The DOI matches its Crossref record; 53 of the 53 references it cites were found in a registry or an index.
The origin and cell lineage of microglia: new concepts
Abstract
Despite intense study, the precise origin and cell lineage of microglia, the resident mononuclear phagocytes of the nervous system, are still a matter for debate. Unlike macroglia (astrocytes and oligodendrocytes) and neurons, which are derived from neuroectoderm, microglial progenitors arise from peripheral mesodermal (myeloid) tissue. The view still commonly held is that tissue-resident mononuclear phagocytes (including microglia) are derived from circulating blood monocytes and these take up residence late in gestation and postnatally. However, microglial progenitors colonise the nervous system primarily during embryonic and fetal periods of development. Recent evidence indicates differences between the lineage of mononuclear phagocytes during the embryonic and fetal period from that in the neonate and adult-mononuclear phagocytes that take up residence within tissues are derived from a lineage of myeloid cells that is independent of the monocyte lineage. Our own findings on the development and differentiation of microglial progenitors, taken together with findings by other investigators, and in the context of the heterogeneity between myeloid differentiation in the fetus and in the adult, support the view that microglia are derived prenatally from mesodermal progenitors that are distinct from monocytes. Furthermore, microglial progenitors colonise the nervous system via extravascular routes initially. These findings challenge the concept that resident microglia in the nervous system are derived from circulating blood monocytes. Work is still underway to establish the tissue of origin and lineage of microglial progenitors in vivo. This information is critical not only from a developmental perspective, but significantly from a therapeutic viewpoint, as (i) the unique property of microglial progenitors to colonise the nervous system from the periphery allows these cells to be exploited as a biological and non-invasive means for cell therapy by delivering genes to the nervous system (microglial engraftment), and (ii) there are indications that microglial progenitors are specifically able to home to the nervous system. Use of microglial progenitors for therapeutic purposes becomes feasible only if the origin and cell lineage of these microglial progenitors are known and these cells can be isolated and manipulated in vitro (i.e., to express specific trophic factors) prior to therapeutic transfer (e.g., intravenously) in vivo. In this paper, we shall briefly consider the existing concepts on the origin and lineage of microglial progenitors and discuss new hypotheses in the light of emerging data that suggest clear differences between fetal and adult ontogeny of myeloid cells.
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“Subsequent reports showed that microglia arise early during development from progenitors in the embryonic yolk sac4,38,39.”
From Identification of a unique TGF-β–dependent molecular and functional signature in microglia (2014) · cites this paper as [39]
In the citing paper
“Iba1+/Dab2+ cells resembled the early fetal macrophages previously reported in the developing CNS [35], several of which were found in the proximity of blood vessels at E10.5 (Fig 3D) and E11.5 (Fig 3E).”
From Dynamic expression of Dab2 in the mouse embryonic central nervous system (2008) · cites this paper as [35]
In the citing paper
“these results allude to differences in myeloid cell differentiation (and/or commitment) between macrophages and microglial cells [35]”
From Dynamic expression of Dab2 in the mouse embryonic central nervous system (2008) · cites this paper as [35]
In the citing paper
“PU.1 is an essential factor required for myeloid cell differentiation [35].”
From Dynamic expression of Dab2 in the mouse embryonic central nervous system (2008) · cites this paper as [35]
In the citing paper
“These observations may imply that at least a subpopulation of early microglia (Iba1+/Dab2+) are derived from myeloid progenitors migrating into neural tube via microvessels, rather than derived in situ [35].”
From Dynamic expression of Dab2 in the mouse embryonic central nervous system (2008) · cites this paper as [35]
In the citing paper
“Many of these cytokines are known to be highly elevated in neurological diseases and/or involved in the recruitment of peripheral immune cells into the CNS under pathological conditions”
From iPSC-derived human microglia-like cells to study neurological diseases (2017) · cites this paper as Chan et al., 2007
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BackgroundMicroglia 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
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“Whether murine YS macrophages enter via the blood circulation directly in the brain parenchyma or first enter in the cephalic mesenchyme and then migrate to the neuro-epithelium (Chan et al., 2007) remains to be clearly defined.”
