Sex differences in microglial colonization of the developing rat brain
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J. Neurochem. (2012) 120 , 948–963. Microglia are the resident immune cells within the brain and their production of immune molecules such as cytokines and chemokines is critical for the processes of normal brain development including neurogenesis, axonal migration, synapse formation, and programmed cell death. Notably, sex differences exist in many of these processes throughout brain development; however, it is unknown whether a sex difference concurrently exists in the colonization, number, or morphology of microglia within the developing brain. We demonstrate for the first time that the number and morphology of microglia throughout development is dependent upon the sex and age of the individual, as well as the brain region of interest. Males have overall more microglia early in postnatal development [postnatal day (P) 4], whereas females have more microglia with an activated/amoeboid morphology later in development, as juveniles and adults (P30–60). Finally, gene expression of a large number of cytokines, chemokines and their receptors shifts dramatically over development, and is highly dependent upon sex. Taken together, these data warrant further research into the role that sex‐dependent mechanisms may play in microglial colonization, number, and function, and their potential contribution to neural development, function, or potential dysfunction.
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Microglia are highly affected by sex hormones.
“Microglia, which are the resident innate immune cells of the CNS, are highly affected by sex hormones [14, 16–20].”
From Sex chromosomes and sex hormones differently shape microglial properties during normal physiological conditions in the adult mouse hippocampus (2025) · cites this paper as [17]
The Discussion reports substantial sex differences in microglial number and morphology in developing rats and proposes that early differences may be induced by sex hormones. It also says the hormonal mechanism is unclear, so it does not establish the claim that microglia are highly affected by sex hormones. Page numbers are unavailable in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredAnimal work indicates that males possess more microglia early in life, whereas females have more primed or activated microglia in adolescence and adulthood.
“Early exploration of these pathways in preclinical models suggests that males have more microglia in early life and females have more activated or primed microglia during adolescence and adulthood (Schwarz et al., 2012).”
From The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. (2018) · cites this paper as Schwarz et al., 2012
Gene expression profiles for many cytokines and chemokines are sex-dependent.
“Further, gene expression profiles for a large number of cytokines and chemokines are sex-dependent (Schwarz et al., 2012).”
From The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. (2018) · cites this paper as Schwarz et al., 2012
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Cites
Fate Mapping Analysis Reveals That Adult Microglia Derive from Primitive Macrophages
Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., Mehler, M. F., Conway, S. J., Ng, L. G., Stanley, E. R., et al. (2010) · Science · doi:10.1126/science.1194637 · Cited by 5,175 · see citing works
Microglia: a sensor for pathological events in the CNS
Kreutzberg, G. W. (1996) · Trends in Neurosciences · doi:10.1016/0166-2236(96)10049-7 · Cited by 4,396 · see citing works
The Classical Complement Cascade Mediates CNS Synapse Elimination
Stevens, B., Allen, N. J., Vazquez, L. E., Howell, G. R., Christopherson, K. S., Nouri, N., Micheva, K. D., Mehalow, A. K., Huberman, A. D., Stafford, B., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.036 · Cited by 3,313 · see citing works
Microglial physiology: unique stimuli, specialized responses
