Reciprocal Interactions between Neurons and Glia Are Required for<i>Drosophila</i>Peripheral Nervous System Development

Sepp, Katharine J.; Auld, Vanessa J.

doi:10.1523/jneurosci.23-23-08221.2003

Cited by 88 publications

(86 citation statements)

References 60 publications

(68 reference statements)

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“…It has been already noted earlier that expression of Gliotactin is absent in egfr and vein mutants but is expressed in spitz mutants (Sepp and Auld, 2003b). Likewise, it was shown that expression of Neuroglian is dramatically reduced in egfr mutants (Sepp and Auld, 2003b).…”

Section: Discussionmentioning

confidence: 76%

Axonal wrapping in theDrosophilaPNS is controlled by glia-derived neuregulin homolog Vein

et al. 2015

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Efficient neuronal conductance requires that axons are insulated by glial cells. For this, glial membranes need to wrap around axons. Invertebrates show a relatively simple extension of glial membranes around the axons, resembling Remak fibers formed by Schwann cells in the mammalian peripheral nervous system. To unravel the molecular pathways underlying differentiation of glial cells that provide axonal wrapping, we are using the genetically amenable Drosophila model. At the end of larval life, the wrapping glia differentiates into very large cells, spanning more than 1 mm of axonal length. The extension around axonal membranes is not influenced by the caliber of the axon or its modality. Using cell typespecific gene knockdown we show that the extension of glial membranes around the axons is regulated by an autocrine activation of the EGF receptor through the neuregulin homolog Vein. This resembles the molecular mechanism employed during cell-autonomous reactivation of glial differentiation after injury in mammals. We further demonstrate that Vein, produced by the wrapping glia, also regulates the formation of septate junctions in the abutting subperineurial glia. Moreover, the wrapping glia indirectly controls the proliferation of the perineurial glia. Thus, the wrapping glia appears center stage to orchestrate the development of the different glial cell layers in a peripheral nerve.

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Section: Discussionmentioning

confidence: 76%

Axonal wrapping in theDrosophilaPNS is controlled by glia-derived neuregulin homolog Vein

et al. 2015

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“…Fly stocks were obtained from the Bloomington Stock Center and the Vienna Drosophila RNAi Center (VDRC), or alternative published sources as noted: P{EPgy2}Eaat1 EY20741 ; Df(2L)30A-C (here denoted Eaat1 Df ); UAS-mCD8::RFP; UAS-Eaat1; UAS-Pros RNAi (VDRC ID 101477); Eaat1-Gal4 (Rival et al, 2004); htl-Gal4 (Shishido et al, 1997); Repo-Gal4 (Sepp and Auld, 2003); tub-Gal80 ts (McGuire et al, 2003); UAS-N ICD (Go et al, 1998); UAS-Hairless (Maier et al, 1999); UAS-Tom (Lai et al, 2000); UAS-Eaat1::GFP (Rival et al, 2004); UAS-mCD8::GFP (Lee and Luo, 1999); UAS-nuclearGFP (van Meyel et al, 2003); Su(H)-lacZ (Griffiths et al, 2007); and fng L73 and fng 13 (Irvine and Wieschaus, 1994;Correia et al, 2003). To create CG31235-nuclear green fluorescent protein (nGFP) and CG31235-Gal4, we PCR amplified 3004 base pairs (bp) of regulatory sequences located immediately upstream of CG31235 using the primers 5Ј-CATAGTGCATTGGTGAGGTGT-3Ј and 5Ј-TACTGGGTGCGCGTTAGGTC-3Ј.…”

Section: Methodsmentioning

confidence: 99%

“…Two additional glial-specific Gal4 drivers were also tested for their ability to rescue Eaat1 SM2/SM2 mutants: Eaat1-Gal4 (Rival et al, 2004) and Repo-Gal4 (Sepp and Auld, 2003), which is expressed more broadly in all lateral glia. Like CG31235-Gal4, these drivers also rescued larval contractions (data not shown).…”

Section: Severe Locomotor Dysfunction In Eaat1 Mutantsmentioning

confidence: 99%

DrosophilaGlial Glutamate Transporter Eaat1 Is Regulated by Fringe-Mediated Notch Signaling and Is Essential for Larval Locomotion

