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Glia delimit shape changes of sensory neuron receptive endings in C. elegans.

ABSTRACT: Neuronal receptive endings, such as dendritic spines and sensory protrusions, are structurally remodeled by experience. How receptive endings acquire their remodeled shapes is not well understood. In response to environmental stressors, the nematode Caenorhabditis elegans enters a diapause state, termed dauer, which is accompanied by remodeling of sensory neuron receptive endings. Here, we demonstrate that sensory receptive endings of the AWC neurons in dauers remodel in the confines of a compartment defined by the amphid sheath (AMsh) glial cell that envelops these endings. AMsh glia remodel concomitantly with and independently of AWC receptive endings to delimit AWC receptive ending growth. Remodeling of AMsh glia requires the OTD/OTX transcription factor TTX-1, the fusogen AFF-1 and probably the vascular endothelial growth factor (VEGFR)-related protein VER-1, all acting within the glial cell. ver-1 expression requires direct binding of TTX-1 to ver-1 regulatory sequences, and is induced in dauers and at high temperatures. Our results demonstrate that stimulus-induced changes in glial compartment size provide spatial constraints on neuronal receptive ending growth.

SUBMITTER: Procko C

PROVIDER: S-EPMC3050665 | biostudies-literature | 2011 Apr

REPOSITORIES: biostudies-literature

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Glia delimit shape changes of sensory neuron receptive endings in C. elegans.

Procko Carl C Lu Yun Y Shaham Shai S

Development (Cambridge, England) 20110224 7

Neuronal receptive endings, such as dendritic spines and sensory protrusions, are structurally remodeled by experience. How receptive endings acquire their remodeled shapes is not well understood. In response to environmental stressors, the nematode Caenorhabditis elegans enters a diapause state, termed dauer, which is accompanied by remodeling of sensory neuron receptive endings. Here, we demonstrate that sensory receptive endings of the AWC neurons in dauers remodel in the confines of a compar ...[more]

PMID: 21350017

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Project description:Neuromodulators, such as serotonin (5-HT), alter neuronal excitability and synaptic strengths, and define different behavioral states. Neuromodulator-dependent changes in neuronal activity patterns are frequently measured using calcium reporters because calcium imaging can easily be performed on intact functioning nervous systems. With only 302 neurons, the nematode Caenorhabditis elegans provides a relatively simple, yet powerful, system to understand neuromodulation at the level of individual neurons. C. elegans hermaphrodites are repelled by 1-octanol, and the initiation of these aversive responses is potentiated by 5-HT. 5-HT acts on the ASH polymodal nociceptors that sense the 1-octanol stimulus. Surprisingly, 5-HT suppresses ASH Ca2+ transients while simultaneously potentiating 1-octanol-dependent ASH depolarization. Here we further explore this seemingly inverse relationship. Our results show the following (1) 5-HT acts downstream of depolarization, through Gαq-mediated signaling and calcineurin, to inhibit L-type voltage-gated Ca2+ channels; (2) the 1-octanol-evoked Ca2+ transients in ASHs inhibit depolarization; and (3) the Ca2+-activated K+ channel, SLO-1, acts downstream of 5-HT and is a critical regulator of ASH response dynamics. These findings define a Ca2+-dependent inhibitory feedback loop that can be modulated by 5-HT to increase neuronal excitability and regulate behavior, and highlight the possibility that neuromodulator-induced changes in the amplitudes of Ca2+ transients do not necessarily predict corresponding changes in depolarization.SIGNIFICANCE STATEMENT Neuromodulators, such as 5-HT, modify behavior by regulating excitability and synaptic efficiency in neurons. Neuromodulation is often studied using Ca2+ imaging, whereby neuromodulator-dependent changes in neuronal activity levels can be detected in intact, functioning circuits. Here we show that 5-HT reduces the amplitude of depolarization-dependent Ca2+ transients in a C. elegans nociceptive neuron, through Gαq signaling and calcineurin but that Ca2+ itself inhibits depolarization, likely through Ca2+-activated K+ channels. The net effect of 5-HT, therefore, is to increase neuronal excitability through disinhibition. These results establish a novel 5-HT signal transduction pathway, and demonstrate that neuromodulators can change Ca2+ signals and depolarization amplitudes in opposite directions, simultaneously, within a single neuron.

Dataset Information

Glia delimit shape changes of sensory neuron receptive endings in C. elegans.

Publications

Glia delimit shape changes of sensory neuron receptive endings in C. elegans.

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