Microglia across the lifespan: from origin to function in brain development, plasticity and cognition
Open accessAbstract
Microglia are the only immune cells that permanently reside in the central nervous system (CNS) alongside neurons and other types of glial cells. The past decade has witnessed a revolution in our understanding of their roles during normal physiological conditions. Cutting‐edge techniques revealed that these resident immune cells are critical for proper brain development, actively maintain health in the mature brain, and rapidly adapt their function to physiological or pathophysiological needs. In this review, we highlight recent studies on microglial origin (from the embryonic yolk sac) and the factors regulating their differentiation and homeostasis upon brain invasion. Elegant experiments tracking microglia in the CNS allowed studies of their unique roles compared with other types of resident macrophages. Here we review the emerging roles of microglia in brain development, plasticity and cognition, and discuss the implications of the depletion or dysfunction of microglia for our understanding of disease pathogenesis. Immune activation, inflammation and various other conditions resulting in undesirable microglial activity at different stages of life could severely impair learning, memory and other essential cognitive functions. The diversity of microglial phenotypes across the lifespan, between compartments of the CNS, and sexes, as well as their crosstalk with the body and external environment, is also emphasised. Understanding what defines particular microglial phenotypes is of major importance for future development of innovative therapies controlling their effector functions, with consequences for cognition across chronic stress, ageing, neuropsychiatric and neurological diseases. image
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Microglia in a homeostatic state use their ramified processes to survey the microenvironment in real time for potential signals that warrant further action.
“Microglia in a homeostatic state use their ramified processes to survey the microenvironment in real time for potential signals that warrant further action.”
From Microglia in neurodegenerative diseases: mechanism and potential therapeutic targets (2023) · cites this paper as [77]
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1 retracted
Bialas, A. R., & Stevens, B. (2013) · Nature Neuroscience · doi:10.1038/nn.3560 · Cited by 519 · see citing works
RetractedPolazzi, 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
Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo
Nimmerjahn, A., Kirchhoff, F., & Helmchen, F. (2005) · Science · doi:10.1126/science.1110647 · Cited by 5,827 · see citing works
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
The M1 and M2 paradigm of macrophage activation: Time for reassessment
Martinez, F. O., & Gordon, S. (2014) · F1000Prime Reports · doi:10.12703/p6-13 · Cited by 4,689 · 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 · cited 5× · see citing works
“…adolescence, adulthood and normal ageing, within the thalamus, cerebral cortex and hippocampus (Tremblay et al. 2010, 2012; Paolicelli et al. 2011; Schafer et al. 2012; Milior et al. 2015), suggesting a crucial role in synaptic plasticity and behavioural adaptation to the environment (Tremblay et…”
BackgroundInfluentialATP mediates rapid microglial response to local brain injury in vivo
Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., Littman, D. R., Dustin, M. L., & Gan, W.-B. (2005) · Nature Neuroscience · doi:10.1038/nn1472 · Cited by 3,913 · see citing works
Host microbiota constantly control maturation and function of microglia in the CNS
Erny, D., Hrabě de Angelis, A. L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4030 · Cited by 3,569 · 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
Fate Mapping Reveals Origins and Dynamics of Monocytes and Tissue Macrophages under Homeostasis
Yona, S., Kim, K.-W., Wolf, Y., Mildner, A., Varol, D., Breker, M., Strauss-Ayali, D., Viukov, S., Guilliams, M., Misharin, A., et al. (2013) · Immunity · doi:10.1016/j.immuni.2012.12.001 · Cited by 3,245 · 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 2,579 · see citing works
A Lineage of Myeloid Cells Independent of Myb and Hematopoietic Stem Cells
Schulz, C., Perdiguero, E. G., Chorro, L., Szabo-Rogers, H., Cagnard, N., Kierdorf, K., Prinz, M., Wu, B., Jacobsen, S. E. W., Pollard, J. W., et al. (2012) · Science · doi:10.1126/science.1219179 · Cited by 2,578 · see citing works
The gut microbiota influences blood-brain barrier permeability in mice
Braniste, V., Al-Asmakh, M., Kowal, C., Anuar, F., Abbaspour, A., Tóth, M., Korecka, A., Bakocevic, N., Ng, L. G., Kundu, P., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009759 · Cited by 2,530 · see citing works
Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors
Gomez Perdiguero, E., Klapproth, K., Schulz, C., Busch, K., Azzoni, E., Crozet, L., Garner, H., Trouillet, C., de Bruijn, M. F., Geissmann, F., et al. (2015) · Nature · doi:10.1038/nature13989 · Cited by 2,339 · cited 5× · see citing works
“…arise mainly from yolk sac (YS) primitive macrophages (Ginhoux et al. 2010; Hoeffel et al. 2012; Schulz et al. 2012; Kierdorf et al. 2013; Gomez Perdiguero et al. 2015; Hoeffel et al. 2015), reside in the brain throughout life, and maintain their numbers through a process of self-renewal…”
BackgroundInfluentialHashimoto, D., Chow, A., Noizat, C., Teo, P., Beasley, M. B., Leboeuf, M., Becker, C. D., See, P., Price, J., Lucas, D., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.04.004 · Cited by 2,311 · see citing works