Ransohoff, R. M., & Perry, V. H. (2009) · Annual Review of Immunology · doi:10.1146/annurev.immunol.021908.132528 · Cited by 1,858 · see citing works
Pubertal hormones organize the adolescent brain and behavior
Sisk, C. L., & Zehr, J. L. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.10.003 · Cited by 1,082 · see citing works
Deverman, B. E., & Patterson, P. H. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.002 · Cited by 865 · see citing works
Immune proteins in brain development and synaptic plasticity
Boulanger, L. M. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.001 · Cited by 555 · see citing works
Principles and Practices of Unbiased Stereology: An Introduction for Bioscientists
Mouton, P. R. (2002) · Cited by 404 · see citing works
Nishiyori, A., Minami, M., Ohtani, Y., Takami, S., Yamamoto, J., Kawaguchi, N., Kume, T., Akaike, A., & Satoh, M. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00583-3 · Cited by 367 · see citing works
The origin and differentiation of microglial cells during development
Cuadros, M. Á. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00035-5 · Cited by 305 · see citing works
Neuroinflammation and microglia: considerations and approaches for neurotoxicity assessment
Harry, G. J., & Kraft, A. D. (2008) · Expert Opinion on Drug Metabolism & Toxicology · doi:10.1517/17425255.4.10.1265 · Cited by 292 · see citing works
Microglia and Memory: Modulation by Early-Life Infection
Williamson, L. L., Sholar, P. W., Mistry, R. S., Smith, S. H., & Bilbo, S. D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3688-11.2011 · Cited by 274 · see citing works
Self-citationBaker, A. E., Brautigam, V. M., & Watters, J. J. (2004) · Endocrinology · doi:10.1210/en.2004-0619 · Cited by 227 · see citing works
Mong, J. A., Glaser, E. M., & McCarthy, M. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-04-01464.1999 · Cited by 226 · see citing works
Sex Differences in the Brain, Behavior, and Neuropsychiatric Disorders
Bao, A., & Swaab, D. F. (2010) · The Neuroscientist · doi:10.1177/1073858410377005 · Cited by 225 · see citing works
Neonatal Infection Induces Memory Impairments Following an Immune Challenge in Adulthood.
Bilbo, S. D., Levkoff, L. H., Mahoney, J. H., Watkins, L. R., Rudy, J. W., & Maier, S. F. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.1.293 · Cited by 222 · see citing works
Self-citationMicroglia and cell death in the developing mouse cerebellum
Ashwell, K. W. S. (1990) · Developmental Brain Research · doi:10.1016/0165-3806(90)90203-b · Cited by 219 · see citing works
Garay, P. (2010) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2010.00136 · Cited by 217 · see citing works
Deletion of Bax eliminates sex differences in the mouse forebrain
Forger, N. G., Rosen, G. J., Waters, E. M., Jacob, D. A., Simerly, R. B., & Vries, G. J. D. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404644101 · Cited by 216 · see citing works
Female sex steroids: effects upon microglial cell activation
Drew, P. D., & Chavis, J. A. (2000) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(00)00386-6 · Cited by 209 · see citing works
The distribution of microglia and cell death in the fetal rat forebrain
Ashwell, K. W. S. (1991) · Developmental Brain Research · doi:10.1016/0165-3806(91)90231-7 · Cited by 200 · see citing works
Sex differences in the inflammatory response of primary astrocytes to lipopolysaccharide
Santos‐Galindo, M., Acaz‐Fonseca, E., Bellini, M. J., & García‐Segura, L. M. (2011) · Biology of Sex Differences · doi:10.1186/2042-6410-2-7 · Cited by 190 · 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
Minireview: Sex Chromosomes and Brain Sexual Differentiation
Arnold, A. P., Xu, J., Grisham, W., Chen, X., Kim, Y., & Itoh, Y. (2003) · Endocrinology · doi:10.1210/en.2003-1491 · Cited by 164 · see citing works
Cell death and sexual differentiation of the nervous system
Forger, N. G. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.006 · Cited by 153 · see citing works
Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster
