Drosophila astrocytes cover specific territories of CNS neuropil and are instructed to differentiate by Prospero, a key effector of Notch

Peco, Emilie; Davla, Sejal; Camp, Darius; Stacey, Stephanie M.; Landgraf, Matthias; Meyel, Donald J. van

doi:10.1242/dev.133165

“…In order to characterize the cellular organization of the NG in the adult VNC, we expressed fluorescent reporters under the control of two Gal4 drivers, alrm-Gal4 (astrocyte specific; Doherty et al, 2009) and R56FO3-Gal4 (EG specific; Kremer et al, 2017; Peco et al, 2016; Pfeiffer et al, 2008), which we confirmed are expressed in all adult astrocytes and EG, respectively (Figures 1 and S1). We also used as a marker Distalless (Dll), which we found to be expressed in all NG in the adult VNC (Figure S1).…”

Section: Resultsmentioning

confidence: 69%

“…In a second experiment, we used Dll-Gal4 to activate the Flybow system ( UAS-FB1.1 ), which permanently labels cells with different fluorescent markers (Hadjieconomou et al, 2011). We co-stained the resulting adult VNCs with Prospero, which is expressed in astrocytes but not in EG (Griffiths and Hidalgo, 2004; Peco et al, 2016) (Figures 2F and S1). Based on Prospero expression and morphology, we found that both astrocytes and EG were labeled.…”

Section: Resultsmentioning

confidence: 99%

“…NG are further subdivided into astrocytes and ensheathing glia (EG) (Muthukumar et al, 2014; Peco et al, 2016). EG extend flat processes that surround neuropil and glomeruli as well as a small portion of axon bundles as they enter or leave the neuropil (Omoto et al, 2015; Peco et al, 2016). More recently, EG have been shown to extend small protrusions inside the neuropil of the adult brain (Kremer et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Differing Strategies Despite Shared Lineages of Motor Neurons and Glia to Achieve Robust Development of an Adult Neuropil in Drosophila

Enriquez

¹

,

Rio

²

,

Blazeski

³

et al. 2018

Neuron

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SUMMARY In vertebrates and invertebrates, neurons and glia are generated in a stereotyped manner from neural stem cells, but the purpose of invariant lineages is not understood. We show that two stem cells that produce leg motor neurons in Drosophila also generate neuropil glia, which wrap and send processes into the neuropil where motor neuron dendrites arborize. The development of the neuropil glia and leg motor neurons is highly coordinated. However, although motor neurons have a stereotyped birth order and transcription factor code, the number and individual morphologies of the glia born from these lineages are highly plastic, yet the final structure they contribute to is highly stereotyped. We suggest that the shared lineages of these two cell types facilitate the assembly of complex neural circuits and that the two birth order strategies—hardwired for motor neurons and flexible for glia—are important for robust nervous system development, homeostasis, and evolution.

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“…The subset of Drosophila glial cells examined in this study has been named 'interface glia' (Ito et al, 1995), 'longitudinal glia' (Beckervordersandforth et al, 2008), 'astrocyte-like glia' (Awasaki et al, 2008), and, most recently, just 'astrocytes' Muthukumar et al, 2014;Peco et al, 2016), based on their morphology and molecular identity. The present study is the first to characterize the electrical membrane properties of Drosophila astrocytes.…”

Section: Discussionmentioning

confidence: 99%

“…Specificity of Eaat1 antiserum was confirmed by loss of Eaat1 immunoreactivity in Eaat1 null mutants. (Peco et al, 2016).…”

Section: Antibody Characterizationmentioning

confidence: 99%

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

MacNamee

¹

,

Liu

²

,

Gerhard

³

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...

show abstract

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

MacNamee

¹

,

Liu

²

,

Gerhard

³

et al. 2016

J of Comparative Neurology

View full text Add to dashboard Cite

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.

show abstract

Drosophila astrocytes cover specific territories of CNS neuropil and are instructed to differentiate by Prospero, a key effector of Notch

Cited by 67 publications

References 61 publications

Differing Strategies Despite Shared Lineages of Motor Neurons and Glia to Achieve Robust Development of an Adult Neuropil in Drosophila

Differing Strategies Despite Shared Lineages of Motor Neurons and Glia to Achieve Robust Development of an Adult Neuropil in Drosophila

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

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

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