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Drosophila Central Nervous System Glia Downloaded from http://cshperspectives.cshlp.org/ on October 4, 2021 - Published by Cold Spring Harbor Laboratory Press Drosophila Central Nervous System Glia Marc R. Freeman Department of Neurobiology, Howard Hughes Medical Institute, University of Massachusetts Medical School, Worcester, Massachusetts 01605 Correspondence: [email protected] 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 be- coming clear they share significant molecular and functional attributes with mammalian astrocytes. nvertebrate preparations have contributed with which invertebrates were used to dissect Ienormously to our understanding of funda- fundamental aspects of the cell biology of the mental principles of nervous system biology, neuron, interest in the potential of small genetic including the chemical and electrophysiologi- model organisms to contribute to unraveling cal basis of the action potential, synaptic vesi- the mysteries of glial cells has grown signifi- cle release, neural cell fate specification, and cantly. This article will provide a brief over- axon pathfinding. This is largely thanks to view of Drosophila glial cell biology, then focus the high experimental accessibility, ease of cul- on fly glial cell subtypes that are tightly asso- ture, rapid growth, and the panoply of molecu- ciated with neurons in the central nervous sys- lar genetic tools with which to manipulate indi- tem (CNS)—astrocytes, ensheathing glia, and vidual cells in vivo in organisms like Drosophila cortex glia. A growing body of work argues and Caenorhabditis elegans. The focus of many strongly that these glia share a range morpho- neuroscientists has shifted in recent years to- logical and functional features with mammalian ward careful exploration of how glial cells par- astrocytes, and recent molecular studies indi- ticipate in nervous system development, neural cate that conservation of basic glial cell biology circuit function and plasticity, and neurolog- extends, perhaps not surprisingly, to the molec- ical disease. Based on the remarkable success ular level. Editors: Ben A. Barres, Marc R. Freeman, and Beth Stevens Additional Perspectives on Glia available at www.cshperspectives.org Copyright # 2015 Cold Spring Harbor Laboratory Press; all rights reserved Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a020552 1 Downloaded from http://cshperspectives.cshlp.org/ on October 4, 2021 - Published by Cold Spring Harbor Laboratory Press M.R. Freeman OVERVIEW OF Drosophila NERVOUS superficial layer of neuronal cell bodies in the SYSTEM HISTOLOGY cortex; whether they make any contact with neurites has not been carefully studied, but In total, the adult fly brain and thoracic gan- seems unlikely. Deeper in the CNS, a number glion (the fly equivalent of the mammalian spi- of specialized glial subtypes—cortex glia, en- nal cord) houses 200,000–300,000 neurons. sheathing glia, and astrocytes—associate closely Drosophila neurons are quite similar in terms with neurons. These will be the focus of this of electrophysiological properties to mamma- review and discussed in detail below, along lian neurons. They fire proper Naþ/Kþ-based with a comparison of these cells to their mam- action potentials; they use highly conserved malian counterparts. mechanisms for synaptic vesicle release of con- Drosophila also have a number of glial served neurotransmitters, such as g-aminobu- subtypes outside of the CNS that ensheath, tyric acid (GABA), glutamate, and acetylcholine, support, and modulate the development and and neuromodulators, such as biogenic amines function of peripheral sensory neurons, and and neuropeptides; and they modulate a diverse motorneuron axons and terminals (Fig. 1A– behavioral repertoire that can be studied in the C) (Freeman 2012; Stork et al. 2012). Peripheral intact organism that shows both electrophysio- nerves are covered by the PG- and SPG-based logical and behavioral plasticity. The histology BBB similar to the CNS, but additionally house of the adult Drosophila nervous system is rela- a population of glia termed wrapping glia that tively complex. The brain houses multiple ana- ensheath motor and sensory axons and whose tomically distinct brain lobes, which are con- histology is very similar to that of mammalian nected to one another by