Zehr, J. L., Todd, B. J., Schulz, K. M., McCarthy, M. M., & Sisk, C. L. (2006) · Journal of Neurobiology · doi:10.1002/neu.20251 · Cited by 145 · see citing works
Soucy, G., Boivin, G., Labrie, F., & Rivest, S. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.10.6391 · Cited by 138 · see citing works
Steroid‐induced sexual differentiation of the developing brain: multiple pathways, one goal
Schwarz, J. M., & McCarthy, M. M. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05384.x · Cited by 136 · see citing works
Self-citationKrebs-Kraft, D. L., Hill, M. N., Hillard, C. J., & McCarthy, M. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005003107 · Cited by 130 · see citing works
A Lifespan Approach to Neuroinflammatory and Cognitive Disorders: A Critical Role for Glia
Bilbo, S. D., Smith, S. H., & Schwarz, J. M. (2011) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-011-9299-y · Cited by 127 · see citing works
Self-citationRezaie, P., Trillo‐Pazos, G., Everall, I., & Male, D. K. (2001) · Glia · doi:10.1002/glia.1128 · Cited by 120 · see citing works
Viewing chemokines as a third major system of communication in the brain
Adler, M. W., Geller, E. B., Chen, X., & Rogers, T. J. (2005) · The AAPS Journal · doi:10.1208/aapsj070484 · Cited by 117 · see citing works
Sex differences and laterality in astrocyte number and complexity in the adult rat medial amygdala
Johnson, R. T., Breedlove, S. M., & Jordan, C. L. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21859 · Cited by 114 · see citing works
Astrocytes modulate the chemokine network in a pathogen-specific manner
McKimmie, C. S., & Graham, G. J. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.03.111 · Cited by 108 · see citing works
A behavioural characterization of neonatal infection-facilitated memory impairment in adult rats
Bilbo, S. D., Rudy, J. W., Watkins, L. R., & Maier, S. F. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.12.002 · Cited by 106 · see citing works
Self-citationBilbo, S. D., Barrientos, R. M., Eads, A. S., Northcutt, A. L., Watkins, L. R., Rudy, J. W., & Maier, S. F. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.10.003 · Cited by 104 · see citing works
Self-citationLlorente, R., López‐Gallardo, M., Llorente‐Berzal, A., Prada, C., García‐Segura, L. M., & Viveros, M. (2009) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2009.01.002 · Cited by 101 · see citing works
Balancing function vs. self defense: The CNS as an active regulator of immune responses
Carson, M. J., & Sutcliffe, J. G. (1999) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19990101)55:1 · Cited by 99 · see citing works
Wu, C., Wen, C. Y., Shieh, J., & Ling, E. (1992) · Europe PMC (PubMed Central) · Cited by 94 · 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
Arias, C., Zepeda, A., Hernández‐Ortega, K., Leal‐Galicia, P., Lojero, C., & Camacho‐Arroyo, I. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.10.016 · Cited by 83 · see citing works
Kipp, M., Karakaya, S., Johann, S., Kampmann, E., Mey, J., & Beyer, C. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2007.01588.x · Cited by 83 · see citing works
A novel model for prenatal brain damage
Nuñez, J. L., Alt, J., & McCarthy, M. M. (2003) · Experimental Neurology · doi:10.1016/s0014-4886(03)00051-7 · Cited by 75 · see citing works
Sex differences in response to kainic acid and estradiol in the hippocampus of newborn rats
Hilton, G. D., Nu�ez, J. L., & McCarthy, M. M. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00716-9 · Cited by 56 · see citing works
Developmental changes in the expression of chemokine receptor CCR1 in the rat cerebellum
Cowell, R. M., & Silverstein, F. S. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10554 · Cited by 44 · see citing works
Xu, J., Kaur, C., & Ling, E. A. (1993) · PubMed · Cited by 40 · see citing works
Hahn, Y. K., Vo, P., Fitting, S., Block, M. L., Hauser, K. F., & Knapp, P. E. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06744.x · Cited by 40 · see citing works
