Astrocyte‐like glial cells physiologically regulate olfactory processing through the modification of <scp>ORN</scp>‐<scp>PN</scp> synaptic strength in <i><scp>D</scp>rosophila</i>

Liu, He; Zhou, Bangyu; Yan, Wenjun; Lei, Zhengchang; Zhao, Xinghui; Zhang, Ke; Guo, Aike

doi:10.1111/ejn.12646

Cited by 27 publications

(29 citation statements)

References 51 publications

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“…In the olfactory circuit, stimulation of astrocytes using channel rhodopsin 2 (ChR2) inhibited odor-evoked responses of second-order olfactory projection neurons. Astrocyte activation decreased the amplitude and slope of excitatory postsynaptic potentials after antennal nerve stimulation (Liu et al 2014). These data begin to make a case for astrocytes directly reg-…”

Section: Roles For Astrocytes In Neural Circuit Function and Behaviormentioning

confidence: 74%

DrosophilaCentral Nervous System Glia

Freeman

2015

Cold Spring Harb Perspect Biol

265

282

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Molecular genetic approaches in small model organisms like Drosophila have helped to elucidate fundamental principles of neuronal cell biology. Much less is understood about glial cells, although interest in using invertebrate preparations to define their in vivo functions has increased significantly in recent years. This review focuses on our current understanding of the three major neuron-associated glial cell types found in the Drosophila central nervous system (CNS)-astrocytes, cortex glia, and ensheathing glia. Together, these cells act like mammalian astrocytes: they surround neuronal cell bodies and proximal neurites, are coupled to the vasculature, and associate closely with synapses. Exciting recent work has shown essential roles for these CNS glial cells in neural circuit formation, function, plasticity, and pathology. As we gain a more firm molecular and cellular understanding of how Drosophila CNS glial cells interact with neurons, it is becoming clear they share significant molecular and functional attributes with mammalian astrocytes. Invertebrate preparations have contributed enormously to our understanding of fundamental principles of nervous system biology, including the chemical and electrophysiological basis of the action potential, synaptic vesicle release, neural cell fate specification, and axon pathfinding. This is largely thanks to the high experimental accessibility, ease of culture, rapid growth, and the panoply of molecular genetic tools with which to manipulate individual cells in vivo in organisms like Drosophila and Caenorhabditis elegans. The focus of many neuroscientists has shifted in recent years toward careful exploration of how glial cells participate in nervous system development, neural circuit function and plasticity, and neurological disease. Based on the remarkable success with which invertebrates were used to dissect fundamental aspects of the cell biology of the neuron, interest in the potential of small genetic model organisms to contribute to unraveling the mysteries of glial cells has grown significantly. This article will provide a brief overview of Drosophila glial cell biology, then focus on fly glial cell subtypes that are tightly associated with neurons in the central nervous system (CNS)-astrocytes, ensheathing glia, and cortex glia. A growing body of work argues strongly that these glia share a range morphological and functional features with mammalian astrocytes, and recent molecular studies indicate that conservation of basic glial cell biology extends, perhaps not surprisingly, to the molecular level.

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Section: Roles For Astrocytes In Neural Circuit Function and Behaviormentioning

confidence: 74%

DrosophilaCentral Nervous System Glia

Freeman

2015

Cold Spring Harb Perspect Biol

265

282

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“…Although they did not examine the underlying anatomy, results of Liu et al (2014) in the olfactory pathway of Drosophila lend support to the notion that astrocytes regulate synaptic signaling in this species: they overexpressed the TrpA1 channel in astrocytes and found that thermogenetic astrocyte activation modulates excitatory post-synaptic potentials in antennallobe projection neurons. The nature of the anatomical relationship between astrocytes and those synapses, however, was not investigated.…”

Section: Spatial Relationships That Support Astrocyte Regulation Of Smentioning

confidence: 99%

Astrocytic glutamate transport regulates a Drosophila CNS synapse that lacks astrocyte ensheathment

