Identity, origin, and migration of peripheral glial cells in the Drosophila embryo

Abstract

Glial cells are crucial for the proper development and function of the nervous system. In the Drosophila embryo, the glial cells of the peripheral nervous system are generated both by central neuroblasts and sensory organ precursors. Most peripheral glial cells need to migrate along axonal projections of motor and sensory neurons to reach their final positions in the periphery. Here we studied the spatial and temporal pattern, the identity, the migration, and the origin of all peripheral glial cells in the truncal segments of wildtype embryos. The establishment of individual identities among these cells is reflected by the expression of a combinatorial code of molecular markers. This allows the identification of individual cells in various genetic backgrounds. Furthermore, mutant analysis of two of these marker genes, spalt major and castor, reveal their implication in peripheral glial development. Using confocal 4D microscopy to monitor and follow peripheral glia migration in living embryos, we show that the positioning of most of these cells is predetermined with minor variations, and that the order in which cells migrate into the periphery is almost fixed. By studying their lineages, we uncovered the origin of each of the peripheral glial cells and linked them to identified central and peripheral neural stem cells.

Development of a glial network in the olfactory nerve: role of calcium and neuronal activity

“…Labeling of the migrating AN glial cell population with anti-glutamine synthetase antibody shows that glial cells often appear in chains, as has been seen in other systems (Sepp et al, 2000;Gilmour et al, 2002;Silies et al, 2007;von Hilchen et al, 2008, Aigouy et al, 2008 (Fig. 3 A-D).…”

“…Collective or chain migration is a fundamental feature of migration in Drosophila wing and peripheral nerve (Giangrande, 1994;Sepp et al, 2000;Aigouy et al, 2004;von Hilchen et al, 2008), in the Manduca enteric nervous system (Copenhaver and Taghert, 1989;Wright and Copenhaver, 2000) and in zebrafish peripheral nerves (Kucenas et al, 2008). In the moth antennal nerve, AN glial cells often appear in chains in vivo especially at the early stages of migration although the dimensions of the nerve and the pattern of glial process extension indicate that chaining along cannot be responsible for continuous ensheathment of axon bundles.…”

CASZ1, a candidate tumor-suppressor gene, suppresses neuroblastoma tumor growth through reprogramming gene expression

“…5,[7][8][9] Our study provides compelling functional evidence that the CASZ1 suppresses tumor cell growth in vitro and in vivo (Figures 6 and 7). CASZ1 induces NB cells differentiation in vitro; and in CASZ1-expressing xenograft tumors there is an increase in expression of NGFR and TrkA (Figures 7c and d), which are highly expressed in differentiated NB tumors and markers of good prognosis in NB.…”

“…[5][6][7] Dcas functions to regulate neural fate and loss of dcas in Drosophila results in impaired differentiation and alterations in glial cell number and migration. 5,7,8 In Xeneopus CASZ1 is required for heart development and onset of cardiomyocytes differentiation at the ventral midline; the CASZ1-depleted midline cells overproliferate and remain a coherent population of nonintegrated cells positioned on the outer wall of the ventricle. 9 Although functional studies have not been performed in mammals to date, murine studies indicate developmental regulation of CASZ1 in the neural crest-derived peripheral nervous system 10 cells, which are thought to be the origin of NB tumors.…”

Spinster Controls Dpp Signaling during Glial Migration in theDrosophilaEye

“…Glial migration is extensively studied in Drosophila. During embryonic PNS development, glial cells born in the CNS migrate outward along the segmental nerves guided by diffusible signals and differential adhesion (Sepp et al, 2000;von Hilchen et al, 2008von Hilchen et al, , 2010. During wing formation, peripherally born glia follow sensory axons as they travel toward the CNS (Aigouy et al, 2004(Aigouy et al, , 2008.…”