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“Therefore, a new wave of microglia progenitors, which enter the brain from the periphery, is thought to contribute (Chan et al., 2007; Arnold and Betsholtz, 2013; Swinnen et al., 2013).”
BackgroundInfluentialMicroglial Activation in Young Adults With Autism Spectrum Disorder
Suzuki, K., Sugihara, G., Ouchi, Y., Nakamura, K., Futatsubashi, M., Takebayashi, K., Yoshihara, Y., Omata, K., Matsumoto, K., Tsuchiya, K. J., et al. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.272 · Cited by 523
“Under pathologic conditions, however, microglia in neonates and adults are considered to derive from circulating blood monocytes originating primarily within the bone marrow.(50) In brain tissues from children and adults with ASD, macrophage chemoattractant protein-1, which can facilitate the infiltration and accumula…”
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Harry, G. J. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.04.013 · Cited by 524
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Ginhoux, F., & Prinz, M. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020537 · Cited by 446
“The first macrophage-like cells with an amoeboid shape appear in the rodent neuroepithelium at a similar time point (Ashwell 1990; Ashwell and Waite 1991; Chan et al. 2007) and were suggested to be the precursors of microglial cells (Alliot et al.”
BackgroundInfluentialMicroglia: actively surveying and shaping neuronal circuit structure and function
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“In this review, we focus on the positive and negative interactions between oligodendrocytes, astrocytes, and microglia during developmental myelination and remyelination.”
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“These findings support the idea that there is heterogeneity of the microglial cell origins in the CNS, with one population from myeloid/ mesenchymal origin (not necessarily derived from monocytes) and a second population representing a developmental and transitory form of fetal macrophage (possibly monocyte), which is…”
Regulation of microglial activation in stroke
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Mandrekar-Colucci, S., & Landreth, G. E. (2010) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152710791012071 · Cited by 421
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“The Role of Microglia Microglial cells, arising from the mesodermal (myeloid) lineage (42), are the main category of macrophages in the CNS parenchyma.”
BackgroundMicroglia and ischemic stroke: a double-edged sword.
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Microglia Function in Alzheimer’s Disease
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“Many questions remain about the recruitment and the life of the resident microglial in adult and aging brain (Chan et al., 2007).”
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Microglia: gatekeepers of central nervous system immunology
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Features of Microglia and Neuroinflammation Relevant to Environmental Exposure and Neurotoxicity
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Yolk sac macrophage progenitors traffic to the embryo during defined stages of development
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“After several decades of debate as to whether microglia are derived from a single wave of progenitors that enter the CNS only once during development and locally expand and maintain themselves within the CNS throughout an individual’s life, or whether microglial hematopoietic progenitors invade the CNS during early em…”
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“Chan et al. (2007) have suggested that, late in fetal development, when the bone marrow becomes a haematopoietic organ, cells of monocyte lineage may be recruited to the developing central nervous system, to which they may gain entry via the vasculature (specifically within white-matter areas)…”
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Neuroinflammation in Alzheimer’s disease
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“drocytes, they are derived from the neuroectoderm, which is in contrast to microglia.(40) Astrocytes are morphologically heterogeneous.”
ResultMicroglia in the developing brain: a potential target with lifetime effects
Harry, G. J., & Kraft, A. D. (2012) · NeuroToxicology · doi:10.1016/j.neuro.2012.01.012 · Cited by 250
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BackgroundResultInfluentialLysophosphatidic acid (LPA) and its receptors
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“As development proceeds, NPCs sequentially differentiate from peripheral mesodermal tissue [89] and not shown here.”
BackgroundContribution of Microglia‐Mediated Neuroinflammation to Retinal Degenerative Diseases
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“Microglial cells are from mesodermal/mesenchymal origin deriving frommyeloid progenitors thatmigrated from the periphery during late embryonic and postnatal life (reviewed in [9, 22, 23]).”