MacNamee

Liu

Gerhard

et al. 2016

J of Comparative Neurology

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Anatomical, molecular, and physiological interactions between astrocytes and neuronal synapses regulate information processing in the brain. The fruit fly Drosophila melanogaster has become a valuable experimental system for genetic manipulation of the nervous system and has enormous potential for elucidating mechanisms that mediate neuron glia interactions. Here, we show the first electrophysiological recordings from Drosophila astrocytes and characterize their spatial and physiological relationship with particular synapses. Astrocyte intrinsic properties were found to be strongly analogous to those of vertebrate astrocytes, including a passive current-voltage relationship, low membrane resistance, high capacitance, and dye-coupling to local astrocytes. Responses to optogenetic stimulation of glutamatergic pre-motor neurons were correlated directly with anatomy using serial electron microscopy reconstructions of homologous identified neurons and surrounding astrocytic processes. Robust bidirectional communication was present: neuronal activation triggered astrocytic glutamate transport via Eaat1, and blocking Eaat1 extended glutamatergic interneuron-evoked inhibitory post-synaptic currents in motor neurons. The neuronal synapses were always located within a micron of an astrocytic process, but none were ensheathed by those processes. Thus, fly astrocytes can modulate fast synaptic transmission via neurotransmitter transport within these anatomical parameters. Graphical AbstractCorresponding Author: Sarah E. MacNamee, University of Arizona Dept. of Neuroscience, 1040 E 4 th St GS Rm 611, Tucson AZ 85721, (520) 621 6671, Smac3@email.arizona.edu. Role of AuthorsAll authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: SEM, LAO. Acquisition of data: SEM, KEL, SG, CTT, RDF, AC. Analysis and interpretation of data: SEM, KEL, CTT. Drafting of the manuscript: SEM. Critical revision of the manuscript for important intellectual content: LAO, LPT, AC. Statistical analysis: SEM. Obtained funding: LAO, LPT, AC. Administrative, technical, and material support: none. Study supervision: LAO, LPT. Conflict of Interest StatementThe authors have no conflict of interest to disclose. Data AccessibilityData generated in the lab and the subsequent analyses will be made available upon request to the Oland/Tolbert laboratory by qualified individuals as long as doing so would not compromise intellectual property interests or interfere with publication. Any shared data would include notations, standards, and the like that are necessary for interpretation of the data. HHMI Author Manuscript HHMI Author Manuscript HHMI Author ManuscriptThe authors show the first recordings from Drosophila astrocytes and find that their electrophysiological properties are strongly analogous to those of vertebrate astrocytes. Using correlative electron microscopy and physiology, they found no glial ensheathment of glutamatergic synap...

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“…Whereas sleep homeostasis is beginning to be understood, there is little known about the circadian control of sleep. Therefore, it is of interest that a mutant called wide awake ( wake ) alters the clock regulation of sleep (Liu et al, 2014). WAKE is required within a subset of the PDF neurons (the l-LNv cells) where it interacts with the GABA-A receptor to modulate excitability of these neurons.…”

Section: Studies Of Glial Cell Function In Circadian Behavior and mentioning

confidence: 99%

Glial Cell Regulation of Rhythmic Behavior

Jackson

Sengupta

et al. 2015

Methods in Enzymology

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Brain glial cells, in particular astrocytes and microglia, secrete signaling molecules that regulate glia–glia or glia–neuron communication and synaptic activity. While much is known about roles of glial cells in nervous system development, we are only beginning to understand the physiological functions of such cells in the adult brain. Studies in vertebrate and invertebrate models, in particular mice and Drosophila, have revealed roles of glia–neuron communication in the modulation of complex behavior. This chapter emphasizes recent evidence from studies of rodents and Drosophila that highlight the importance of glial cells and similarities or differences in the neural circuits regulating circadian rhythms and sleep in the two models. The chapter discusses cellular, molecular, and genetic approaches that have been useful in these models for understanding how glia–neuron communication contributes to the regulation of rhythmic behavior.

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Astrocyte‐like glial cells physiologically regulate olfactory processing through the modification of ORN‐PN synaptic strength in Drosophila

Cited by 27 publications

References 51 publications

DrosophilaCentral Nervous System Glia

DrosophilaCentral Nervous System Glia

Astrocytic glutamate transport regulates a Drosophila CNS synapse that lacks astrocyte ensheathment

Glial Cell Regulation of Rhythmic Behavior

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