Immune attack: the role of inflammation in Alzheimer disease
Heppner, F. L., Ransohoff, R. M., & Becher, B. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3880 · Cited by 2,134 · see citing works
the Immunological Genome Consortium, Gautier, E. L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K. G., et al. (2012) · Nature Immunology · doi:10.1038/ni.2419 · Cited by 1,972 · cited 3× · see citing works
“…and high throughput gene expression analyses that differentiated microglia from their myeloid relatives and other brain cells (Butovsky et al. 2012; Gautier et al. 2012; Chiu et al. 2013; Hickman et al. 2013; Butovsky et al. 2014), have aided the rapid progress towards unravelling the multiple…”
BackgroundElmore, M. R. P., Najafi, A. R., Koike, M. A., Dagher, N. N., Spangenberg, E. E., Rice, R. A., Kitazawa, M., Matusow, B., Nguyen, H., West, B. L., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.040 · Cited by 1,968 · see citing works
New tools for studying microglia in the mouse and human CNS
Bennett, M. L., Bennett, F. C., Liddelow, S. A., Ajami, B., Zamanian, J. L., Fernhoff, N. B., Mulinyawe, S. B., Bohlen, C. J., Adil, A., Tucker, A., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1525528113 · Cited by 1,804 · see citing works
Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny
Guilliams, M., Ginhoux, F., Jakubzick, C., Naik, S. H., Onai, N., Schraml, B. U., Segura, É., Tussiwand, R., & Yona, S. (2014) · Nature reviews. Immunology · doi:10.1038/nri3712 · Cited by 1,802 · see citing works
Microglia Shape Adult Hippocampal Neurogenesis through Apoptosis-Coupled Phagocytosis
Sierra, A., Encinas, J. M., Deudero, J. J. P., Chancey, J. H., Enikolopov, G., Overstreet-Wadiche, L. S., Tsirka, S. E., & Maletic-Savatic, M. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.08.014 · Cited by 1,622 · see citing works
Wake, H., Moorhouse, A. J., Jinno, S., Kohsaka, S., & Nabekura, J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4363-08.2009 · Cited by 1,619 · see citing works
Microglial interactions with synapses are modulated by visual experience
Tremblay, M.-È., Lowery, R. L., & Majewska, A. K. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000527 · Cited by 1,542 · see citing works
Self-citationThe P2Y12 receptor regulates microglial activation by extracellular nucleotides
Haynes, S. E., Hollopeter, G., Yang, G., Kurpius, D., Dailey, M. E., Gan, W.-B., & Julius, D. (2006) · Nature Neuroscience · doi:10.1038/nn1805 · Cited by 1,542 · see citing works
The microglial sensome revealed by direct RNA sequencing
Hickman, S. E., Kingery, N. D., Ohsumi, T. K., Borowsky, M. L., Wang, L.-C., Means, T. K., & El Khoury, J. (2013) · Nature Neuroscience · doi:10.1038/nn.3554 · Cited by 1,511 · see citing works
Hematopoietic Stem Cell Gene Therapy with a Lentiviral Vector in X-Linked Adrenoleukodystrophy
Cartier, N., Hacein-Bey-Abina, S., Bartholomae, C. C., Veres, G., Schmidt, M., Kutschera, I., Vidaud, M., Abel, U., Dal-Cortivo, L., Caccavelli, L., et al. (2009) · Science · doi:10.1126/science.1171242 · Cited by 1,508 · 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 1,468 · see citing works
Different immune cells mediate mechanical pain hypersensitivity in male and female mice
Sorge, R. E., Mapplebeck, J. C. S., Rosen, S., Beggs, S., Taves, S., Alexander, J. K., Martin, L. J., Austin, J.-S., Sotocinal, S. G., Chen, D., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4053 · Cited by 1,442 · see citing works
Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease
Prinz, M., & Priller, J. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3722 · Cited by 1,329 · see citing works
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
Zhan, Y., Paolicelli, R. C., Sforazzini, F., Weinhard, L., Bolasco, G., Pagani, F., Vyssotski, A. L., Bifone, A., Gozzi, A., Ragozzino, D., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3641 · Cited by 1,236 · see citing works
Hoeffel, G., Chen, J., Lavin, Y., Low, D., Almeida, F. F., See, P., Beaudin, A. E., Lum, J., Low, I., Forsberg, E. C., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.03.011 · Cited by 1,135 · see citing works
Microglial priming in neurodegenerative disease
Perry, V. H., & Holmes, C. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.38 · Cited by 1,127 · see citing works
Young blood reverses age-related impairments in cognitive function and synaptic plasticity in mice
Villeda, S. A., Plambeck, K. E., Middeldorp, J., Castellano, J. M., Mosher, K. I., Luo, J., Smith, L. K., Bieri, G., Lin, K., Berdnik, D., et al. (2014) · Nature Medicine · doi:10.1038/nm.3569 · Cited by 1,081 · see citing works
Vascular and Neurogenic Rejuvenation of the Aging Mouse Brain by Young Systemic Factors
Katsimpardi, L., Litterman, N. K., Schein, P. A., Miller, C. M., Loffredo, F. S., Wojtkiewicz, G. R., Chen, J. W., Lee, R. T., Wagers, A. J., & Rubin, L. L. (2014) · Science · doi:10.1126/science.1251141 · Cited by 1,037 · see citing works
Wang, Y., Szretter, K. J., Vermi, W., Gilfillan, S., Rossini, C., Cella, M., Barrow, A. D., Diamond, M. S., & Colonna, M. (2012) · Nature Immunology · doi:10.1038/ni.2360 · Cited by 1,011 · 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
Self-citationMicroglia 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
Maternal immune activation and abnormal brain development across CNS disorders
Knuesel, I., Chicha, L., Britschgi, M., Schobel, S. A., Bodmer, M., Hellings, J. A., Toovey, S., & Prinssen, E. P. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.187 · Cited by 880 · see citing works
Microglia: Scapegoat, saboteur, or something else?
