Mechanisms Underlying Glial Regulation of Neuronal Excitability in Drosophila

NIH RePORTER · NIH · R21 · $193,750 · view on reporter.nih.gov ↗

Abstract

We propose to use Drosophila as a model system for determining how glial Ca2+ oscillations couple to K+ buffering and neurotransmitter uptake to regulate neuronal excitability. Glial cells, including astrocytes, can increase their intracellular Ca2+ both spontaneously and in response to neuronal activity, and growing evidence indicates astrocytic Ca2+ signaling acutely influences neuronal physiology. However, little is known about the molecular machinery underlying different types of glial Ca2+ signals and how they act to regulate neuronal excitability. Like mammals, we have found that Drosophila glia display microdomain Ca2+ oscillatory activity that acutely regulates neuronal function and behavior. Drosophila has two main glial subtypes that are intimately associated with neurons in the CNS and that share features with mammalian astrocytes -- astrocyte-like glia and cortex glia. The Drosophila CNS is compartmentalized into the cell cortex that contains neuronal cell bodies, and the synaptic neuropil that contains all neurites and synapses. Astrocytes and cortex glia are similarly compartmentalized into these brain regions, with astrocytes associating with synapses and cortex glia surrounding neuronal somas that are devoid of synapses. As such, Drosophila provides an ideal system to study spatially-localized glial-neuronal signaling at somas versus synapses. We have identified mutations in a Drosophila cortex glial-specific NCKX exchanger that controls microdomain Ca2+ oscillations and that acutely triggers neuronal seizures when inactivated. In addition, we found that ectopic glial expression of a heat-activated TRPA1 channel can induce rapid Ca2+ influx and neuronal seizures in cortex glial, or rapid paralysis and neuronal silencing when expressed in astrocytes. Using unbiased genetic suppressor screens for the behavioral seizure and paralysis phenotypes, we have generated initial data that indicates Ca2+ influx controls membrane trafficking of either leak K+ channels or neurotransmitter transporters, providing an unexpected and exciting connection between glial Ca2+ oscillations and the more well-known roles of glia in K+ buffering and neurotransmitter clearance. In the current application, we propose experiments that will provide a foundation to examine how glial Ca2+ oscillatory activity modulates spatial K+ buffering and neurotransmitter uptake to acutely modulate neuronal excitability through either glial-soma or glial-synapse interactions, respectively.

Key facts

NIH application ID
9936453
Project number
5R21MH120440-02
Recipient
MASSACHUSETTS INSTITUTE OF TECHNOLOGY
Principal Investigator
J. TROY LITTLETON
Activity code
R21
Funding institute
NIH
Fiscal year
2020
Award amount
$193,750
Award type
5
Project period
2019-06-01 → 2022-04-30