Talk:Neural System - Glial Development

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Cite this page: Hill, M.A. (2020, January 23) Embryology Neural System - Glial Development. Retrieved from



Grassivaro F, Menon R, Acquaviva M, Ottoboni L, Ruffini F, Bergamaschi A, Muzio L, Farina C & Martino G. (2019). Convergence between microglia and peripheral macrophages phenotype during development and neuroinflammation. J. Neurosci. , , . PMID: 31818979 DOI. Convergence between microglia and peripheral macrophages phenotype during development and neuroinflammation.

Abstract Differently, from other myeloid cells, microglia derive exclusively from precursors originating within the yolk sac (YS) and migrating to the central nervous system (CNS) under development, without any contribution from fetal liver or postnatal hematopoiesis. Consistent with their unique ontology, microglia may express specific physiological markers, which have been partly described in recent years. Here we wondered whether profiles distinguishing microglia from peripheral macrophages vary with age and under pathology. To this goal, we profiled transcriptomes of microglia throughout the lifespan and included a parallel comparison with peripheral macrophages under physiological and neuroinflammatory settings using age and sex-matched wild type and bone marrow chimera mouse models. This comprehensive approach demonstrated that the phenotypic differentiation between microglia and peripheral macrophages is age-dependent and that peripheral macrophages do express some of the most commonly described microglia-specific markers early during development, such as Fcrls, P2ry12, Tmem119, and Trem2. Further, during chronic neuroinflammation CNS-infiltrating macrophages and not peripheral myeloid cells acquire microglial markers, indicating that the CNS niche may instruct peripheral myeloid cells to gain the phenotype and, presumably, the function of the microglia cell. In conclusion, our data provide further evidence about the plasticity of the myeloid cell and suggest caution in the strict definition and application of microglia-specific markers.Significant StatementUnderstanding the respective role of microglia and infiltrating monocytes in neuroinflammatory conditions has recently seemed possible by the identification of a specific microglia signature. Here instead we provide evidence that peripheral macrophages may express some of the most commonly described microglia markers at some developmental stages or pathological conditions, in particular during chronic neuroinflammation. Further, our data support the hypothesis about phenotypic plasticity and convergence among distinct myeloid cells so that they may act as a functional unit rather than as different entities, boosting their mutual functions in different phases of disease. This holds relevant implications in the view of the growing use of myeloid cell therapies to treat brain disease in humans. Copyright © 2019 the authors. KEYWORDS: Development; EAE; Macrophages; Microglia; Plasticity; Tissue-reprogramming PMID: 31818979 DOI: 10.1523/JNEUROSCI.1523-19.2019


TGFβ-Signaling and FOXG1-Expression Are a Hallmark of Astrocyte Lineage Diversity in the Murine Ventral and Dorsal Forebrain

Front Cell Neurosci. 2018 Nov 28;12:448. doi: 10.3389/fncel.2018.00448. eCollection 2018.

Weise SC1,2,3, Villarreal A1, Heidrich S1, Dehghanian F1,4, Schachtrup C1, Nestel S3, Schwarz J5,6, Thedieck K7,8, Vogel T1. Author information Abstract Heterogeneous astrocyte populations are defined by diversity in cellular environment, progenitor identity or function. Yet, little is known about the extent of the heterogeneity and how this diversity is acquired during development. To investigate the impact of TGF (transforming growth factor) β-signaling on astrocyte development in the telencephalon we deleted the TGFBR2 (transforming growth factor beta receptor 2) in early neural progenitor cells in mice using a FOXG1 (forkhead box G1)-driven CRE-recombinase. We used quantitative proteomics to characterize TGFBR2-deficient cells derived from the mouse telencephalon and identified differential protein expression of the astrocyte proteins GFAP (glial fibrillary acidic protein) and MFGE8 (milk fat globule-EGF factor 8). Biochemical and histological investigations revealed distinct populations of astrocytes in the dorsal and ventral telencephalon marked by GFAP or MFGE8 protein expression. The two subtypes differed in their response to TGFβ-signaling. Impaired TGFβ-signaling affected numbers of GFAP astrocytes in the ventral telencephalon. In contrast, TGFβ reduced MFGE8-expression in astrocytes deriving from both regions. Additionally, lineage tracing revealed that both GFAP and MFGE8 astrocyte subtypes derived partly from FOXG1-expressing neural precursor cells.

