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About the Authors:
Mark A. Charlton-Perkins
Current address: Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom
Affiliation: Department of Pediatrics, Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, United States of America
Edward D. Sendler
Affiliation: Center of Molecular Medicine and Genetics, Wayne State University School of Medicine, Detroit, Michigan, United States of America
ORCID http://orcid.org/0000-0002-5334-0119
Elke K. Buschbeck
Affiliation: Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio, United States of America
ORCID http://orcid.org/0000-0001-8563-0826
Tiffany A. Cook
* E-mail: [email protected]
Affiliations Center of Molecular Medicine and Genetics, Wayne State University School of Medicine, Detroit, Michigan, United States of America, Department of Ophthalmology, Wayne State University School of Medicine, Detroit, Michigan, United States of America
ORCID http://orcid.org/0000-0002-3100-5248Abstract
Glial cells play structural and functional roles central to the formation, activity and integrity of neurons throughout the nervous system. In the retina of vertebrates, the high energetic demand of photoreceptors is sustained in part by Müller glia, an intrinsic, atypical radial glia with features common to many glial subtypes. Accessory and support glial cells also exist in invertebrates, but which cells play this function in the insect retina is largely undefined. Using cell-restricted transcriptome analysis, here we show that the ommatidial cone cells (aka Semper cells) in the Drosophila compound eye are enriched for glial regulators and effectors, including signature characteristics of the vertebrate visual system. In addition, cone cell-targeted gene knockdowns demonstrate that such glia-associated factors are required to support the structural and functional integrity of neighboring photoreceptors. Specifically, we show that distinct support functions (neuronal activity, structural integrity and sustained neurotransmission) can be genetically separated in cone cells by down-regulating transcription factors associated with vertebrate gliogenesis (pros/Prox1, Pax2/5/8, and Oli/Olig1,2, respectively). Further, we find that specific factors critical for glial function in other species are also critical in cone cells to support Drosophila photoreceptor activity. These include ion-transport proteins (Na/K+-ATPase, Eaat1, and Kir4.1-related channels) and metabolic homeostatic factors (dLDH and Glut1). These data define genetically distinct glial signatures in cone/Semper cells that regulate their structural, functional and homeostatic interactions with photoreceptor neurons in the compound eye of Drosophila. In addition to providing a new high-throughput model to study neuron-glia interactions, the fly eye will further help elucidate glial...