Aguzzi, A., Barres, B. A., & Bennett, M. L. (2013) · Science · doi:10.1126/science.1227901 · Cited by 836 · see citing works
Godbout, J. P., Chen, J., Abraham, J., Richwine, A. F., Berg, B. M., Kelley, K. W., & Johnson, R. W. (2005) · The FASEB Journal · doi:10.1096/fj.05-3776fje · Cited by 813 · see citing works
Review: microglia of the aged brain: primed to be activated and resistant to regulation
Norden, D. M., & Godbout, J. P. (2013) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2012.01306.x · Cited by 792 · see citing works
Ponomarev, E. D., Veremeyko, T., Barteneva, N., Krichevsky, A. M., & Weiner, H. L. (2011) · Nature Medicine · doi:10.1038/nm.2266 · Cited by 787 · see citing works
Neuronal ‘On’ and ‘Off’ signals control microglia
Biber, K., Neumann, H., Inoue, K., & Boddeke, H. W. G. M. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.08.007 · Cited by 787 · see citing works
Hoeffel, G., Wang, Y., Greter, M., See, P., Teo, P., Malleret, B., Leboeuf, M., Low, D., Oller, G., Almeida, F., et al. (2012) · Journal of Experimental Medicine · doi:10.1084/jem.20120340 · Cited by 786 · 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
Microglia and neurodegeneration: The role of systemic inflammation
Cunningham, C. (2013) · Glia · doi:10.1002/glia.22350 · Cited by 769 · see citing works
Microglia Promote the Death of Developing Purkinje Cells
Marı́n-Teva, J. L., Dusart, I., Colin, C., Gervais, A., van Rooijen, N., & Mallat, M. (2004) · Neuron · doi:10.1016/s0896-6273(04)00069-8 · Cited by 757 · see citing works
Beers, D. R., Henkel, J. S., Xiao, Q., Zhao, W., Wang, J., Yen, A. A., Siklos, L., McKercher, S. R., & Appel, S. H. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607423103 · Cited by 733 · see citing works
Streit, W. J., Braak, H., Xue, Q.-S., & Bechmann, I. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0556-6 · Cited by 727 · see citing works
Dystrophic microglia in the aging human brain
Streit, W. J., Sammons, N. W., Kuhns, A. J., & Sparks, D. L. (2004) · Glia · doi:10.1002/glia.10319 · Cited by 705 · see citing works
A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation
Goldmann, T., Wieghofer, P., Müller, P. F., Wolf, Y., Varol, D., Yona, S., Brendecke, S. M., Kierdorf, K., Staszewski, O., Datta, M., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3531 · Cited by 688 · see citing works
Microglia derived from aging mice exhibit an altered inflammatory profile
Sierra, A., Gottfried‐Blackmore, A. C., McEwen, B. S., & Bulloch, K. (2007) · Glia · doi:10.1002/glia.20468 · Cited by 688 · see citing works
Shechter, R., Miller, O., Yovel, G., Rosenzweig, N., London, A., Ruckh, J., Kim, K.-W., Klein, E., Kalchenko, V., Bendel, P., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.02.012 · Cited by 683 · see citing works
Heterogeneity of CNS myeloid cells and their roles in neurodegeneration
Prinz, M., Priller, J., Sisodia, S. S., & Ransohoff, R. M. (2011) · Nature Neuroscience · doi:10.1038/nn.2923 · Cited by 674 · see citing works
Sex differences in microglial colonization of the developing rat brain
Schwarz, J. M., Sholar, P. W., & Bilbo, S. D. (2012) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07630.x · Cited by 672 · see citing works
Kreisel, T., Frank, M. G., Licht, T., Reshef, R., Ben-Menachem-Zidon, O., Baratta, M. V., Maier, S. F., & Yirmiya, R. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.155 · Cited by 663 · see citing works
Microglia: Dynamic Mediators of Synapse Development and Plasticity
Wu, Y., Dissing-Olesen, L., MacVicar, B. A., & Stevens, B. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.08.008 · Cited by 661 · see citing works
Microglia Modulate Wiring of the Embryonic Forebrain
Squarzoni, P., Oller, G., Hoeffel, G., Pont‐Lezica, L., Rostaing, P., Low, D., Bessis, A., Ginhoux, F., & Garel, S. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.042 · Cited by 655 · see citing works
Chiu, I. M., Morimoto, E. T. A., Goodarzi, H., Liao, J. T., O’Keeffe, S., Phatnani, H. P., Muratet, M., Carroll, M. C., Levy, S., Tavazoie, S., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.06.018 · Cited by 651 · 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
Greter, M., Lelios, I., Pelczar, P., Hoeffel, G., Price, J., Leboeuf, M., Kündig, T. M., Frei, K., Ginhoux, F., Merad, M., et al. (2012) · Immunity · doi:10.1016/j.immuni.2012.11.001 · Cited by 630 · see citing works
CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity
Rogers, J. T., Morganti, J. M., Bachstetter, A. D., Hudson, C. E., Peters, M. M., Grimmig, B. A., Weeber, E. J., Bickford, P. C., & Gemma, C. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3667-11.2011 · Cited by 624 · see citing works
Microglial dysfunction in brain aging and Alzheimer's disease
Mosher, K. I., & Wyss-Coray, T. (2014) · Biochemical Pharmacology · doi:10.1016/j.bcp.2014.01.008 · Cited by 618 · see citing works
Peri, F., & Nüsslein-Volhard, C. (2008) · Cell · doi:10.1016/j.cell.2008.04.037 · Cited by 617 · see citing works