KEYWORDS: SILAC; Tgfbr2 knockout; astrocyte-diversity; lineage-tracing; neural differentiation PMID: 30555301 PMCID: PMC6282056 DOI: 10.3389/fncel.2018.00448

Microglia and early brain development: An intimate journey

Science. 2018 Oct 12;362(6411):185-189. doi: 10.1126/science.aat0474.

Thion MS1, Ginhoux F2,3, Garel S1. Author information Abstract Cross-talk between the nervous and immune systems has been well described in the context of adult physiology and disease. Recent advances in our understanding of immune cell ontogeny have revealed a notable interplay between neurons and microglia during the prenatal and postnatal emergence of functional circuits. This Review focuses on the brain, where the early symbiotic relationship between microglia and neuronal cells critically regulates wiring, contributes to sex-specific differences in neural circuits, and relays crucial information from the periphery, including signals derived from the microbiota. These observations underscore the importance of studying neurodevelopment as part of a broader framework that considers nervous system interactions with microglia in a whole-body context.

Copyright © 2018, American Association for the Advancement of Science.

PMID: 30309946 DOI: 10.1126/science.aat0474

Strong sonic hedgehog signaling in the mouse ventral spinal cord is not required for oligodendrocyte precursor cell (OPC) generation but is necessary for correct timing of its generation

Neurochem Int. 2018 Oct;119:178-183. doi: 10.1016/j.neuint.2017.11.003. Epub 2017 Nov 6.

Hashimoto H1, Jiang W1, Yoshimura T1, Moon KH2, Bok J3, Ikenaka K4.


In the mouse neural tube, sonic hedgehog (Shh) secreted from the floor plate (FP) and the notochord (NC) regulates ventral patterning of the neural tube, and later is essential for the generation of oligodendrocyte precursor cells (OPCs). During early development, the NC is adjacent to the neural tube and induces ventral domains in it, including the FP. In the later stage of development, during gliogenesis in the spinal cord, the pMN domain receives strong Shh signaling input. While this is considered to be essential for the generation of OPCs, the actual role of this strong input in OPC generation remains unclear. Here we studied OPC generation in bromi mutant mice which show abnormal ciliary structure. Shh signaling occurs within cilia and has been reported to be weak in bromi mutants. At E11.5, accumulation of Patched1 mRNA, a Shh signaling reporter, is observed in the pMN domain of wild type but not bromi mutants, whereas expression of Gli1 mRNA, another Shh reporter, disappeared. Thus, Shh signaling input to the pMN domain at E12.5 was reduced in bromi mutant mice. In these mutants, induction of the FP structure was delayed and its size was reduced compared to wild type mice. Furthermore, while the p3 and pMN domains were induced, the length of the Nkx2.2-positive region and the number of Olig2-positive cells decreased. The number of OPCs was also significantly decreased in the E12.5 and E14.5 bromi mutant spinal cord. In contrast, motor neuron (MN) production, detected by HB9 expression, significantly increased. It is likely that the transition from MN production to OPC generation in the pMN domain is impaired in bromi mutant mice. These results suggest that strong Shh input to the pMN domain is not required for OPC generation but is essential for producing a sufficient number of OPCs. KEYWORDS: Bromi; Embryonic spinal cord; Floor plate; Oligodendrocyte; Sonic hedgehog signaling PMID: 29122585 DOI: 10.1016/j.neuint.2017.11.003


Radial glial cells: key organisers in CNS development

Int J Biochem Cell Biol. 2014 Jan;46:76-9. doi: 10.1016/j.biocel.2013.11.013. Epub 2013 Nov 21.