Wu, C., Wen, C. Y., Shieh, J., & Ling, E. A. (1993) · PubMed · Cited by 39 · see citing works
Cowell, R. M., Xu, H., Parent, J. M., & Silverstein, F. S. (2006) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2006.01.005 · Cited by 38 · see citing works
Neonatal bacterial infection alters fever to live and simulated infections in adulthood
Bilbo, S. D., Wieseler, J. L., Barrientos, R. M., Tsang, V., Watkins, L. R., & Maier, S. F. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.07.014 · Cited by 33 · see citing works
Self-citationPotentiation of tumor metastasis in adulthood by neonatal endotoxin exposure: sex differences
Hodgson, D. M., & Knott, B. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00080-4 · Cited by 28 · see citing works
Sex Steroid Regulation of Microglial Cell Activation: Relevance to Multiple Sclerosis
DREW, P. D., CHAVIS, J. A., & BHATT, R. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1286.031 · Cited by 25 · see citing works
Microglial distribution and apoptosis in fetal rat brain
Wang, C.-C., Wu, C., Shieh, J.-Y., & Wen, C.-Y. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00584-9 · Cited by 23 · see citing works
Early life infection alters adult BALB/c hippocampal gene expression in a sex specific manner
Wynne, O., Horvat, J. C., Osei-Kumah, A., Smith, R., Hansbro, P. M., Clifton, V. L., & Hodgson, D. M. (2011) · Stress · doi:10.3109/10253890.2010.532576 · Cited by 19 · see citing works
Reyna‐Neyra, A., Arias, C., Ferrera, P., Morimoto, S., & Camacho‐Arroyo, I. (2004) · Journal of Neurobiology · doi:10.1002/neu.20042 · Cited by 15 · see citing works
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Semple, B. D., Blomgren, K., Gimlin, K., Ferriero, D. M., & Noble-Haeusslein, L. J. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.04.001 · Cited by 2,132 · see citing works
Microglia emerge as central players in brain disease
Salter, M. W., & Stevens, B. (2017) · Nature Medicine · doi:10.1038/nm.4397 · Cited by 1,767 · see citing works
Microbiome Influences Prenatal and Adult Microglia in a Sex-Specific Manner
Thion, M. S., Low, D., Silvin, A., Chen, J., Grisel, P., Schulte-Schrepping, J., Blecher, R., Ulas, T., Squarzoni, P., Hoeffel, G., et al. (2018) · Cell · doi:10.1016/j.cell.2017.11.042 · Cited by 779 · see citing works
Microglia Heterogeneity in the Single-Cell Era
Masuda, T., Sankowski, R., Staszewski, O., & Prinz, M. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.01.010 · Cited by 784 · 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 Indispensable Roles of Microglia and Astrocytes during Brain Development
Reemst, K., Noctor, S. C., Lucassen, P. J., & Hol, E. M. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00566 · Cited by 516 · 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
Microbiome–microglia connections via the gut–brain axis
Abdel-Haq, R., Schlachetzki, J. C. M., Glass, C. K., & Mazmanian, S. K. (2019) · Journal of Experimental Medicine · doi:10.1084/jem.20180794 · Cited by 471 · see citing works
“These trends might help to explain the inherent functional differences in microglia from intact male versus female mice, as well as the sex variations in incidence rates of several neurological disorders (Schwarz et al., 2012; Hanamsagar et al., 2015).”
BackgroundTranscriptional and Translational Differences of Microglia from Male and Female Brains
Guneykaya, D., Ivanov, A., Hernandez, D. P., Haage, V., Wojtas, B., Meyer, N., Maricos, M., Jordan, P., Buonfiglioli, A., Gielniewski, B., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.08.001 · Cited by 477 · see citing works
Estrogens, Neuroinflammation, and Neurodegeneration
Villa, A., Vegeto, E., Poletti, A., & Maggi, A. (2016) · Endocrine Reviews · doi:10.1210/er.2016-1007 · Cited by 423 · see citing works
Layé, S., Nadjar, A., Joffre, C., & Bazinet, R. P. (2018) · Pharmacological Reviews · doi:10.1124/pr.117.014092 · Cited by 420 · 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