BackgroundThe hematopoietic stem cell and its niche: a comparative viewPreprint
Martínez-Agosto, J. A., Mikkola, H. K., Hartenstein, V., & Banerjee, U. K. (2007) · Genes & Development · doi:10.1101/gad.1602607 · Cited by 232
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Drowning stars: reassessing the role of astrocytes in brain edema
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“Due to their common myeloid origin during embryogenesis, distinguishing between resident microglia and infiltrating monocytes is highly challenging (Chan et al., 2007).”
BackgroundChen, V. S., Morrison, J. P., Southwell, M. F., Foley, J. F., Bolon, B. N., & Elmore, S. A. (2017) · Toxicologic Pathology · doi:10.1177/0192623317728134 · Cited by 240
“5 (Ginhoux et al. 2010; Rigato et al. 2011; Chan, Kohsaka, and Rezaie 2007; Saijo and Glass 2011).”
BackgroundCazareth, J., Guyon, A., Heurteaux, C., Chabry, J., & Petit-Paitel, A. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-132 · Cited by 206
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Hannestad, J. O., Gallezot, J., Schafbauer, T., Lim, K., Kloczynski, T., Morris, E. D., Carson, R. E., Ding, Y., & Cosgrove, K. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.06.055 · Cited by 218
“When provided with signals indicating tissue damage or inflammation, microglia become activated; this is a key event in the pathophysiology of brain ischemia, trauma, and infection, and in neurodegenerative and autoimmune diseases (Chan et al., 2007; Chen et al., 2010; Tambuyzer et al., 2009).”
BackgroundProliferation of parenchymal microglia is the main source of microgliosis after ischaemic stroke
Li, T., Pang, S., Yu, Y., Wu, X., Guo, J., & Zhang, S. (2013) · Brain · doi:10.1093/brain/awt287 · Cited by 199
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“When provided with signals that indicate tissue damage or infection, microglia become activated, a key event in the initiation and maintenance of neuroinflammation (Chan et al., 2007; Tambuyzer et al., 2009; Chen et al., 2010).”
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The interplay between macrophages and angiogenesis in development, tissue injury and regeneration
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“For instance, it is not clear whether Kupffer cells and microglia originate from adult HSC-derived monocytes or self-renewing, nonHSC-derived macrophage precursors of yolk-sac origin (Chan et al., 2007; Geissmann et al., 2010).”
BackgroundImmune Players in the CNS: The Astrocyte
Jensen, C., Massie, A., & Keyser, J. D. (2013) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-013-9480-6 · Cited by 216
“Like neurons and oligodendrocytes, astrocytes are derived from the neuroectoderm, this is in contrast to the other major cell type in the brain, microglia, which arise from the mesodermal (myeloid) lineage (Chan et al. 2007).”
M1 and M2 immune activation in Parkinson’s Disease: Foe and ally?
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“Microglia were originally thought to derive developmentally from origins similar to that of monocytes and macrophages (Rio-Hortega, 1939; Chan et al., 2007).”
BackgroundMurine models of acute neuronopathic Gaucher disease
Enquist, I. B., Bianco, C. L., Ooka, A., Nilsson, E., Månsson, J., Ehinger, M., Richter, J., Brady, R. O., Kirik, D., & Karlsson, S. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708086104 · Cited by 197
Insights into TREM2 biology by network analysis of human brain gene expression data
Forabosco, P., Ramasamy, A., Trabzuni, D., Walker, R., Smith, C., Bras, J., Levine, A. P., Hardy, J., Pocock, J. M., Guerreiro, R., et al. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.05.001 · Cited by 180
“Furthermore, these findings highlight the unique properties of microglia, as compared to related myeloid cell types, in keeping with their distinct developmental origin (Chan et al., 2007).”
Mazza, M. G., Lucchi, S., Rossetti, A., & Clerici, M. (2020) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2019.1583371 · Cited by 191
“Signal transduction between microglia and circulating monocytes is mediated by pro-inflammatory cytokines, such as IL-1b, IL-6, IL-8 or TNF-a (Chan et al. 2007; Beumer et al. 2012).”