Barry DS1, Pakan JM2, McDermott KW2.

Abstract Radial glia are elongated bipolar cells present in the CNS during development. Our understanding of the unique roles these cells play has significantly expanded in the last decade. Historically, radial glial cells were primarily thought to provide an architectural framework for neuronal migration. Recent research reveals that radial glia play a more dynamic and integrated role in the development of the brain and spinal cord. They represent a major progenitor pool during early development and can give rise to a small population of multipotent cells in neurogenic niches of the adult CNS. Radial glial cells are a heterogeneous population, with divergent and often poorly understood roles across different brain and spinal cord regions during development; this heterogeneity extends to specialised adult subtypes, such as tanycytes, Müller glial cells and Bergman glial cells which possess morphological similarities to radial glial but play distinct functional roles in the CNS. Copyright © 2013 Elsevier Ltd. All rights reserved. KEYWORDS: Glioma; Neurodevelopment; Neuronal migration; Radial glia PMID 24269781

Stem cell factor Sox2 and its close relative Sox3 have differentiation functions in oligodendrocytes

Development. 2014 Jan;141(1):39-50. doi: 10.1242/dev.098418. Epub 2013 Nov 20.

Hoffmann SA1, Hos D, Küspert M, Lang RA, Lovell-Badge R, Wegner M, Reiprich S.


Neural precursor cells of the ventricular zone give rise to all neurons and glia of the central nervous system and rely for maintenance of their precursor characteristics on the closely related SoxB1 transcription factors Sox1, Sox2 and Sox3. We show in mouse spinal cord that, whereas SoxB1 proteins are usually downregulated upon neuronal specification, they continue to be expressed in glial precursors. In the oligodendrocyte lineage, Sox2 and Sox3 remain present into the early phases of terminal differentiation. Surprisingly, their deletion does not alter precursor characteristics but interferes with proper differentiation. Although a direct influence on myelin gene expression may be part of their function, we provide evidence for another mode of action. SoxB1 proteins promote oligodendrocyte differentiation in part by negatively controlling miR145 and thereby preventing this microRNA from inhibiting several pro-differentiation factors. This study presents one of the few cases in which SoxB1 proteins, including the stem cell factor Sox2, are associated with differentiation rather than precursor functions. KEYWORDS: Glia; High mobility group; MicroRNA; Myelin; Transcriptional control

PMID 24257626


Sox10 is required for Schwann cell identity and progression beyond the immature Schwann cell stage

J Cell Biol. 2010 May 17;189(4):701-12. Epub 2010 May 10.

Finzsch M, Schreiner S, Kichko T, Reeh P, Tamm ER, Bösl MR, Meijer D, Wegner M.

Institut für Biochemie, Emil-Fischer-Zentrum, Universität Erlangen-Nürnberg, 91054 Erlangen, Germany.

Abstract Mutations in the transcription factor SOX10 cause neurocristopathies, including Waardenburg-Hirschsprung syndrome and peripheral neuropathies in humans. This is partly attributed to a requirement for Sox10 in early neural crest for survival, maintenance of pluripotency, and specification to several cell lineages, including peripheral glia. As a consequence, peripheral glia are absent in Sox10-deficient mice. Intriguingly, Sox10 continues to be expressed in these cells after specification. To analyze glial functions after specification, we specifically deleted Sox10 in immature Schwann cells by conditional mutagenesis. Mutant mice died from peripheral neuropathy before the seventh postnatal week. Nerve alterations included a thinned perineurial sheath, increased lipid and collagen deposition, and a dramatically altered cellular composition. Nerve conduction was also grossly aberrant, and neither myelinating nor nonmyelinating Schwann cells formed. Instead, axons of different sizes remained unsorted in large bundles. Schwann cells failed to develop beyond the immature stage and were unable to maintain identity. Thus, our study identifies a novel cause for peripheral neuropathies in patients with SOX10 mutations.