Wild-type microglia arrest pathology in a mouse model of Rett syndrome
Derecki, N. C., Cronk, J. C., Lu, Z., Xu, E., Abbott, S. B. G., Guyenet, P. G., & Kipnis, J. (2012) · Nature · doi:10.1038/nature10907 · Cited by 607 · see citing works
Transcription factors in myeloid development: balancing differentiation with transformation
Rosenbauer, F., & Tenen, D. G. (2007) · Nature Reviews Immunology · doi:10.1038/nri2024 · Cited by 606 · cited 1× · see citing works
“The early development of YS microglia precursors is dependent on key transcription factors Pu.1, a member of the Ets family (Rosenbauer & Tenen, 2007) and interferon regulatory factor Irf8, which both function as heterodimers in the determination of brain macrophage phenotype (Beers et al. 2006;…”
BackgroundReciprocal Regulation between Resting Microglial Dynamics and Neuronal Activity In Vivo
Li, Y., Du, X.-F., Liu, C., Wen, Z., & Du, J. (2012) · Developmental Cell · doi:10.1016/j.devcel.2012.10.027 · Cited by 553 · 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
Eyo, U. B., Peng, J., Swiatkowski, P., Mukherjee, A., Bispo, A., & Wu, L.-J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0416-14.2014 · Cited by 509 · see citing works
Age-related alterations in the dynamic behavior of microglia
Damani, M. R., Zhao, L., Fontainhas, A. M., Amaral, J., Fariss, R. N., & Wong, W. T. (2011) · Aging Cell · doi:10.1111/j.1474-9726.2010.00660.x · Cited by 504 · see citing works
Microglia Enhance Neurogenesis and Oligodendrogenesis in the Early Postnatal Subventricular Zone
Shigemoto‐Mogami, Y., Hoshikawa, K., Goldman, J. E., Sekino, Y., & Sato, K. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1619-13.2014 · Cited by 499 · see citing works
A role for glia in the progression of Rett’s syndrome
Lioy, D. T., Garg, S. K., Monaghan, C. E., Raber, J., Foust, K. D., Kaspar, B. K., Hirrlinger, P. G., Kirchhoff, F., Bissonnette, J. M., Ballas, N., et al. (2011) · Nature · doi:10.1038/nature10214 · Cited by 496 · see citing works
Trends in Infectious Diseases Mortality in the United States
Pinner, R. W. (1996) · JAMA: The Journal of the American Medical Association · doi:10.1001/jama.1996.03530270029027 · Cited by 487 · see citing works
Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS
Butovsky, O., Siddiqui, S., Gabriely, G., Lanser, A. J., Dake, B., Murugaiyan, G., Doykan, C. E., Wu, P. M., Gali, R. R., Iyer, L. K., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci62636 · Cited by 481 · see citing works
Microglial control of neuronal death and synaptic properties
Bessis, A., Béchade, C., Bernard, D., & Roumier, A. (2006) · Glia · doi:10.1002/glia.20459 · Cited by 454 · see citing works
Hematopoietic origin of pathological grooming in Hoxb8 mutant mice
Chen, S.-K., Tvrdik, P., Peden, E., Cho, S., Wu, S., Spangrude, G., & Capecchi, M. R. (2010) · Cell · doi:10.1016/j.cell.2010.03.055 · Cited by 450 · see citing works
Origin of microglia: current concepts and past controversies
Ginhoux, F., & Prinz, M. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020537 · Cited by 446 · see citing works
Most Tissue-Resident Macrophages Except Microglia Are Derived from Fetal Hematopoietic Stem Cells.
Sheng, J., Ruedl, C., & Karjalainen, K. (2015) · Immunity · doi:10.1016/j.immuni.2015.07.016 · Cited by 441 · see citing works
Dark microglia: A new phenotype predominantly associated with pathological states
Bisht, K., Sharma, K. P., Lecours, C., Gabriela Sánchez, M., El Hajj, H., Milior, G., Olmos‐Alonso, A., Gómez‐Nicola, D., Luheshi, G., Vallières, L., et al. (2016) · Glia · doi:10.1002/glia.22966 · Cited by 421 · see citing works
Self-citationHinwood, M., Morandini, J., Day, T. A., & Walker, F. R. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr229 · Cited by 420 · see citing works
Steroid hormone receptor expression and function in microglia
Sierra, A., Gottfried‐Blackmore, A., Milner, T. A., McEwen, B. S., & Bulloch, K. (2008) · Glia · doi:10.1002/glia.20644 · Cited by 405 · see citing works
Microglia instruct subventricular zone neurogenesis
Walton, N. M., Sutter, B. M., Laywell, E. D., Levkoff, L. H., Kearns, S. M., Marshall, G. P., Scheffler, B., & Steindler, D. A. (2006) · Glia · doi:10.1002/glia.20419 · Cited by 403 · see citing works
Microglial senescence: does the brain's immune system have an expiration date?
Streit, W. J. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.07.001 · Cited by 397 · see citing works
Dilger, R. N., & Johnson, R. W. (2008) · Journal of Leukocyte Biology · doi:10.1189/jlb.0208108 · Cited by 391 · see citing works
Hoshiko, M., Arnoux, I., Avignone, E., Yamamoto, N., & Audinat, E. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.1167-12.2012 · Cited by 384 · cited 2× · see citing works
“It is necessary for the timely recruitment of microglial cells into the early postnatal hippocampus and cerebral cortex (Hoshiko et al. 2012; Ueno et al. 2013; Paolicelli et al. 2014).”