BackgroundEffects of Microglia on Neurogenesis
Sato, K. (2015) · Glia · doi:10.1002/glia.22858 · Cited by 187
“Approximately 50 surface markers that are characteristic of the mononuclear phagocyte lineage have been identified for macrophages, and 35 of these markers are considered useful for discriminating subsets of macrophages and dendritic cells (Chan et al., 2007).”
BackgroundMolecular imaging of microglia/macrophages in the brain
Venneti, S., Lopresti, B. J., & Wiley, C. A. (2012) · Glia · doi:10.1002/glia.22357 · Cited by 194
“…injury by producing a myriad of neurotoxins such as interleukins (Giulian et al., 1986; Righi et al., 1989), tumor necrosis factor-a(Chao et al., 1995b), free radicals (Chao et al., 1995a), nitric oxide (Chao et al., 1992), proteinases (Colton et al., 1993), and eicosanoids (Heyes et al., 1996).”
BackgroundSakuma, R., Kawahara, M., Nakano‐Doi, A., Takahashi, A., Tanaka, Y., Narita, A., Kuwahara‐Otani, S., Hayakawa, T., Yagi, H., Matsuyama, T., et al. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0523-9 · Cited by 184
“The precise origin of microglia has long remained the subject of debate [1, 2].”
Monocyte chemoattractant protein-1 and the blood–brain barrier
Yao, Y., & Tsirka, S. E. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1459-1 · Cited by 182
Toll-Like Receptors in Alzheimer's Disease
Landreth, G. E., & Reed-Geaghan, E. G. (2009) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-00549-7_8 · Cited by 180
“A number of hypotheses exist for the origin of microglia; currently, the consensus is that they are derived from mesodermal/mesenchymal sources in the periphery and infiltrate the brain during development (reviewed in Chan et al. 2007 ).”
BackgroundEarly hematopoiesis and macrophage development
McGrath, K. E., Frame, J. M., & Palis, J. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2016.03.013 · Cited by 172
Functions of microglia in the central nervous system—beyond the immune response
Wake, H., Moorhouse, A. J., & Nabekura, J. (2011) · Neuron Glia Biology · doi:10.1017/s1740925x12000063 · Cited by 167
Ernst, C., Mechawar, N., & Turecki, G. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.09.001 · Cited by 166
“Microglial progenitor cells are derived from mesodermal origins, unlike oligodendrocytes and astrocytes which are derived from ectodermal origins (Chan et al., 2007).”
Guruswamy, R., & ElAli, A. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18030496 · Cited by 166
“Different possible origins have been proposed; some have proposed that microglia are derived from progenitors that originate from the neuroectoderm and/or the mesoderm colonizing the brain at the early embryonic stage throughout the fetal development stage [16–18], while others have proposed that microglia are derived…”
BackgroundMicroglia and neuronal cell death
Marín‐Teva, J. L., Cuadros, M. Á., Martín‐Oliva, D., & Navascués, J. (2011) · Neuron Glia Biology · doi:10.1017/s1740925x12000014 · Cited by 158
Jacome-Galarza, C. E., Lee, S., Lorenzo, J., & Aguila, H. L. (2012) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1822 · Cited by 160
Immune privilege or privileged immunity?
Forrester, J. V., Xu, H., Lambe, T., & Cornall, R. J. (2008) · Mucosal Immunology · doi:10.1038/mi.2008.27 · Cited by 161
Immunoadolescence: Neuroimmune development and adolescent behavior
Brenhouse, H. C., & Schwarz, J. M. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.035 · Cited by 163
“…M anuscript Microglial cells are of mesodermal lineage (similar to other immune cells) and they first colonize the developing rodent brain around embryonic day (E) 9-10 via the infiltration of primitive macrophage precursors from the yolk sac of the embryo (Chan et al., 2007, Ginhoux et al., 2010).”
BackgroundWard, R. J., Crichton, R. R., Taylor, D. L., Corte, L., Srai, S. K., & Dexter, D. T. (2010) · Journal of Neural Transmission · doi:10.1007/s00702-010-0479-3 · Cited by 150
“It is thought that microglia originate from circulating monocytes or precursor cells that colonise the nervous system primarily during embryonic and foetal periods of development (reviewed by Chan et al. 2007 ).”