PMID 20457761


Growth of the human corpus callosum: modular and laminar morphogenetic zones

Front Neuroanat. 2009;3:6. Epub 2009 Jun 9.

Jovanov-Milosević N, Culjat M, Kostović I.

Croatian Institute for Brain Research, School of Medicine, University of Zagreb Zagreb, Croatia. Abstract The purpose of this focused review is to present and discuss recent data on the changing organization of cerebral midline structures that support the growth and development of the largest commissure in humans, the corpus callosum. We will put an emphasis on the callosal growth during the period between 20 and 45 postconceptual weeks (PCW) and focus on the advantages of a correlated histological/magnetic resonance imaging (MRI) approach. The midline structures that mediate development of the corpus callosum in rodents, also mediate its early growth in humans. However, later phases of callosal growth in humans show additional medial transient structures: grooves made up of callosal septa and the subcallosal zone. These modular (septa) and laminar (subcallosal zone) structures enable the growth of axons along the ventral callosal tier after 18 PCW, during the rapid increase in size of the callosal midsagittal cross-section area. Glial fibrillary acidic protein positive cells, neurons, guidance molecule semaphorin3A in cells and extracellular matrix (ECM), and chondroitin sulfate proteoglycan in the ECM have been identified along the ventral callosal tier in the protruding septa and subcallosal zone. Postmortem MRI at 3 T can demonstrate transient structures based on higher water content in ECM, and give us the possibility to follow the growth of the corpus callosum in vivo, due to the characteristic MR signal. Knowledge about structural properties of midline morphogenetic structures may facilitate analysis of the development of interhemispheric connections in the normal and abnormal fetal human brain.

PMID: 19562029

Cell migration in the normal and pathological postnatal mammalian brain


Integrin-mediated axoglial interactions initiate myelination in the central nervous system

J Cell Biol. 2009 May 18;185(4):699-712.

Câmara J, Wang Z, Nunes-Fonseca C, Friedman HC, Grove M, Sherman DL, Komiyama NH, Grant SG, Brophy PJ, Peterson A, ffrench-Constant C.

Department of Pathology, University of Cambridge, Cambridge CB2 1QP, England, UK. Abstract

All but the smallest-diameter axons in the central nervous system are myelinated, but the signals that initiate myelination are unknown. Our prior work has shown that integrin signaling forms part of the cell-cell interactions that ensure only those oligodendrocytes contacting axons survive. Here, therefore, we have asked whether integrins regulate the interactions that lead to myelination. Using homologous recombination to insert a single-copy transgene into the hypoxanthine phosphoribosyl transferase (hprt) locus, we find that mice expressing a dominant-negative beta1 integrin in myelinating oligodendrocytes require a larger axon diameter to initiate timely myelination. Mice with a conditional deletion of focal adhesion kinase (a signaling molecule activated by integrins) exhibit a similar phenotype. Conversely, transgenic mice expressing dominant-negative beta3 integrin in oligodendrocytes display no myelination abnormalities. We conclude that beta1 integrin plays a key role in the axoglial interactions that sense axon size and initiate myelination, such that loss of integrin signaling leads to a delay in myelination of small-diameter axons.

PMID: 19451276

The contributions of Santiago Ramón y Cajal to cancer research — 100 years on


J Anat. 2005 Sep;207(3):241-50. Role of radial glia in cytogenesis, patterning and boundary formation in the developing spinal cord. McDermott KW1, Barry DS, McMahon SS. Author information Abstract Radial glial fibres provide a transient scaffold and impose constraints in the developing central nervous system (CNS) that facilitate cell migration and axon growth. Recent reports have raised doubts about the distinction between radial glia and precursor cells by demonstrating that radial glia are themselves neuronal progenitor cells in the developing cortex, indicating a dual role for radial glia in both neurogenesis and migration guidance. Radial glia shift toward exclusive generation of astrocytes after neurogenesis has ceased. Radial progenitor cell differentiation and lineage relationships in CNS development are complex processes depending on genetic programming, cell-cell interaction and microenvironmental factors. In the spinal cord, radial cells that arise directly from the neuroepithelium have been identified. At least in the spinal cord, these radial cells appear to be the precursors to radial glia. It remains unknown whether radial glial cells or their precursors, the radial cells, or both can give rise to neurons in the spinal cord. Radial glial cells are also important in regulating the axon out-growth and pathfinding processes that occur during white matter patterning of the developing spinal cord. PMID 16185248


