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

Abstract

In adult olfactory nerves of mammals and moths, a network of glial cells ensheathes small bundles of olfactory receptor axons. In the developing antennal nerve (AN) of the moth Manduca sexta, the axons of olfactory receptor neurons (ORNs) migrate from the olfactory sensory epithelium toward the antennal lobe. Here we explore developmental interactions between ORN axons and AN glial cells. During early stages in AN glial-cell migration, glial cells are highly dye coupled, dividing glia are readily found in the nerve and AN glial cells label strongly for glutamine synthetase. By the end of this period, dye-coupling is rare, glial proliferation has ceased, glutamine synthetase labeling is absent, and glial processes have begun to extend to enwrap bundles of axons, a process that continues throughout the remainder of metamorphic development. Whole-cell and perforated-patch recordings in vivo from AN glia at different stages of network formation revealed two potassium currents and an R-like calcium current. Chronic in vivo exposure to the R-type channel blocker SNX-482 halted or greatly reduced AN glial migration. Chronically blocking spontaneous Na-dependent activity by injection of tetrodotoxin reduced the glial calcium current implicating an activity-dependent interaction between ORNs and glial cells in the development of glial calcium currents.

Spatial and developmental heterogeneity of calcium signaling in olfactory ensheathing cells

“…A significant role for P2Y 1 in the development of radial glial cells and neurons could be shown in the subventricular zone, where proliferation of glial cells and migration of neuronal progenitors depends on ATPmediated calcium signals (Weissman et al, 2004;Liu et al, 2008). In addition, neuronal activity evokes calcium signaling in glial cells in the insect olfactory nerve and the olfactory lobe (homologous to the vertebrate olfactory bulb) (Hartl et al, 2007;Heil et al, 2007), and this calcium signaling is required for glial cell migration in these structures (Lohr et al, 2005;Koussa et al, 2011). A similar function of mGluR 1 and P2Y 1 receptor-mediated calcium signaling for migration of OECs from the olfactory placode to the telencephalon, a key step in early development of the olfactory system in mammals (Ekberg et al, 2012), could be speculated, but needs further investigation.…”

A cellular network of dye-coupled glia associated with the embryonic central complex in the grasshopper Schistocerca gregaria

“…No dye coupling to other neighboring cells occurred in the presence of nheptanol. Arrow indicates ventral according to the neuraxis, and the scale bar represents 65 μm throughout Swales and Lane 1985;Carlson and Saint Marie 1990;Carlson et al 2000;Pereanu et al 2005;Banerjee and Bhat 2007), in phagocytic functions (Doherty et al 2009), and in modulating synaptic transmission, for example, via K + and Ca 2+ signaling (Schmidt and Deitmar 1996;Edwards and Meinertzhagen 2010;Koussa et al 2010). Glial/neuronal interactions are also an integral component of insect nervous system development.…”

“…Migration of glia in the central and peripheral nervous system of insects has been shown to depend on both neuron/glia and glia/glia interactions (Rangarajaran et al 1999;Silies et al 2007;Klämbt 2009;Silies and Klämbt 2011). Among the factors playing a role in such glial interactions in the nervous systems of both insects (Koussa et al 2010) and vertebrates (Parys et al 2010) is Ca 2+ signaling via gap junctions, and one indicator of gap junctional communication is the presence of dye coupling as revealed by fluorescent dyes (Hossain et al 1995;Ball et al 2007;Lanosa et al 2008;Koussa et al 2010).…”

N-cadherin negatively regulates collective Drosophila glial migration via actin cytoskeleton remodeling

“…Tumor glial cells move through the nerve tissue, leading to formation of glioma, the most aggressive form of cancer in the nervous system (Cayre et al, 2009). In addition, glia of the peripheral nervous system (PNS), such as vertebrate perineurium and Schwann cells (Klämbt, 2009), as well as embryonic and pupal Drosophila and Manduca glia, move as collectives to reach their final destination (Cafferty and Auld, 2007;Klämbt, 2009;Koussa et al, 2010;Silies and Klambt, 2010a;von Hilchen et al, 2008;von Hilchen et al, 2013). This makes glia a valuable tool to analyze the role of cadherins in cell migration in the nervous system.…”