BackgroundRett Syndrome Microglia Damage Dendrites and Synapses by the Elevated Release of Glutamate
Maezawa, I., & Jin, L. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5966-09.2010 · Cited by 348 · see citing works
Mizutani, M., Pino, P. A., Saederup, N., Charo, I. F., Ransohoff, R. M., & Cardona, A. E. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1100421 · Cited by 346 · see citing works
Fontainhas, A. M., Wang, M., Liang, K. J., Chen, S., Mettu, P., Damani, M., Fariss, R. N., Li, W., & Wong, W. T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0015973 · Cited by 334 · see citing works
mRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging
Frank, M. G., Barrientos, R. M., Biedenkapp, J. C., Rudy, J. W., Watkins, L. R., & Maier, S. F. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.03.013 · Cited by 327 · see citing works
Age and gender effects on microglia and astrocyte numbers in brains of mice
Mouton, P. R., Long, J. M., Lei, D.-L., Howard, V., Jucker, M., Calhoun, M. E., & Ingram, D. K. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03475-3 · Cited by 320 · see citing works
Homeostatic and injury‐induced microglia behavior in the aging brain
Hefendehl, J. K., Neher, J. J., Sühs, R. B., Kohsaka, S., Skodras, A., & Jucker, M. (2014) · Aging Cell · doi:10.1111/acel.12149 · Cited by 319 · see citing works
Neuroinflammation in the normal aging hippocampus
Barrientos, R. M., Kitt, M. M., Watkins, L. R., & Maier, S. F. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.03.007 · Cited by 315 · see citing works
Otero, K., Turnbull, I. R., Poliani, P. L., Vermi, W., Cerutti, E., Aoshi, T., Tassi, I., Takai, T., Stanley, S. L., Miller, M., et al. (2009) · Nature Immunology · doi:10.1038/ni.1744 · Cited by 315 · see citing works
Fractalkine regulation of microglial physiology and consequences on the brain and behavior
Paolicelli, R. C., Bisht, K., & Tremblay, M. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00129 · Cited by 314 · see citing works
Self-citationEffects of aging and sensory loss on glial cells in mouse visual and auditory cortices
Tremblay, M., Zettel, M. L., Ison, J. R., Allen, P. D., & Majewska, A. K. (2012) · Glia · doi:10.1002/glia.22287 · Cited by 309 · 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
Activation of Neuronal NMDA Receptors Triggers Transient ATP-Mediated Microglial Process Outgrowth
Dissing-Olesen, L., LeDue, J. M., Rungta, R. L., Hefendehl, J. K., Choi, H. B., & MacVicar, B. A. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0405-14.2014 · Cited by 286 · see citing works
Entry and Distribution of Microglial Cells in Human Embryonic and Fetal Cerebral Cortex
Monier, A., Adle‐Biassette, H., Delezoide, A., Evrard, P., Gressèns, P., & Verney, C. (2007) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3180517b46 · Cited by 278 · 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 · cited 2× · see citing works
“2014) also increased synaptic density in the hippocampus (Rice et al. 2015).”
BackgroundVerney, C., Monier, A., Fallet‐Bianco, C., & Gressèns, P. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01245.x · Cited by 266 · see citing works
Region‐specific expression of immunoregulatory proteins on microglia in the healthy CNS
Haas, A. H. D., Boddeke, H. W. G. M., & Biber, K. P. H. (2008) · Glia · doi:10.1002/glia.20663 · Cited by 258 · see citing works
Dual Roles for Perivascular Macrophages in Immune-to-Brain Signaling
Serrats, J., Schiltz, J. C., García-Bueno, B., van Rooijen, N., Reyes, T. M., & Sawchenko, P. E. (2010) · Neuron · doi:10.1016/j.neuron.2009.11.032 · Cited by 253 · see citing works
Sierra, A., Beccari, S., Díaz‐Aparicio, I., Encinas, J. M., Comeau, S., & Tremblay, M. (2014) · Neural Plasticity · doi:10.1155/2014/610343 · Cited by 249 · see citing works
Self-citationFractalkine 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
Self-citationGlia engulf degenerating axons during developmental axon pruning.
Watts, R., Schuldiner, O., Perrino, J., Larsen, C., & Luo, L.-Q. (2004) · Current Biology · doi:10.1016/j.cub.2004.03.035 · Cited by 241 · see citing works
Microglia in the aging brain: relevance to neurodegeneration
Luo, X.-G., Ding, J.-Q., & Chen, S.-D. (2010) · Molecular Neurodegeneration · doi:10.1186/1750-1326-5-12 · Cited by 236 · cited 1× · see citing works
“These parameters indicate that as humans and rodents age microglia take on a phenotype consistent with a pro-inflammatory response, even in the absence of overt pathological stimuli (Luo et al. 2010; Choi & Won, 2011; Wong, 2013; Sierra et al. 2014; Ojo et al. 2015; Barrientos et al. 2015a).”
BackgroundMicroglial Expression of MHC Class II Increases in Normal Aging of Nonhuman Primates
Sheffield, L. G., & Berman, N. E. J. (1998) · Neurobiology of Aging · doi:10.1016/s0197-4580(97)00168-1 · Cited by 234 · see citing works
Neural progenitor cells orchestrate microglia migration and positioning into the developing cortex
Arnò, B., Grassivaro, F., Rossi, C., Bergamaschi, A., Castiglioni, V., Furlan, R., Greter, M., Favaro, R., Comı, G., Becher, B., et al. (2014) · Nature Communications · doi:10.1038/ncomms6611 · Cited by 233 · see citing works
Impaired Synaptic Function in the Microglial KARAP/DAP12-Deficient Mouse
Roumier, A., Béchade, C., Poncer, J. C., Smalla, K., Tomasello, E., Vivier, É., Gundelfinger, E. D., Triller, A., & Bessis, A. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2251-04.2004 · Cited by 228 · see citing works