Progressive loss of PAX6, TBR2, NEUROD and TBR1 mRNA gradients correlates with translocation of EMX2 to the cortical plate during human cortical development

Eur J Neurosci. 2008 Oct;28(8):1449-56.

Bayatti N, Sarma S, Shaw C, Eyre JA, Vouyiouklis DA, Lindsay S, Clowry GJ.

Institute of Neuroscience, Newcastle University, Newcastle-upon-Tyne, UK. Abstract The transcription factors Emx2 and Pax6 are expressed in the proliferating zones of the developing rodent neocortex, and gradients of expression interact in specifying caudal and rostral identities. Pax6 is also involved in corticoneurogenesis, being expressed by radial glial progenitors that give rise to cells that also sequentially express Tbr2, NeuroD and Tbr1, genes temporally downstream of Pax6. In this study, using in situ hybridization, we analysed the expression of EMX2, PAX6, TBR2, NEUROD and TBR1 mRNA in the developing human cortex between 8 and 12 postconceptional weeks (PCW). EMX2 mRNA was expressed in the ventricular (VZ) and subventricular zones (SVZ), but also in the cortical plate, unlike in the rodent. However, gradients of expression were similar to that of the rodent at all ages studied. PAX6 mRNA expression was limited to the VZ and SVZ. At 8 PCW, PAX6 was highly expressed rostrally but less so caudally, as has been seen in the rodent, however this gradient disappeared early in corticogenesis, by 9 PCW. There was less restricted compartment-specific expression of TBR2, NEUROD and TBR1 mRNA than in the rodent, where the gradients of expression were similar to that of PAX6 prior to 9 PCW. The gradient disappeared for TBR2 by 10 PCW, and for NEUROD and TBR1 by 12 PCW. These data support recent reports that EMX2 but not PAX6 is more directly involved in arealization, highlighting that analysis of human development allows better spatio-temporal resolution than studies in rodents.


Role of radial glia in cytogenesis, patterning and boundary formation in the developing spinal cord

J Anat. 2005 Sep;207(3):241-50.

McDermott KW1, Barry DS, McMahon SS.


Radial glial fibres provide a transient scaffold and impose constraints in the developing central nervous system (CNS) that facilitate cell migration and axon growth. Recent reports have raised doubts about the distinction between radial glia and precursor cells by demonstrating that radial glia are themselves neuronal progenitor cells in the developing cortex, indicating a dual role for radial glia in both neurogenesis and migration guidance. Radial glia shift toward exclusive generation of astrocytes after neurogenesis has ceased. Radial progenitor cell differentiation and lineage relationships in CNS development are complex processes depending on genetic programming, cell-cell interaction and microenvironmental factors. In the spinal cord, radial cells that arise directly from the neuroepithelium have been identified. At least in the spinal cord, these radial cells appear to be the precursors to radial glia. It remains unknown whether radial glial cells or their precursors, the radial cells, or both can give rise to neurons in the spinal cord. Radial glial cells are also important in regulating the axon out-growth and pathfinding processes that occur during white matter patterning of the developing spinal cord. PMID: 16185248


Radial glia: multi-purpose cells for vertebrate brain development

Trends Neurosci. 2002 May;25(5):235-8.

Campbell K1, Götz M.


Radial glia are specialized cells in the developing nervous system of all vertebrates, and are characterized by long radial processes. These processes facilitate the best known function of radial glia: guiding the radial migration of newborn neurons from the ventricular zone to the mantle regions. Recent data indicate further important roles for these cells as ubiquitous precursors that generate neurons and glia, and as key elements in patterning and region-specific differentiation of the CNS. Thus, from being regarded mainly as support cells, radial glia have emerged as multi-purpose cells involved in most aspects of brain development. PMID 11972958


Patterns of glial development in the human foetal spinal cord during the late first and second trimester

J Neurocytol. 1994 Jun;23(6):343-53.

