC5010940
- OpenAlex
- W2419356453
- Cited by
- 193
- References
- 80
- Citations by year
- 2026: 13 · 2025: 17 · 2024: 22 · 2023: 14 · 2022: 32 · 2021: 22 · 2020: 23 · 2019: 18 · 2018: 19 · 2017: 9 · 2016: 2
- FWCI
- 8.76
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion)
- Oskar-Bordeaux (Universite de Bordeaux) (submittedVersion)
- Funders
- NIMH (R21MH098181, R01MH100078)
- VA National Center for PTSD
- NIH-NINDS (1R01NS088137)
- National Multiple Sclerosis Society (5092A1)
- Nancy Davis Foundation Faculty
- 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
- early life stress, microglia, hippocampus, microglial development, phagocytic activity, transcription factors, PU.1, CREB1, Sp1, RelA, neuroinflammation, synaptic pruning, child abuse, developmental programming
- MeSH terms
- Age Factors, Animals, Hippocampus, Maternal Deprivation, Mice, Inbred BALB C, Stress, Psychological, Microglia, Mice
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