Microglial aging in the healthy CNS: phenotypes, drivers, and rejuvenation
Wong, W. T. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00022 · Cited by 227 · see citing works
Swinnen, N., Smolders, S., Ávila, A., Notelaers, K., Paesen, R., Ameloot, M. M., Brône, B., Legendre, P., & Rigo, J. (2012) · Glia · doi:10.1002/glia.22421 · Cited by 226 · see citing works
A distinct population of microglia supports adult neurogenesis in the subventricular zone
Ribeiro Xavier, A. L., Kress, B. T., Goldman, S. A., Lacerda de Menezes, J. R., & Nedergaard, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1217-15.2015 · Cited by 225 · see citing works
USP18 lack in microglia causes destructive interferonopathy of the mouse brain
Goldmann, T., Zeller, N., Raasch, J., Kierdorf, K., Frenzel, K., Ketscher, L., Basters, A., Staszewski, O., Brendecke, S. M., Spiess, A., et al. (2015) · The EMBO Journal · doi:10.15252/embj.201490791 · Cited by 223 · see citing works
Self-citationO’Koren, E. G., Mathew, R., & Saban, D. R. (2016) · Scientific Reports · doi:10.1038/srep20636 · Cited by 220 · 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
Karlstetter, M., Nothdurfter, C., Aslanidis, A., Moeller, K., Horn, F., Scholz, R., Neumann, H., Weber, B. H. F., Rupprecht, R., & Langmann, T. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-3 · Cited by 216 · see citing works
Three-Dimensional Analysis of Vascular Development in the Mouse Embryo
Walls, J. R., Coultas, L., Rossant, J., & Henkelman, R. M. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002853 · Cited by 209 · see citing works
Wild-type microglia do not reverse pathology in mouse models of Rett syndrome
Wang, J., Wegener, E., Huang, T.-W., Sripathy, S. P., Jesús‐Cortés, H. D., Xu, P., Tran, S., Knobbe, W., Leko, V., Britt, J. K., et al. (2015) · Nature · doi:10.1038/nature14444 · Cited by 201 · see citing works
Wang, M., Wang, X., Zhao, L., Ma, W., Rodríguez, I. R., Fariss, R. N., & Wong, W. T. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3153-13.2014 · Cited by 201 · 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 · cited 4× · see citing works
“Interestingly the decline in microglial numbers after the third postnatal week was not mitigated by upregulating brain Csf-1 levels (Nikodemova et al. 2015), indicating the existence of alternative microglial responses to unknown developmental signals that drive the apoptosis of a population of microglial cells during…”
BackgroundInfluentialGalea, I., Palin, K., Newman, T. A., van Rooijen, N., Perry, V. H., & Boche, D. (2004) · Glia · doi:10.1002/glia.20124 · Cited by 183 · see citing works
Castanon, N., Luheshi, G. N., & Layé, S. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00229 · Cited by 179 · see citing works
Xu, J., Zhu, L., He, S., Wu, Y., Jin, W., Yu, T., Qu, J. Y., & Wen, Z. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.08.018 · Cited by 177 · see citing works
Selective activation of microglia facilitates synaptic strength
Clark, A. K., Gruber-Schoffnegger, D., Drdla-Schutting, R., Gerhold, K. J., Malcangio, M., & Sandkühler, J. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.2061-14.2015 · Cited by 171 · see citing works
Activation of microglia in the brains of humans with heart disease and hypercholesterolemic rabbits
Streit, W. J., & Sparks, D. L. (1997) · Journal of Molecular Medicine · doi:10.1007/s001090050097 · Cited by 168 · see citing works
Microglia change from a reactive to an age-like phenotype with the time in culture
Caldeira, C., Oliveira, A. F., Cunha, C., Vaz, A. R., Falcão, A. S., Fernandes, A., & Brites, D. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00152 · Cited by 156 · see citing works
Zusso, M., Methot, L., Lo, R., Greenhalgh, A. D., David, S., & Stifani, S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6182-11.2012 · Cited by 154 · see citing works
Modulation of Microglial Process Convergence Toward Neuronal Dendrites by Extracellular Calcium
Eyo, U. B., Gu, N., De, S., Dong, H., Richardson, J. R., & Wu, L.-J. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.3279-14.2015 · Cited by 154 · see citing works
Maggi, L. (2011) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2011.00022 · Cited by 149 · see citing works
Prenatal activation of microglia induces delayed impairment of glutamatergic synaptic function
Roumier, A., Pascual, O., Béchade, C., Wakselman, S., Poncer, J.-C., Réal, E., Triller, A., & Bessis, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002595 · Cited by 146 · see citing works
Long Term Potentiation Is Impaired in Membrane Glycoprotein CD200-deficient Mice
Costello, D. A., Lyons, A., Denieffe, S., Browne, T. C., Cox, F., & Lynch, M. A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.280826 · Cited by 145 · see citing works
Microglial activation in healthy aging
Schuitemaker, A., van der Doef, T. F., Boellaard, R., van der Flier, W. M., Yaqub, M., Windhorst, A. D., Barkhof, F., Jonker, C., Kloet, R. W., Lammertsma, A. A., et al. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.09.016 · Cited by 142 · see citing works
Regulation of microglia development and homeostasis.
Greter, M., & Merad, M. (2013) · Glia · doi:10.1002/glia.22408 · Cited by 141 · see citing works
What is microglia neurotoxicity (Not)?
Biber, K. P. H., Owens, T., & Boddeke, E. (2014) · Glia · doi:10.1002/glia.22654 · Cited by 141 · see citing works
The role of microglia in human disease: therapeutic tool or target?