Stacey¹,

Muraro²,

Peco³

et al. 2010

J. Neurosci.

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In the mammalian CNS, glial cells expressing excitatory amino acid transporters (EAATs) tightly regulate extracellular glutamate levels to control neurotransmission and protect neurons from excitotoxic damage. Dysregulated EAAT expression is associated with several CNS pathologies in humans, yet mechanisms of EAAT regulation and the importance of glutamate transport for CNS development and function in vivo remain incompletely understood. Drosophila is an advanced genetic model with only a single high-affinity glutamate transporter termed Eaat1. We found that Eaat1 expression in CNS glia is regulated by the glycosyltransferase Fringe, which promotes neuron-to-glia signaling through the Delta-Notch ligand-receptor pair during embryogenesis. We made Eaat1 loss-of-function mutations and found that homozygous larvae could not perform the rhythmic peristaltic contractions required for crawling. We found no evidence for excitotoxic cell death or overt defects in the development of neurons and glia, and the crawling defect could be induced by postembryonic inactivation of Eaat1. Eaat1 fully rescued locomotor activity when expressed in only a limited subpopulation of glial cells situated near potential glutamatergic synapses within the CNS neuropil. Eaat1 mutants had deficits in the frequency, amplitude, and kinetics of synaptic currents in motor neurons whose rhythmic patterns of activity may be regulated by glutamatergic neurotransmission among premotor interneurons; similar results were seen with pharmacological manipulations of glutamate transport. Our findings indicate that Eaat1 expression is promoted by Fringe-mediated neuron-glial communication during development and suggest that Eaat1 plays an essential role in regulating CNS neural circuits that control locomotion in Drosophila.

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“…Role of localized neurotrophic factor-NRG signaling in peripheral nerve development, maintenance, and disease Although much of the research emphasis in neurotrophic factors has centered on their roles as target-derived factors important for neuronal survival during development, neuronal survival is also highly dependent on glial-derived signals (Sepp and Auld, 2003). Disruption of NRG signaling in mice not only leads to an almost complete loss of Schwann cells, but shortly thereafter, all motor and sensory neurons die.…”

Section: Rapid Axoglial Communication Through Schwann Cell Neurotrophmentioning

confidence: 99%

Rapid Axoglial Signaling Mediated by Neuregulin and Neurotrophic Factors

Esper¹,

Loeb²

2004

J. Neurosci.

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During peripheral nervous system development, Schwann cells are precisely matched to the axons that they support. This is mediated by axonal neuregulins that are essential for Schwann cell survival and differentiation. Here, we show that sensory and motor axons rapidly release heparin-binding forms of neuregulin in response to Schwann cell-derived neurotrophic factors in a dose-dependent manner. Neuregulin release occurs within minutes, is saturable, and occurs from axons that were isolated using a newly designed chamber slide apparatus. Although NGF and glial cell line-derived neurotrophic factor (GDNF) were the most potent neurotrophic factors to release neuregulin from sensory neurons, GDNF and BDNF were most potent for motor neurons and were the predominant neuregulin-releasing neurotrophic factors produced by cultured Schwann cells. Comparable levels of neuregulin could be released at a similar rate from neurons after protein kinase C activation with the phorbol ester, phorbol 12-myristate 13-acetate, which has also been shown to promote the cleavage and release of neuregulin from its transmembrane precursor. The rapid release of neuregulin from axons in response to Schwann cell-derived neurotrophic factors may be part of a spatially restricted system of communication at the axoglial interface important for proper peripheral nerve development, function, and repair.

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Reciprocal Interactions between Neurons and Glia Are Required forDrosophilaPeripheral Nervous System Development

Cited by 88 publications

References 60 publications

Axonal wrapping in theDrosophilaPNS is controlled by glia-derived neuregulin homolog Vein

Axonal wrapping in theDrosophilaPNS is controlled by glia-derived neuregulin homolog Vein

DrosophilaGlial Glutamate Transporter Eaat1 Is Regulated by Fringe-Mediated Notch Signaling and Is Essential for Larval Locomotion

Rapid Axoglial Signaling Mediated by Neuregulin and Neurotrophic Factors

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