Glial Cells Mediate Target Layer Selection of Retinal Axons in the Developing Visual System of Drosophila

Poeck, Burkhard; Fischer, Susanne; Gunning, Dorian; Zipursky, S. Lawrence; Salecker, Iris

doi:10.1016/s0896-6273(01)00183-0

Cited by 159 publications

(136 citation statements)

References 51 publications

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“…These glia, which migrate independently of retinal innervation, may serve a necessary early role in photoreceptor axon guidance. They may be targets for the first retinal axons to arrive in the optic lobe, and provide the first signals that differentiate the outgrowth termination points of the R1-R6 and R7/8 axons (Poeck et al, 2001). We propose that the first photoreceptor axons to arrive in the optic lobe elicit outgrowth of the scaffold axons from neurons at the dorsal and ventral margins.…”

Section: Discussionmentioning

confidence: 92%

“…This migration depends on local signaling from the photoreceptor axons, as it largely fails to occur in mutants that do not produce photoreceptor neurons (Perez and Steller, 1996) or are deficient in the activity of the COP9 signalosome (Suh et al, 2002). Conversely, lamina glia are required for the guidance of photoreceptor axons, and provide an essential stop signal for the R1-R6 subset of photoreceptor axons to terminate their outgrowth in the lamina (Poeck et al, 2001). These complex processes are controlled with precision in the threedimensional milieu of the developing brain by mechanisms that remain unclear.…”

Section: Introductionmentioning

confidence: 99%

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An axon scaffold induced by retinal axons directs glia to destinations in theDrosophilaoptic lobe

Dearborn

Kunes

2004

Development

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In the developing Drosophila visual system, glia migrate into stereotyped positions within the photoreceptor axon target fields and provide positional information for photoreceptor axon guidance. Glial migration conversely depends on photoreceptor axons, as glia precursors stall in their progenitor zones when retinal innervation is eliminated. Our results support the view that this requirement for retinal innervation reflects a role of photoreceptor axons in the establishment of an axonal scaffold that guides glial cell migration. Optic lobe cortical axons extend from dorsal and ventral positions towards incoming photoreceptor axons and establish at least four separate pathways that direct glia to proper destinations in the optic lobe neuropiles. Photoreceptor axons induce the outgrowth of these scaffold axons. Most glia do not migrate when the scaffold axons are missing. Moreover, glia follow the aberrant pathways of scaffold axons that project aberrantly, as occurs in the mutant dachsous. The local absence of glia is accompanied by extensive apoptosis of optic lobe cortical neurons. These observations reveal a mechanism for coordinating photoreceptor axon arrival in the brain with the distribution of glia to multiple target destinations, where they are required for axon guidance and neuronal survival.

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Section: Discussionmentioning

confidence: 92%

Section: Introductionmentioning

confidence: 99%

An axon scaffold induced by retinal axons directs glia to destinations in theDrosophilaoptic lobe

Dearborn

Kunes

2004

Development

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“…Further to the requirement for Scny, a second H2B ubiquitin protease, Nonstop, also plays a role in fruit fly development. [33][34][35] First identified as the result of a screen for mutations that affect neuronal connectivity in the brain, Nonstop expression in glia was subsequently found to be required for the migration of these cells into the axonal projection field. 34,35 Nonstop is the fly orthologue of yeast Ubp8, a component of the SAGA complex required for the activation of certain stressinducible genes (Table 1).…”

mentioning

confidence: 99%

“…[33][34][35] First identified as the result of a screen for mutations that affect neuronal connectivity in the brain, Nonstop expression in glia was subsequently found to be required for the migration of these cells into the axonal projection field. 34,35 Nonstop is the fly orthologue of yeast Ubp8, a component of the SAGA complex required for the activation of certain stressinducible genes (Table 1). 10,33 Weake et al 33 demonstrated that Nonstop may affect glial migration as part of the SAGA complex, as mutations in genes encoding other components of SAGA also disrupt axonal projections to varying extents.…”

mentioning

confidence: 99%

Flickin’ the ubiquitin switch

Wright¹,

Wang²,

Kao³

2011

Epigenetics

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“…R8 axons also establish a scaffold along which glia migrate (19). Glia then direct the correct targeting of R1-R6 axons in the lamina (20), a process that requires a combination of signaling and transcription factordependent events (reviewed in ref. 3).…”

mentioning

confidence: 99%

Central projections of photoreceptor axons originating from ectopic eyes in Drosophila

Clements

Lǚ

Gehring

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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Ectopic expression of the retinal determination gene eyeless (ey) induces the formation of supernumerary eyes on antennae, legs, wings, and halteres. These ectopic eyes form ommatidia that contain photoreceptors and accessory cells and respond to light. Here, we demonstrate that ectopic eyes on antennae and legs extend axonal projections to the central nervous system. Furthermore, electroretinograms and morphological evidence indicate that the photoreceptor axons of at least the antennal ectopic eyes can form completely constituted ectopic synapses with foreign postsynaptic elements and suggest that transmission at these sites may be functional. However, the ectopic axons do not connect to their correct optic lobe targets and do not project deeply into the neuropile, but rather form synapses at superficial positions in the neuropils. By means of confocal and electron microscopy we show that these ectopic synapses resemble normal synapses, albeit with some distinct morphological differences. Our data strongly suggest that the developmental programs controlling photoreceptor synaptogenesis and visual map formation depend to a considerable extent on presynaptic and thus photoreceptor-autonomous steps. Our data also suggest that photoreceptor axon projections and the establishment of the highly stereotypical neural circuitry in the optic lobe, the normal target neuropil, may depend on targetspecific cues that appear to be absent from the antennal lobe and thoracic ganglion.T he compound eyes of the Drosophila visual system relay visual information to the underlying optic lobes via four successive neuropils, the distalmost lamina, medulla, and proximal lobula and lobula plate (1). The compound eyes consist of Ϸ800 ommatidia, each of which contains eight photoreceptors and 11 accessory cells (2). Photoreceptors R1-R6 project to the lamina, whereas R7 and R8 axons terminate in the medulla (reviewed in refs. 1 and 3).In the past decade, considerable insight has been gained in the genetic basis of early eye development, photoreceptor determination and ommatidium formation, and circuit assembly in the optic lobe. Early eye development is controlled by a genetic cascade comprising the Pax6 genes eyeless (ey) and twin of eyeless (toy), considered master control genes acting as the first step in the hierarchy, the SIX family members sine oculis (so) and optix, eyes absent (eya), dachshund (dac), and the Pax6-related gene eyegone (eyg). These genes act in complex gene networks and are integrated with signaling pathways (reviewed in refs. 4-6). Some of these genes individually, or in combination with others, are capable of inducing the formation of ectopic eyes (7-12).Photoreceptor differentiation is initiated at the posterior margin of the eye imaginal disc with the formation of the morphogenetic furrow and involves the integration of the decapentaplegic, hedgehog, and wingless signaling pathways with the retinal determination gene network (reviewed in refs. 5 and 13). Signaling by the Notch and Epidermal Growth Factor Recept...

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Glial Cells Mediate Target Layer Selection of Retinal Axons in the Developing Visual System of Drosophila

Cited by 159 publications

References 51 publications

An axon scaffold induced by retinal axons directs glia to destinations in theDrosophilaoptic lobe

An axon scaffold induced by retinal axons directs glia to destinations in theDrosophilaoptic lobe

Flickin’ the ubiquitin switch

Central projections of photoreceptor axons originating from ectopic eyes in Drosophila

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