Weidenheim KM, Epshteyn I, Rashbaum WK, Lyman WD.

Department of Pathology (Neuropathology), Albert Einstein College of Medicine, Bronx, New York. Abstract

Although the presence of radial glia, astrocytes, oligodendrocytes and microglia has been reported in the human foetal spinal cord by ten gestational weeks, neuroanatomic studies employing molecular probes that describe the interrelated development of these cells from the late first trimester through the late second trimester are few. In this study, immunocytochemical methods using antibodies to vimentin and glial fibrillary acidic protein were used to identify radial glial and/or astrocytes. An antibody to myelin basic protein was used for oligodendrocytes and myelin; and, an antibody to phosphorylated high and medium molecular weight neurofilaments identified axons. Lectin histochemistry using Ricinus communis agglutinin-I was employed to identify microglia. Vibratome sections from 35 human foetal spinal cord ranging in age from 9-20 gestation weeks were studied. By 12 gestational weeks, vimentin-positive radial glia were present at all three levels of the spinal cord. Their processes were easily identified in the dorsal two-thirds of cord sections, and reaction product for vimentin was more intense at cervical and thoracic levels than lumbosacral sections. By 15 gestational weeks, vimentin-positive processes were radially arranged in the white matter. At this time, glial fibrillary acidic protein-positive astrocytes were more obvious in both the anterior and anterolateral funiculi than in the dorsal funiculus, and the same rostral to caudal gradient was seen for glial fibrillary acidic protein as it was for vimentin. Myelin basic protein expression followed similar temporal and spatial patterns. Ricinus communis agglutinin-I labelling revealed more microglia in the white matter than in grey matter throughout the spinal cord from 10-20 gestational weeks. By 20 gestational weeks, the gradients of glial fibrillary acidic protein and vimentin expression were more difficult to discern. White matter contained more microglia than grey matter. These results suggest that astrocytes as well as oligodendrocytes follow anterior-to-posterior and rostral-to-caudal developmental patterns in the human foetus during middle trimester development.

12 gestational weeks - vimentin-positive radial glia 15 gestational weeks - vimentin-positive processes were radially arranged in the white matter. 20 gestational weeks - gradients of glial fibrillary acidic protein and vimentin expression were more difficult to discern.

PMID: 7522270


Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain

Brain Res Dev Brain Res. 1999 Nov 18;117(2):145-52.

Alliot F1, Godin I, Pessac B.


Microglia, the resident CNS macrophages, represent about 10% of the adult brain cell population. Although described a long time ago, their origin and developmental lineage is still debated. While del Rio-Hortega suggested that microglia originate from meningeal macrophages penetrating the brain during embryonic development, many authors claim that brain parenchymal microglia derive from circulating blood monocytes originating from bone marrow. We have previously reported that the late embryonic and adult mouse brain parenchyma contains potential microglial progenitors [F. Alliot, E. Lecain, B. Grima, B. Pessac, Microglial progenitors with a high proliferative capacity in the embryonic and the adult mouse brain, Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 1541-1545]. We now report that they can be detected in the brain rudiment from embryonic day 8, after their appearance in the yolk sac and that their number increases until late gestation. We also show that microglia appear during embryonic development and that their number increases steadily during the first two postnatal weeks, when about 95% of microglia are born. Finally, the main finding of this study is that microglia is the result of in situ proliferation, as shown by the high proportion of parenchymal microglial cells that express PCNA, a marker of cell multiplication, in embryonic and postnatal brain. Taken together, our data support the hypothesis that terminally differentiated brain parenchymal microglia are derived from cells originating from the yolk sac whose progeny actively proliferates in situ during development.

PMID 10567732


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