BackgroundThe importance of microglia in the development of the vasculature in the central nervous system
Arnold, T., & Betsholtz, C. (2013) · Vascular Cell · doi:10.1186/2045-824x-5-4 · Cited by 157
“Notably, microglia populate the embryonic retina well before post-natal retinal angiogenesis occurs [16,31,32], and as mentioned above appear to colonize zebrafish and chick brains before CNS vascular invasion [11-13].”
Sorrentino, F. S., Allkabes, M., Salsini, G., Bonifazzi, C., & Perri, P. (2016) · Life Sciences · doi:10.1016/j.lfs.2016.08.001 · Cited by 150
“They origin from mesoderma/mesenchima deriving from myeloid progenitors that migrate from periphery during the late embriogenic and postnatal life [58-60].”
Progranulin expression in the developing and adult murine brain
Petkau, T. L., Neal, S. J., Orban, P. C., MacDonald, J. L., Hill, A. M., Lu, G., Feldman, H. H., Mackenzie, I. R. A., & Leavitt, B. R. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22430 · Cited by 152
“Microglia originate as myeloid cells in the spleen, which differentiate into monocytes and infiltrate the CNS during late embryogenesis (Chan et al., 2007).”
BackgroundBone-marrow-derived microglia: myth or reality?
Soulet, D., & Rivest, S. (2008) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.04.002 · Cited by 139
Axon Initial Segment–Associated Microglia
Baalman, K., Marin, M. A., Ho, T., Godoy, M. I., Cherian, L., Robertson, C., & Rasband, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3751-14.2015 · Cited by 129
“5; Chan et al., 2007; Ginhoux et al., 2010), they are relatively sparse until postnatal day 7 (P7)–P9, when microglia proliferate and undergo rapid local expansion (Hristova et al., 2010).”
BackgroundDynamics and regulation of lipid droplet formation in lipopolysaccharide (LPS)-stimulated microglia
Khatchadourian, A., Bourque, S. D., Richard, V. R., Titorenko, V. I., & Maysinger, D. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2012.01.007 · Cited by 143
“Upon activationmicroglia express cell surface markers that are also present on macrophages [23].”
BackgroundAstrocytic Mechanisms Explaining Neural-Activity-Induced Shrinkage of Extraneuronal Space
Østby, I., Øyehaug, L., Einevoll, G. T., Nagelhus, E. A., Plahte, E., Zeuthen, T., Lloyd, C. M., Ottersen, O. P., & Omholt, S. W. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000272 · Cited by 136
“These cells constitute the most abundant type of macroglia in the brain [2].”
BackgroundMicroglia in Alzheimer’s disease: A multifaceted relationship
ElAli, A., & Rivest, S. (2016) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.07.021 · Cited by 134
“In addition, it has been proposed that microglia are derived from circulating blood monocytes, especially from the late gestational stage throughout the early postnatal stage (Chan et al., 2007).”
BackgroundReciprocal Modulation Between Microglia and Astrocyte in Reactive Gliosis Following the CNS Injury
Gao, Z., Zhu, Q., Zhang, Y., Zhao, Y., Cai, L., Shields, C. B., & Cai, J. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8460-4 · Cited by 148
“cantly detected within the superficial mantle layer of the spinal cord as well as the subventricular zone in the brain [12].”
Schwartz, M., & Shechter, R. (2010) · Molecular Psychiatry · doi:10.1038/mp.2010.31 · Cited by 129
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
“It is now clear that yolk sac macrophages colonize the brain at around Day 10 of the developing embryo and serve as precursors of the major resident microglia population of the adult mouse (Chan et al., 2007; Ginhoux et al., 2010).”
BackgroundNeurodegeneration and Neuro-Regeneration—Alzheimer’s Disease and Stem Cell Therapy
Vasić, V., Barth, K., & Schmidt, M. H. H. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20174272 · Cited by 129
“Microglia are the brain’s resident macrophages arising from the mesenchyme [9], or are blood-derived (review, see [10]).”
