Development of depolarization‐induced calcium transients in insect glial cells is dependent on the presence of afferent axons

Lohr, Christian; Tucker, Eric S.; Oland, Lynne A.; Tolbert, Leslie P.

doi:10.1002/neu.10075

Cited by 13 publications

(18 citation statements)

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“…Calcium signaling in Manduca antennal lobe glial cells and neurons has been shown to be due to voltage-gated calcium channels (Lohr et al, 2002;Lohr, 2003). We have now used three specific blockers of voltage-gated calcium channels, verapamil, diltiazem, and flunarizine, to suppress glial and neuronal calcium signaling (Fig.…”

Section: Effect Of Calcium Channel Blockagementioning

confidence: 97%

“…Migration of sorting zone glial cells into the olfactory nerve and of neuropilassociated glial cells around immature glomeruli is a crucial step for several developmental aspects such as axon sorting and glomerulus formation in insects Rössler et al, 1999). Despite the important functions of glial cells for the development of both the vertebrate and the insect olfactory system, physiological properties of ensheathing cells and olfactory bulb astrocytes have not been investigated in detail, while antennal lobe glial cells have been studied only recently (Lohr et al, , 2002.…”

Section: Introductionmentioning

confidence: 99%

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Blockage of voltage-gated calcium signaling impairs migration of glial cells in vivo

Lohr

Heil

Deitmer

2005

Glia

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Migration of glial cells is an essential step in the development of the antennal lobe, the primary olfactory center of insects, to establish well-defined borders between olfactory glomeruli required for odor discrimination. In the present study, we used two-photon microscopy to visualize calcium signaling in developing antennal lobe glial cells of the sphinx moth Manduca sexta. We found a correlation between the upregulation of functional voltage-gated calcium channels and the onset of glial cell migration. In addition, glial cells migrating into the center of the antennal lobe express larger voltage-gated calcium transients than glial cells that remain at the periphery. Migration behavior and calcium signaling of glial cells in vivo were manipulated either by deafferentation, by injection of the calcium channel blockers diltiazem, verapamil, and flunarizine, or by injection of the calcium chelators BAPTA-AM and Fluo-4-AM. In deafferented antennal lobes, glial cells failed to express functional voltage-gated calcium channels and did not migrate. Calcium channel blockage or reducing glial calcium signals by calcium chelators prevented glial cell migration and resulted in antennal lobes lacking glial borders around glomeruli, indicating that voltage-gated calcium signaling is required for the migration of antennal lobe glial cells and the development of mature olfactory glomeruli.

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Section: Effect Of Calcium Channel Blockagementioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

Blockage of voltage-gated calcium signaling impairs migration of glial cells in vivo

Lohr

Heil

Deitmer

2005

Glia

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“…149.9 mM NaCl, 3 mM KCl, 3 mM CaCl 2 , 0.5 mM MgCl 2 , 10 mM TES, 11 mM D-glucose, 3 g/liter lactalbumin hydrosylate (11800-026; Gibco), 2.5 g/liter TC yeastolate (255772; Difco, Detroit, MI), 5% fetal bovine serum (FBS; Hyclone, Logan, UT), 100 U/ml penicillin, and 100 µg/ml streptomycin, osmolarity adjusted to 360 mOsm with mannitol. Culture medium (supplemented Leibovitz's L-15 culture medium; Lohr et al, 2002).…”

Section: Culture Solutionsmentioning

confidence: 99%

“…Developmentally, glial migration in the AN has begun as early as stage 3 of metamorphic development, a stage at which NP glia have not yet developed calcium transients (Lohr et al, 2002). In the latter, calcium transients begin to appear at stage 6, and are present in all NP glial cells by stage 7; stage 6 is the stage at which NP glial cells begin to migrate to surround and stabilize developing glomeruli (Lohr et al, 2005;Lohr and Deitmer, 2006;Bauman et al, 1996).…”

Section: Calcium Current In the An Glial Cellsmentioning

confidence: 99%

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

2010

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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.

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“…Acutely isolated glial cells were prepared by using essentially the methods described previously by Lohr et al (2002). Briefly, female pupae from stages late 6 to early 7 of metamorphic adult development were cooled on ice, and brains were dissected into 35-mm culture dishes containing sterile dissecting medium.…”

Section: Preparation Of Culturesmentioning

confidence: 99%

In vitro analyses of interactions between olfactory receptor growth cones and glial cells that mediate axon sorting and glomerulus formation

Tucker

Oland

Tolbert

2004

J of Comparative Neurology

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During development, the axons of olfactory receptor neurons project to the CNS and converge on glomerular targets. For vertebrate and invertebrate olfactory systems, neuron-glia interactions have been hypothesized to regulate the sorting and targeting of olfactory receptor axons and the development of glomeruli. In the moth Manduca sexta, glial reduction experiments have directly implicated two types of central olfactory glia, the sorting zone- and neuropil-associated glia, in key events in olfactory development, including axon sorting and glomerulus stabilization. By using cocultures containing central olfactory glial cells and explants of olfactory receptor epithelium, we show that olfactory receptor growth cones elaborate extensively and cease advancement following contact with sorting zone- and neuropil-associated glial cells. These effects on growth cone behavior were specific to central olfactory glia; peripheral glial cells of the olfactory nerve failed to elicit similar responses in olfactory receptor growth cones. We propose that sorting zone- and neuropil-associated glial cells similarly modify axon behavior in vitro by altering the adhesive properties and cytoskeleton of olfactory receptor growth cones and that these in vitro changes may underlie functionally relevant changes in growth cone behavior in vivo.

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Development of depolarization‐induced calcium transients in insect glial cells is dependent on the presence of afferent axons

Abstract: Changes in the intracellular

Cited by 13 publications

References 72 publications

Blockage of voltage-gated calcium signaling impairs migration of glial cells in vivo

Blockage of voltage-gated calcium signaling impairs migration of glial cells in vivo

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

In vitro analyses of interactions between olfactory receptor growth cones and glial cells that mediate axon sorting and glomerulus formation

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