Cartier, N., Lewis, C. B., Zhang, R., & Rossi, F. M. V. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1330-y · Cited by 135 · see citing works
VanGuilder, H. D., Bixler, G. V., Brucklacher, R. M., Farley, J. A., Yan, H., Warrington, J. P., Sonntag, W. E., & Freeman, W. M. (2011) · Journal of Neuroinflammation · doi:10.1186/1742-2094-8-138 · Cited by 132 · see citing works
Microglial P2Y12 receptors regulate microglial activation and surveillance during neuropathic pain
Gu, N., Eyo, U. B., Murugan, M., Peng, J., Matta, S., Dong, H., & Wu, L. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.11.007 · Cited by 131 · 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
Microglial control of neuronal activity
Béchade, C., Cantaut-Belarif, Y., & Bessis, A. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00032 · Cited by 122 · see citing works
Abutbul, S., Shapiro, J., Szaingurten‐Solodkin, I., Levy, N., Carmy, Y., Baron, R., Jung, S., & Monsonego, A. (2012) · Glia · doi:10.1002/glia.22343 · Cited by 122 · see citing works
Genetic targeting of microglia
Wieghofer, P., Knobeloch, K., & Prinz, M. (2014) · Glia · doi:10.1002/glia.22727 · Cited by 116 · see citing works
Wasserman, J. K., Yang, H. H., & Schlichter, L. C. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06442.x · Cited by 113 · see citing works
Brain region-specific gene expression profiles in freshly isolated rat microglia
Doorn, K. J., Brevé, J. J. P., Drukarch, B., Boddeke, H. W. G. M., Huitinga, I., Lucassen, P. J., & van Dam, A. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00084 · Cited by 110 · see citing works
Minten, C., Terry, R., Deffrasnes, C., King, N. J. C., & Campbell, I. L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049851 · Cited by 100 · see citing works
Microglia in the developing brain: from immunity to behaviour
Schlegelmilch, T., Henke, K., & Peri, F. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.08.004 · Cited by 99 · see citing works
Arnoux, I., Hoshiko, M., Mandavy, L., Avignone, E., Yamamoto, N., & Audinat, É. (2013) · Glia · doi:10.1002/glia.22503 · Cited by 96 · see citing works
Hellwig, S., Masuch, A., Nestel, S., Katzmarski, N., Meyer-Luehmann, M., & Biber, K. (2015) · Scientific Reports · doi:10.1038/srep14624 · Cited by 91 · see citing works
Williamson, L. L., McKenney, E. A., Holzknecht, Z. E., Belliveau, C., Rawls, J. F., Poulton, S., Parker, W., & Bilbo, S. D. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.07.006 · Cited by 84 · see citing works
Maggi, L., Trettel, F., Scianni, M., Bertollini, C., Eusebi, F., Fredholm, B. B., & Limatola, C. (2009) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2009.07.016 · Cited by 84 · see citing works
Impact of age-related neuroglial cell responses on hippocampal deterioration
Ojo, J. O., Rezaie, P., Gabbott, P. L. A., & Stewart, M. G. (2015) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2015.00057 · Cited by 81 · see citing works
Ahlers‐Dannen, K. E., Karaçay, B., Fuller, L. C., Bonthius, D. J., & Dailey, M. E. (2015) · Glia · doi:10.1002/glia.22835 · Cited by 80 · see citing works
Memory impairments in healthy aging: Role of aging-induced microglial sensitization.
Barrientos, R. M., Frank, M. G., Watkins, L. R., & Maier, S. F. (2010) · PubMed Central · Cited by 80 · see citing works
Microglia and Synapse: Interactions in Health and Neurodegeneration
Šišková, Z., & Tremblay, M.-È. (2013) · Neural Plasticity · doi:10.1155/2013/425845 · Cited by 80 · see citing works
Self-citationRigato, C., Swinnen, N., Buckinx, R., Couillin, I., Mangin, J., Rigo, J., Legendre, P., & Corronc, H. L. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1042-12.2012 · Cited by 73 · see citing works
Neuro-immune dysfunction during brain aging: new insights in microglial cell regulation
Matt, S. M., & Johnson, R. W. (2015) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2015.10.009 · Cited by 73 · see citing works
Suridjan, I., Rusjan, P. M., Voineskos, A. N., Selvanathan, T., Setiawan, E., Strafella, A. P., Wilson, A. A., Meyer, J. H., Houle, S., & Mizrahi, R. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2013.09.021 · Cited by 71 · see citing works
Greater glucocorticoid receptor activation in hippocampus of aged rats sensitizes microglia
Barrientos, R. M., Thompson, V. M., Kitt, M. M., Amat, J., Hale, M. W., Frank, M. G., Crysdale, N. Y., Stamper, C. E., Hennessey, P. A., Watkins, L. R., et al. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.12.003 · Cited by 70 · see citing works
Microglia: An Active Player in the Regulation of Synaptic Activity
Ji, K., Miyauchi, J. T., & Tsirka, S. E. (2013) · Neural Plasticity · doi:10.1155/2013/627325 · Cited by 67 · see citing works
Microglia recapitulate a hematopoietic master regulator network in the aging human frontal cortex
Wehrspaun, C. C., Haerty, W., & Ponting, C. P. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.04.008 · Cited by 64 · see citing works
Gómez‐Nicola, D., Schetters, S. T. T., & Perry, V. H. (2014) · Glia · doi:10.1002/glia.22660 · Cited by 59 · see citing works
Bilbo, S. D. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.02.017 · Cited by 46 · see citing works
Go with your gut: microbiota meet microglia
Mosher, K. I., & Wyss‐Coray, T. (2015) · Nature Neuroscience · doi:10.1038/nn.4051 · Cited by 43 · see citing works
<i>miR‐124</i> Contributes to the functional maturity of microglia
Svahn, A. J., Giacomotto, J., Graeber, M. B., Rinkwitz, S., & Becker, T. S. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22328 · Cited by 42 · see citing works
The initiation of blood flow and flow induced events in early vascular development
Jones, E. A. V. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.09.020 · Cited by 39 · see citing works
Long‐lasting post‐mortem activity of spinal microglia in situ in mice
Dibaj, P., Steffens, H., Nadrigny, F., Neusch, C., Kirchhoff, F., & Schomburg, E. D. (2010) · Journal of Neuroscience Research · doi:10.1002/jnr.22402 · Cited by 36 · see citing works
Microglia in the normally aged hippocampus
Choi, J. H., & Won, M. (2011) · Laboratory Animal Research · doi:10.5625/lar.2011.27.3.181 · Cited by 28 · see citing works
