Sex-Specific Features of Microglia from Adult Mice

Arnold, 1984, Gonadal steroid induction of structural sex differences in the central nervous system, Annu. Rev. Neurosci., 7, 413, 10.1146/annurev.ne.07.030184.002213 Balli, 2012, Foxm1 transcription factor is required for macrophage migration during lung inflammation and tumor formation, Oncogene, 31, 3875, 10.1038/onc.2011.549 Benedusi, 2017, Liver ERα regulates AgRP neuronal activity in the arcuate nucleus of female mice, Sci. Rep., 7, 1194, 10.1038/s41598-017-01393-0 Bennett, 2016, New tools for studying microglia in the mouse and human CNS, Proc. Natl. Acad. Sci. USA, 113, E1738, 10.1073/pnas.1525528113 Ciana, 2003, In vivo imaging of transcriptionally active estrogen receptors, Nat. Med., 9, 82, 10.1038/nm809 Crain, 2013, Microglia express distinct M1 and M2 phenotypic markers in the postnatal and adult central nervous system in male and female mice, J. Neurosci. Res., 91, 1143, 10.1002/jnr.23242 Duan, 2013, Nanog attenuates lipopolysaccharide-induced inflammatory responses by blocking nuclear factor-κB transcriptional activity in BV-2 cells, Neuroreport, 24, 718, 10.1097/WNR.0b013e328363fd67 El Wakil, 2006, The GATA2 transcription factor negatively regulates the proliferation of neuronal progenitors, Development, 133, 2155, 10.1242/dev.02377 Elmore, 2014, Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain, Neuron, 82, 380, 10.1016/j.neuron.2014.02.040 Fonseca, 2017, Cell-specific deletion of C1qa identifies microglia as the dominant source of C1q in mouse brain, J. Neuroinflammation, 14, 48, 10.1186/s12974-017-0814-9 Gardoni, 2002, Lack of PSD-95 drives hippocampal neuronal cell death through activation of an alpha CaMKII transduction pathway, Eur. J. Neurosci., 16, 777, 10.1046/j.1460-9568.2002.02141.x Gelderblom, 2009, Temporal and spatial dynamics of cerebral immune cell accumulation in stroke, Stroke, 40, 1849, 10.1161/STROKEAHA.108.534503 Gelosa, 2014, Microglia is a key player in the reduction of stroke damage promoted by the new antithrombotic agent ticagrelor, J. Cereb. Blood Flow Metab., 34, 979, 10.1038/jcbfm.2014.45 Golomb, 2009, Male predominance in childhood ischemic stroke: findings from the international pediatric stroke study, Stroke, 40, 52, 10.1161/STROKEAHA.108.521203 Hanamsagar, 2017, Generation of a microglial developmental index in mice and in humans reveals a sex difference in maturation and immune reactivity, Glia, 65, 1504, 10.1002/glia.23176 Hooper, 2012, Interactions between the microbiota and the immune system, Science, 336, 1268, 10.1126/science.1223490 Hu, 2015, Microglial and macrophage polarization—new prospects for brain repair, Nat. Rev. Neurol., 11, 56, 10.1038/nrneurol.2014.207 Kettenmann, 2013, Microglia: new roles for the synaptic stripper, Neuron, 77, 10, 10.1016/j.neuron.2012.12.023 Kierdorf, 2013, Factors regulating microglia activation, Front. Cell. Neurosci., 7, 44, 10.3389/fncel.2013.00044 Kierdorf, 2017, Microglia in steady state, J. Clin. Invest., 127, 3201, 10.1172/JCI90602 Kuleshov, 2016, Enrichr: a comprehensive gene set enrichment analysis web server 2016 update, Nucleic Acids Res., 44, W90, 10.1093/nar/gkw377 Lalancette-Hébert, 2007, Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain, J. Neurosci., 27, 2596, 10.1523/JNEUROSCI.5360-06.2007 Lenz, 2013, Microglia are essential to masculinization of brain and behavior, J. Neurosci., 33, 2761, 10.1523/JNEUROSCI.1268-12.2013 MacLusky, 1981, Sexual differentiation