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WIREs Dev Biol
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The early life of a fly glial cell

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Throughout evolution, glia have key regulatory roles in neural development and function. Typically, they control the response to developmental and/or pathological signals, thereby affecting neural proliferation, remodeling, survival, and regeneration. Such complex biology depends on the plastic features of glial cells, but also on the presence of different classes of glial cells, hence the importance of understanding the cellular and the molecular mechanisms underlying their development. The fly community has made major breakthroughs by characterizing the bases of gliogenesis and here we describe the glial lineages as well as the glial promoting factor active in the embryo of Drosophila melanogaster. WIREs Dev Biol 2016, 5:67–84. doi: 10.1002/wdev.200 This article is categorized under: Gene Expression and Transcriptional Hierarchies > Cellular Differentiation Invertebrate Organogenesis > Flies Nervous System Development > Flies
Neurogenic fate map. Schematic representation of the fatemap of a stage 5 (gastrula stage) embryo in lateral view (anterior to the left, dorsal to the top). The neurogenic regions are shown in blue. In each thoracic and abdominal segment, 31 neural precursor cells delaminate on each side of the ventral midline (broken line). They divide in a stem cell mode budding off a smaller ganglion mother cell (GMC) with each division. According to the identity of each precursor, a stereotyped lineage of neurons and/or glial cells is produced [neuroblast (NB) 5‐6 is shown as an example]. For details see text.
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Gcm genes in evolution. Phylogenetic tree of Gcm genes constructed using clustalw (NJ algorithm) with the protein sequences from the following species: Homo sapiens (Hsa), Mus musculus (Mmu), Danio rerio (Dre), and Drosophila melanogaster (Dme). Scale: nucleotide substitution per 100 residues.
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Downstream targets of Gcm. The annotations in gray show the GO‐term associated with the genes identified as downstream targets of Gcm. Straight lines indicate direct targets, dashed lines indicate targets that may be direct or indirect. The direct targets of Repo were identified by ChIP, the list of indirect targets of Gcm on the bottom left part were identified in two genome‐wide screen done by microarray.
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Gcm determines the glial fate in neural stem cells. (a) Immunolabeling of glial cells (anti‐Repo) in Drosophila embryos of the following genotypes: wild type (gcm WT), loss of function for Gcm (gcm LOF, null mutant), gain of function for Gcm (gcm GOF, Gcm ectopic expression). Note the absence of Repo labeling in the gcm LOF embryo and the supernumerary Repo‐positive cells in the gcm GOF embryo. (b) Schematic representation of neural stem cell differentiation in the different animals: in gcm WT the precursors give rise to neurons and glia, in gcm LOF, the precursors only produce neurons and in the gcm GOF, the precursors only produce glia.
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Transcription factors binding map on the gcm promoter. (a) The gcm locus is on the antisense strand of the chromosome 2 (in blue). The promoter of gcm contains canonical Gc‐Binding Sites (GBS in red), canonical Repo Binding Sites confirmed by ChIP (RBS in black), Pros, Dpn, Ase, and Sna binding sites determined by DAM‐ID (in green) and regions bound by positional and temporal genes determined by ChIP (in orange). (b) Schematic representation of the regulation of the levels of Gcm (in red) and Repo (in blue). The arrows represent induction of transcription of gcm and repo, including the feedback and autoregulatory loops; the blunted line from Repo to Gcm represents the proteasome‐mediated degradation of Gcm enhanced by Repo. The initial induction of Gcm mostly relies on transcriptional regulation where the late regulatory phase is mainly posttranslational. Note that the transient expression of the glial fate determinant depends on a feed forward loop triggered by Gcm itself. The x‐axis indicates time and the progression from multipotent, stem cells to glia; the y‐axis indicates the levels of Gcm and Repo proteins on an arbitrary scale.
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Neuroglioblast (NGB) map and glial classes. Neuroblast (NB) map of one hemisegment of the trunk with NGBs/glioblasts (GBs) highlighted. Glial cell nomenclature and class affiliation according to Ref and Refs and . Anterior to the top, dashed line represents the ventral midline.
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Glial layers of a larval peripheral nerve. Schematic drawing of a peripheral nerve (cross section) at third larval stage. Axons (gray) are enwrapped by wrapping glia (blue). Subperineurial glia (green) build the blood–nerve barrier and seal intercellular and intracellular connections via septate junctions. The outermost sheath is formed by perineurial glia (red) and the neurilemma.
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Type 3 neuroglioblast (NGB) lineages. Neuroblast (NB) 6‐4T produces a neuronal and a glial precursor at its first division, the latter generating three cortex‐associated glia. NB 6‐4A and the longitudinal glioblast (LGB) produce pure gliogenic lineages. The complete cell clones are shown on the left column (dorsal view, anterior to the top) and the generated glial cells are highlighted on the right side in a dorsal (anterior to the top, including one peripheral nervous system hemisegment) and a frontal view. Color code of glial cells as above.
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Type 2 neuroglioblast (NGB) lineages. Type 2 lineages are characterized by a switch between neurogenic and gliogenic (or mixed neuro‐gliogenic) phases. All combinations might be possible and the precise division modes of the NGBs neuroblast (NB) 1‐3, NB 2‐5, and NB 7‐4 are not experimentally proven. The complete cell clones are shown on the left column (dorsal view, anterior to the top) and the generated glial cells are highlighted on the right side in a dorsal (anterior to the top, including one peripheral nervous system hemisegment) and a frontal view. Color code of glial cells as above.
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Type 1 neuroglioblast (NGB) lineages. The three NGBs neuroblast (NB) 1‐1A, NB 2‐2T, and NB 5‐6 produce mixed lineages of neurons and glial cells with glial cells arising together with a single neuron from one ganglion mother cell. The complete cell clones (neurons in red, glial cells in green and blue) are shown on the left column (dorsal view, anterior to the top) and the generated glial cells are highlighted on the right side in a cartoon showing the complete glial pattern in a dorsal (anterior to the top, including one peripheral nervous system hemisegment) and a frontal view (dorsal to the top). The color code of glial cells represents the affiliation to the different classes of surface (light green), cortex (dark green), and neuropil‐associated glia (light and dark blue).
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Neuroglioblast (NGB) division modes. Schematic representation of possible division modes of glial precursors in Drosophila. Neuroblasts (NBs) give rise to neurons, NGBs generate mixed lineages of neurons and glial cells, and glioblasts (GBs) produce a pure glial cell clone. GMC: ganglion mother cell. For details see text.
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