fasciculated nerves. Remak bundles (Leiserson et al. 2000; Becker- The CNS can be subdivided into two histolog- vordersandforth et al. 2008; Stork et al. 2008). ical regions: the neuronal cell cortex, where all At the neuromuscular junction, SPGs extend CNS neuronal cell bodies reside; and the neuro- processes that interact with motorneuron pil, to which axons and dendrites project and synaptic contacts on muscles (Fig. 1B) where form neural circuits (Fig. 1A, top). they perform many key functions, including re- As in mammals, glial cells in Drosophila are cycling neurotransmitters (Rival et al. 2004; characterized in large part by their morphol- Danjo et al. 2011), sculpting growing presyn- ogy and association with neurons (Fig. 1A, bot- aptic morphology by engulfing shed axonal/ tom). The precise number of glia in the fly synaptic debris during development (Fuentes- nervous remains unclear, but likely represents Medel et al. 2009), and secreting transforming 5%–10% of the total population of cells within growth factor (TGF)-b molecules that modu- the CNS. The outermost layer of cells associated late retrograde muscle ! presynapse signaling with the surface of the CNS is composed of a and thereby neuromuscular junction (NMJ) subset of glia termed perineural glia (PG), growth (Fuentes-Medel et al. 2012) and regu- which together with macrophages are thought lating synaptic physiology by secreting Wnts to secrete a dense carbohydrate-rich lamella that that modulate postsynaptic glutamate recep- covers the CNS and peripheral nerves and acts tor clustering (Kerr et al. 2014). Finally, exter- as a chemical and physical barrier for the CNS nal sensory organ neurons responsible for (Carlson et al. 2000; Leiserson et al. 2000). The receiving mechanical, chemical, or other stimuli PG layer is discontinuous, with small gaps, but from the environment are closely associated below this is a layer of subperineural glial cells with socket glial cells, sheath glial cells that (SPGs), which show a flattened morphology, wrap the neuronal dendrite and cell body, and cover the entire CNS surface, and establish a an axon-associated glial cell (Fig. 1C). The biol- blood–brain barrier (BBB) by forming pleated ogy of these sensory organ precursors will likely septate junctions with one another (Auld et al. be very similar to C. elegans glia (Shaham 2006), 1995; Baumgartner et al. 1996; Schwabe et al. but their functions have not been studied exten- 2005). SPGs make contact with only the most sively. 2 Advanced Online Article. Cite this article as Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a020552 Downloaded from http://cshperspectives.cshlp.org/ on October 4, 2021 - Published by Cold Spring Harbor Laboratory Press Drosophila CNS Glia CNS NMJ ABWrapping Subperineurial Neuropil MN Neuronal Muscle cell cell cortex IN C Peripheral sensory organs Cross section (glial subtypes) Dendrite Shaft (cuticle) Astrocyte Ensheathing Wrapping Socket Sheath cell cell Sensory neuron Glia (axonal) Perineurial Cell body (cortex) Subperineurial Figure 1. Subtypes, positions, and morphology of Drosophila glia. (A) Overview of the Drosophila larval central nervous system (CNS). The neuronal cell cortex (gray) houses all neuronal and most glial cell bodies. CNS synaptic contacts between neurons are found within the neuropil (light gray). Interneurons (IN) (blue) main- tain all projections within the neuropil: motorneurons (MN) (red) extend axon terminals into the peripheral muscle field. (Bottom) cross-sectional view of glial subtypes (green). Morphological arrangement in the adult brain is similar. See text for details. (B) Glia at the Drosophila larval neuromuscular junction (NMJ). MN terminals (red) penetrate the muscle; subperineurial glia (light green) enter the space between the MN and muscle. (C) Sensory organs in Drosophila contain at least three glial types: the socket cell, sheath cell, and an axon-associated glial cell. (From Freeman 2012; reprinted, with permission, from the author.) CNS GLIAL SUBTYPES CLOSELY neuronal cell bodies, ensheathing glia surround ASSOCIATED WITH NEURONS and compartmentalize the neuropil and nerves as they project out of the CNS, and astrocytes Glial cells that are directly associated with neu- densely infiltrate the synaptic neuropil. The re- rons likely mediate
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