of the central nervous system, Science, 211, 1294, 10.1126/science.6163211 Matcovitch-Natan, 2016, Microglia development follows a stepwise program to regulate brain homeostasis, Science, 353, aad8670, 10.1126/science.aad8670 McCarthy, 2008, Estradiol and the developing brain, Physiol. Rev., 88, 91, 10.1152/physrev.00010.2007 McCarthy, 2015, At the frontier of epigenetics of brain sex differences, Front. Behav. Neurosci., 9, 221, 10.3389/fnbeh.2015.00221 McCullough, 2003, Aromatase cytochrome P450 and extragonadal estrogen play a role in ischemic neuroprotection, J. Neurosci., 23, 8701, 10.1523/JNEUROSCI.23-25-08701.2003 Miao, 2014, Tcf3 promotes cell migration and wound repair through regulation of lipocalin 2, Nat. Commun., 5, 4088, 10.1038/ncomms5088 Murphy, 2004, Stroke in the female: role of biological sex and estrogen, ILAR J., 45, 147, 10.1093/ilar.45.2.147 Neumann, 2009, Debris clearance by microglia: an essential link between degeneration and regeneration, Brain, 132, 288, 10.1093/brain/awn109 Olsson, 2016, Single-cell analysis of mixed-lineage states leading to a binary cell fate choice, Nature, 537, 698, 10.1038/nature19348 Pepe, 2014, Heterogeneous induction of microglia M2a phenotype by central administration of interleukin-4, J. Neuroinflammation, 11, 211, 10.1186/s12974-014-0211-6 Prinz, 2014, Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease, Nat. Rev. Neurosci., 15, 300, 10.1038/nrn3722 Rizzi, 2017, Identification of novel loci for the generation of reporter mice, Nucleic Acids Res., 45, e37, 10.1093/nar/gkw1142 Rupalla, 1998, Time course of microglia activation and apoptosis in various brain regions after permanent focal cerebral ischemia in mice, Acta Neuropathol., 96, 172, 10.1007/s004010050878 Salter, 2017, Microglia emerge as central players in brain disease, Nat. Med., 23, 1018, 10.1038/nm.4397 Schafer, 2013, The “quad-partite” synapse: microglia-synapse interactions in the developing and mature CNS, Glia, 61, 24, 10.1002/glia.22389 Sierra, 2008, Steroid hormone receptor expression and function in microglia, Glia, 56, 659, 10.1002/glia.20644 Spychala, 2017, Sex differences in neuroinflammation and neuroprotection in ischemic stroke, J. Neurosci. Res., 95, 462, 10.1002/jnr.23962 Stell, 2008, Molecular imaging provides novel insights on estrogen receptor activity in mouse brain, Mol. Imaging, 7, 283, 10.2310/7290.2008.00027 Trapnell, 2012, Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks, Nat. Protoc., 7, 562, 10.1038/nprot.2012.016 Tremblay, 2011, The role of microglia in the healthy brain, J. Neurosci., 31, 16064, 10.1523/JNEUROSCI.4158-11.2011 van Gelderen, 1994, Water diffusion and acute stroke, Magn. Reson. Med., 31, 154, 10.1002/mrm.1910310209 Vegeto, 2001, Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia, J. Neurosci., 21, 1809, 10.1523/JNEUROSCI.21-06-01809.2001 Vegeto, 2002, Estrogen and inflammation: hormone generous action spreads to the brain, Mol. Psychiatry, 7, 236, 10.1038/sj.mp.4001007 Villa, 2015, Estrogen accelerates the resolution of inflammation in macrophagic cells, Sci. Rep., 5, 15224, 10.1038/srep15224 Villa, 2016, Estrogens, neuroinflammation, and neurodegeneration, Endocr. Rev., 37, 372, 10.1210/er.2016-1007 Wu, 2009, Estrogen masculinizes neural pathways and sex-specific behaviors, Cell, 139, 61, 10.1016/j.cell.2009.07.036 Wu, 2015, Microglia: dynamic mediators of synapse development and plasticity, Trends Immunol., 36, 605, 10.1016/j.it.2015.08.008