Hanamsagar, R., Alter, M. D., Block, C. S., Sullivan, H., Bolton, J. L., & Bilbo, S. D. (2017) · Glia · doi:10.1002/glia.23176 · Cited by 384 · see citing works
Microglia Function in Central Nervous System Development and Plasticity
Schafer, D. P., & Stevens, B. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020545 · Cited by 353 · see citing works
The role of maternal obesity in the risk of neuropsychiatric disorders
Rivera, H. M., Christiansen, K. J., & Sullivan, E. L. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00194 · Cited by 307 · see citing works
VanRyzin, J. W., Marquardt, A. E., Argue, K. J., Vecchiarelli, H. A., Ashton, S. E., Arambula, S. E., Hill, M. N., & McCarthy, M. M. (2019) · Neuron · doi:10.1016/j.neuron.2019.02.006 · Cited by 272 · see citing works
Sex, glia, and development: Interactions in health and disease
Schwarz, J. M., & Bilbo, S. D. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.02.018 · Cited by 247 · see citing works
Self-citationAllen, J. L., Oberdorster, G., Morris-Schaffer, K., Wong, C., Klocke, C., Sobolewski, M., Conrad, K., Mayer-Proschel, M., & Cory-Slechta, D. A. (2017) · NeuroToxicology · doi:10.1016/j.neuro.2015.12.014 · Cited by 241 · see citing works
The role of sex-differential biology in risk for autism spectrum disorder
Werling, D. M. (2016) · Biology of Sex Differences · doi:10.1186/s13293-016-0112-8 · Cited by 208 · see citing works
Uncovering sex differences of rodent microglia
Han, J., Fan, Y., Zhou, K., Blomgren, K., & Harris, R. A. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02124-z · Cited by 224 · 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
Nikodemova, M., Kimyon, R. S., De, I., Small, A. L., Collier, L. S., & Watters, J. J. (2015) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2014.11.018 · Cited by 192 · see citing works
“Decreased Cd200 expression in the adult CNS is in linewith previous reports (Schwarz et al., 2012).”
BackgroundResultInfluentialEffects of Microglia on Neurogenesis
Sato, K. (2015) · Glia · doi:10.1002/glia.22858 · Cited by 187 · see citing works
Dooley, L. N., Kuhlman, K. R., Robles, T. F., Eisenberger, N. I., Craske, M. G., & Bower, J. E. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.006 · Cited by 176 · see citing works
Kang, S. S., Kurti, A., Fair, D. A., & Fryer, J. D. (2014) · Journal of Neuroinflammation · doi:10.1186/s12974-014-0156-9 · Cited by 167 · see citing works
Exploring Sex-Related Differences in Microglia May Be a Game-Changer in Precision Medicine
Lynch, M. A. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.868448 · Cited by 146 · see citing works
Brain macrophage development, diversity and dysregulation in health and disease
Silvin, A., Qian, J., & Ginhoux, F. (2023) · Cellular & Molecular Immunology · doi:10.1038/s41423-023-01053-6 · Cited by 137 · 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
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
Self-citationMicroglia in Aging and Alzheimer’s Disease: A Comparative Species Review
Edler, M. K., Mhatre-Winters, I., & Richardson, J. R. (2021) · Cells · doi:10.3390/cells10051138 · Cited by 126 · see citing works
APOE genotype and sex affect microglial interactions with plaques in Alzheimer’s disease mice
Stephen, T. L., Cacciottolo, M., Balu, D., Morgan, T. E., LaDu, M. J., Finch, C. E., & Pike, C. J. (2019) · Acta Neuropathologica Communications · doi:10.1186/s40478-019-0729-z · Cited by 115 · see citing works
Sexual dimorphism of microglia and synapses during mouse postnatal development
Weinhard, L., Neniskyte, U., Vadisiute, A., di Bartolomei, G., Aygün, N., Riviere, L., Zonfrillo, F., Dymecki, S., & Gross, C. (2018) · Developmental Neurobiology · doi:10.1002/dneu.22568 · Cited by 107 · see citing works
Inflammation within the neurovascular unit: Focus on microglia for stroke injury and recovery
Eldahshan, W., Fagan, S. C., & Ergul, A. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104349 · Cited by 104 · see citing works