Cho, K. H., Cheong, J. S., Kim, J. H., Abé, H., Murakami, G., & Cho, B. H. (2013) · BioMed Research International · doi:10.1155/2013/762303 · Cited by 23 · see citing works
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- Tremblay ME, Stevens B, Sierra A, Wake H, Bessis A & Nimmerjahn A (2011). The role of microglia in the healthy brain. J Neurosci 31, 16064–16069. [DOI] [PMC free article] [PubMed] [Google Scholar]
Cited by
Sorted by citations
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · 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
Microglia in neurodegenerative diseases: mechanism and potential therapeutic targets
Gao, C., Jiang, J., Tan, Y., & Chen, S. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01588-0 · Cited by 1,616 · 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
Layé, S., Nadjar, A., Joffre, C., & Bazinet, R. P. (2018) · Pharmacological Reviews · doi:10.1124/pr.117.014092 · Cited by 420 · see citing works
Wang, Z., Chen, W.-H., Li, S.-X., He, Z.-M., Zhu, W.-L., Ji, Y.-B., Wang, Z., Zhu, X.-M., Yuan, K., Bao, Y.-P., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01113-1 · Cited by 307 · see citing works
Sex-specific effects of microbiome perturbations on cerebral Aβ amyloidosis and microglia phenotypes
Dodiya, H. B., Kuntz, T., Shaik, S. M., Baufeld, C., Leibowitz, J., Zhang, X., Gottel, N., Zhang, X., Butovsky, O., Gilbert, J. A., et al. (2019) · Journal of Experimental Medicine · doi:10.1084/jem.20182386 · Cited by 288 · see citing works
Cross talk: the microbiota and neurodevelopmental disorders
Kelly, J. R., Minuto, C., Cryan, J. F., Clarke, G., & Dinan, T. G. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00490 · Cited by 271 · see citing works
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Savage, J. C., Carrier, M., & Tremblay, M.-È. (2019) · Methods in Molecular Biology · doi:10.1007/978-1-4939-9658-2_2 · Cited by 232 · see citing works
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Bernaus, A., Blanco, S., & Sevilla, A. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00209 · Cited by 157 · see citing works
Lehmann, M. L., Weigel, T. K., Poffenberger, C. N., & Herkenham, M. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.0184-19.2019 · Cited by 138 · see citing works
Boehme, M., van de Wouw, M., Bastiaanssen, T. F. S., Olavarría-Ramírez, L., Lyons, K., Fouhy, F., Golubeva, A. V., Moloney, G. M., Minuto, C., Sandhu, K. V., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0425-1 · Cited by 128 · see citing works
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Dodiya, H. B., Lutz, H. L., Weigle, I. Q., Patel, P., Michalkiewicz, J., Roman-Santiago, C. J., Zhang, C. M., Liang, Y., Srinath, A., Zhang, X., et al. (2022) · Journal of Experimental Medicine · doi:10.1084/jem.20200895 · Cited by 120 · see citing works
Of microbes and minds: A narrative review on the second brain aging
Calvani, R., Picca, A., Lo Monaco, M. R., Landi, F., Bernabei, R., & Marzetti, E. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00053 · Cited by 92 · see citing works
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(2020) · Advances in Protein Chemistry and Structural Biology · doi:10.1016/bs.apcsb.2019.08.007 · Cited by 83 · see citing works
Zhou, N., Liu, K., Sun, Y., Cao, Y., & Yang, J. (2019) · Protein & Cell · doi:10.1007/s13238-018-0599-3 · Cited by 81 · see citing works
Strackeljan, L., Baczynska, E., Cangalaya, C., Baidoe-Ansah, D., Wlodarczyk, J., Kaushik, R., & Dityatev, A. (2021) · Cells · doi:10.3390/cells10081862 · Cited by 71 · see citing works
González Ibanez, F., Picard, K., Bordeleau, M., Sharma, K., Bisht, K., & Tremblay, M.-È. (2019) · Journal of Visualized Experiments · doi:10.3791/60510 · Cited by 77 · see citing works
Self-citationPistono, C., Bister, N., Stanová, I., & Malm, T. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.623771 · Cited by 75 · see citing works
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Plastini, M. J., Desu, H. L., & Brambilla, R. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00269 · Cited by 48 · see citing works
Tremblay, M.-È. (2021) · Brain, Behavior, & Immunity - Health · doi:10.1016/j.bbih.2021.100301 · Cited by 42 · see citing works
Self-citationDrobny, A., Ngo, P. A., Neurath, M. F., Zunke, F., & López-Posadas, R. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.655123 · Cited by 24 · see citing works
Xie, M., Wang, T., Feng, J., Ma, D., Feng, L., & Hao, Y. (2025) · Current Neuropharmacology · doi:10.2174/1570159x23666250225091729 · Cited by 7 · see citing works
Carrier, M., Robert, M.-È., St-Pierre, M.-K., Ibáñez, F. G., Gonçalves de Andrade, E., Laroche, A., Picard, K., Vecchiarelli, H. A., Savage, J. C., Boilard, É., et al. (2024) · iScience · doi:10.1016/j.isci.2024.110037 · Cited by 5 · see citing works
Self-citation
- Authors
- Tay, T. L., Savage, J. C., Hui, C. W., Bisht, K., & Tremblay, M.
- Affiliations
- University of Freiburg (DE)
- Centre de recherche du CHU de Québec-Université Laval (CA)
- Corresponding author
- Tay, Tuan Leng
- Tremblay, Marie‐Ève
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2016-05-29
- Volume
- 595
- Issue
- 6
- Pages
- 1929-1945
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC5350449
- OpenAlex
- W2340464393
- Cited by
- 562
- References
- 171
- Citations by year
- 2026: 31 · 2025: 55 · 2024: 67 · 2023: 61 · 2022: 71 · 2021: 70 · 2020: 61 · 2019: 65 · 2018: 44 · 2017: 28 · 2016: 8
- FWCI
- 4.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Faculté de Médecine, Université Laval
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- microglia, microglial origin, yolk sac, microglial differentiation, microglial homeostasis, brain development, neuroplasticity, cognition, learning and memory, neuroinflammation, microglial phenotype, sex differences, chronic stress, aging, neuropsychiatric disorders, neurological disorders, microglial depletion
- MeSH terms
- Aging, Animals, Brain, Cognition, Homeostasis, Humans, Microglia
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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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