BackgroundMicroglia in development: linking brain wiring to brain environment
Paolicelli, R. C., & Gross, C. T. (2011) · Neuron Glia Biology · doi:10.1017/s1740925x12000105 · Cited by 129
Tracking neuroinflammation in Alzheimer’s disease: the role of positron emission tomography imaging
Zimmer, E. R., Leuzy, A., Benedet, A. L., Breitner, J., Gauthier, S., & Rosa-Neto, P. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-120 · Cited by 121
“Under pathological conditions, microglial cells proliferate and migrate to the site of injury, acquiring phagocytic abilities and releasing various pro-inflammatory mediators [47-50].”
BackgroundThe microglia in healthy and diseased retina
Li, L., Eter, N., & Heiduschka, P. (2015) · Experimental Eye Research · doi:10.1016/j.exer.2015.04.020 · Cited by 112
Lee, D. C., Ruiz, C. R., Lebson, L. A., Selenica, M. B., Rizer, J., Hunt, J. B., Rojiani, R., Reid, P., Kammath, S., Nash, K. R., et al. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.12.014 · Cited by 122
“Microglia are typically viewed as tissue macrophages of the central nervous system, although their embryonic origin may be different from circulating monocytes (Chan et al., 2007, Ginhoux et al., 2010, Prinz et al., 2011, Ransohoff and Cardona, 2010).”
Microglia-specific targeting by novel capsid-modified AAV6 vectors
Rosario, A. M., Cruz, P. E., Ceballos‐Diaz, C., Strickland, M. R., Siemienski, Z. B., Pardo, M., Schob, K.-L., Li, A., Aslanidi, G., Srivastava, A., et al. (2016) · Molecular Therapy — Methods & Clinical Development · doi:10.1038/mtm.2016.26 · Cited by 120
Linnartz‐Gerlach, B., & Neumann, H. (2012) · Glia · doi:10.1002/glia.22359 · Cited by 117
“precursors locally proliferate within the CNS and mature to become adult microglia (Chan et al., 2007).”
BackgroundKofler, J., & Wiley, C. A. (2010) · Toxicologic Pathology · doi:10.1177/0192623310387619 · Cited by 122
“Current evidence suggests that in mammals, early microglia are derived from yolk-sac progenitors that migrate into the CNS around the second trimester (Ransohoff and Perry 2009; Chan, Kohsaka, and Rezaie 2007).”
Ly6Chigh Monocytes Control Cerebral Toxoplasmosis
Biswas, A., Bruder, D., Wolf, S. A., Jeron, A., Mack, M., Heimesaat, M. M., & Dunay, I. R. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402037 · Cited by 115
“50 characteristic surface markers, making their discrimination between the subpopulations a complex assignment (45, 46).”
Background
Metadata
- Authors
- Chan, W. Y., Kohsaka, S., & Rezaie, P.
- Affiliations
- Chinese University of Hong Kong (HK)
- National Institute of Neuroscience (JP)
- King's College London (GB)
- Venue
- Brain Research Reviews
- Publisher
- Elsevier BV
- Published
- 2007-02
- Volume
- 53
- Issue
- 2
- Pages
- 344-354
- ISSN
- 0165-0173 (ISSN-L)
- OpenAlex
- W2087954391
- Cited by
- 400
- References
- 53
- Citations by year
- 2026: 6 · 2025: 9 · 2024: 8 · 2023: 13 · 2022: 15 · 2021: 19 · 2020: 17 · 2019: 10 · 2018: 13 · 2017: 19 · 2016: 23 · 2015: 28 · 2014: 32 · 2013: 41 · 2012: 38
- FWCI
- 2.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research Reviews (publishedVersion)
- PubMed (publishedVersion)
- Open Research Online - ORO (The Open University) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Keywords
- microglia, cell lineage, embryonic and fetal development, cell therapy, trophic factors, brain development, trophoblast
- MeSH terms
- Animals, Cell Differentiation, Humans, Models, Biological, Stem Cells, Microglia, Cell Lineage
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