Colombo, G., Cubero, R. J. A., Kanari, L., Venturino, A., Schulz, R., Scolamiero, M., Agerberg, J., Mathys, H., Tsai, L.-H., Chachólski, W., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01167-6 · Cited by 100 · see citing works
The microbiota–microglia axis in central nervous system disorders
Mossad, O., & Erny, D. (2020) · Brain Pathology · doi:10.1111/bpa.12908 · Cited by 98 · see citing works
The microbiota influences cell death and microglial colonization in the perinatal mouse brain
Castillo-Ruiz, A., Mosley, M., George, A. J., Mussaji, L. F., Fullerton, E. F., Ruszkowski, E. M., Jacobs, A. J., Gewirtz, A. T., Chassaing, B., & Forger, N. G. (2018) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.08.027 · Cited by 91 · see citing works
Wellman, C. L., Bangasser, D. A., Bollinger, J. L., Coutellier, L., Logrip, M. L., Moench, K. M., & Urban, K. R. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1673-18.2018 · Cited by 88 · see citing works
Hoeijmakers, L., Heinen, Y., van Dam, A.-M., Lucassen, P. J., & Korosi, A. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00398 · Cited by 85 · see citing works
Tiwari, A., & Gonzalez, A. (2018) · Clinical Psychology Review · doi:10.1016/j.cpr.2018.01.006 · Cited by 71 · see citing works
Age of trauma onset and HPA axis dysregulation among trauma-exposed youth
Kuhlman, K. R., Vargas, I., Geiss, E. G., & Lopez‐Duran, N. L. (2015) · Journal of Traumatic Stress · doi:10.1002/jts.22054 · Cited by 75 · see citing works
Vogel Ciernia, A., Careaga, M., LaSalle, J. M., & Ashwood, P. (2018) · Glia · doi:10.1002/glia.23261 · Cited by 69 · see citing works
Makinson, R., Lloyd, K., Rayasam, A., McKee, S., Brown, A., Barila, G., Grissom, N., George, R., Marini, M., Fabry, Z., et al. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.07.016 · Cited by 67 · see citing works
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Activation of neonatal microglia can be influenced by other neural cells
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Self-citationAltered Metabolism and DAM-signatures in Female Brains and Microglia with Aging
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“In contrast, Schwarz and Acaz-Fonseca et al. reported that the mice or rats were in the estrous phase [17, 102].”
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Self-citationConstitutive expression of CX3CR1-BAC-Cre introduces minimal off-target effects in microglia
Mroue-Ruiz, F. H., Desai, B., Garvin, M. M., Shehu, J. H., Kamau, F., Kar, U., & Bolton, J. L. (2026) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2026.153657 · Cited by 3 · see citing works
- Authors
- Schwarz, J. M., Sholar, P. W., & Bilbo, S. D.
- Affiliations
- Duke University (US)
- Venue
- Journal of Neurochemistry
- Publisher
- Wiley
- Published
- 2012-02-09
- Volume
- 120
- Issue
- 6
- Pages
- 948-963
- ISSN
- 0022-3042 (ISSN-L)
- 1471-4159
- PMC
- PMC3296888
- OpenAlex
- W1576427485
- Cited by
- 672
- References
- 55
- Citations by year
- 2026: 29 · 2025: 54 · 2024: 60 · 2023: 62 · 2022: 68 · 2021: 62 · 2020: 58 · 2019: 66 · 2018: 70 · 2017: 45 · 2016: 34 · 2015: 24 · 2014: 25 · 2013: 9 · 2012: 6
- FWCI
- 7.07
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Journal of Neurochemistry (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH083698)
- National Institute on Drug Abuse (R01DA025978, F32DA030136)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Keywords
- microglia, sex differences, brain development, microglial morphology, amoeboid microglia, cytokines, chemokines, cytokine receptors, postnatal development, rat brain
- MeSH terms
- Age Factors, Animals, Animals, Newborn, Brain, Calcium-Binding Proteins, Cell Count, Embryo, Mammalian, Enzyme-Linked Immunosorbent Assay, Female, Flow Cytometry, Male, Microfilament Proteins, RNA, Messenger, Sex Characteristics, Interleukin-10, Rats, Sprague-Dawley, Microglia, Gene Expression Regulation, Developmental, Rats, Interleukin-1beta, Chemokine CXCL9
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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