Temporal Control of Glial Cell Migration in the Drosophila Eye Requires gilgamesh, hedgehog, and Eye Specification Genes

Hummel, Thomas; Attix, Suzanne; Gunning, Dorian; Zipursky, S. Lawrence

doi:10.1016/s0896-6273(01)00581-5

Cited by 90 publications

(123 citation statements)

References 56 publications

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“…As photoreceptor axons grow out, glia require a signal from the neurons to migrate back along the axons. Neurons in turn depend on the glial cells for proper guidance to exit the eyestalk (Rangarajan et al 1999;Hummel et al 2002). Areas of future study might include whether young glia in tracts in vivo have specialized molecules for axon extension, and to what extent neurons signal glial migration and process extension around axon fascicles.…”

Section: Substrata In Vivomentioning

confidence: 99%

Cellular Strategies of Axonal Pathfinding

Raper

Mason

2010

Cold Spring Harbor Perspectives in Biology

157

127

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Axons follow highly stereotyped and reproducible trajectories to their targets. In this review we address the properties of the first pioneer neurons to grow in the developing nervous system and what has been learned over the past several decades about the extracellular and cell surface substrata on which axons grow. We then discuss the types of guidance cues and their receptors that influence axon extension, what determines where cues are expressed, and how axons respond to the cues they encounter in their environment.T his article provides an overview of how growth cones respond to the cellular substrata and molecular cues they encounter as they extend through the developing nervous system. It elaborates on the primer by Kolodkin and TessierLavigne (2010) and touches on many of the topics covered in greater detail in the articles that follow. The first sections describe how axons extend in a directed manner, the substrata on which they grow, interactions between pioneer and follower axons, and growth cone behaviors in emerging tracts and at decision points. The subsequent sections discuss examples of specific cues, their distributions, how their distributions are determined, and how growth cones integrate multiple cues during pathfinding. AXONS EXTEND IN VIVO IN A DIRECTED MANNERThe first person to visualize the growing tips of axons, Ramon y Cajal, recognized that axons for the most part grow very efficiently towards their ultimate targets. He was a strong advocate for axons finding their way in response to chemotactic cues:"If one admits that neuroblasts are endowed with chemotactic properties, then one might also imagine that they are capable of ameboid movements, initiated by factors secreted from epithelial, neural, or mesodermal elements. As a result, their processes may be oriented in the direction of chemical gradients, and thus guided to the secreting cells" (Ramon y Cajal 1892; trans. English, 1995).This surprisingly modern outlook emphasizing directed guidance was temporarily derailed by the views of Weiss during the 1920s and 1930s. He first argued that functional specificity did not arise as a consequence of specific axonal connections (Weiss 1936), and later argued that nonspecific mechanical guidance cues play a predominant role in guiding axons and organizing them into nerves and tracts

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Section: Substrata In Vivomentioning

confidence: 99%

Cellular Strategies of Axonal Pathfinding

Raper

Mason

2010

Cold Spring Harbor Perspectives in Biology

157

127

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“…The molecular nature and features of these new PCP regulatory genes ranged from kinases, phosphatases, enzymes required for lipid biosynthesis or modification, to proteins involved in substrate degradation or modification. Among the kinases, CG7004 (four wheel drive/fwd) encodes a PI4kinaseß, which has been shown to be required for male germ-line development (Polevoy et al 2009), and CG6963 (gilgamesh/gish), a casein kinase1g, known to be involved in many processes including Wnt signaling (Davidson et al 2005), glial cell migration (Hummel et al 2002), and spermatogenesis (Nerusheva et al 2009). Phosphatases of the PAP2 family, CG11426 and CG11438, were also identified.…”

Section: Identification and Loss-of-function Analyses Of New Pcp Candmentioning

confidence: 99%

Novel Regulators of Planar Cell Polarity: A Genetic Analysis in Drosophila

Weber

Gault²,

Olguı́n

et al. 2012

Genetics

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Planar cell polarity (PCP) is a common feature of many epithelia and epithelial organs. Although progress has been made in the dissection of molecular mechanisms regulating PCP, many questions remain. Here we describe a screen to identify novel PCP regulators in Drosophila. We employed mild gain-of-function (GOF) phenotypes of two cytoplasmic Frizzled (Fz)/PCP core components, Diego (Dgo) and Prickle (Pk), and screened these against the DrosDel genome-wide deficiency collection for dominant modifiers. Positive genomic regions were rescreened and narrowed down with smaller overlapping deficiencies from the Exelixis collection and RNAi-mediated knockdown applied to individual genes. This approach isolated new regulators of PCP, which were confirmed with loss-of-function analyses displaying PCP defects in the eye and/or wing. Furthermore, knockdown of a subset was also sensitive to dgo dosage or dominantly modified a dishevelled (dsh) GOF phenotype, supporting a role in Fz/PCP-mediated polarity establishment. Among the new "PCP" genes we identified several kinases, enzymes required for lipid modification, scaffolding proteins, and genes involved in substrate modification and/or degradation. Interestingly, one of them is a member of the Meckel-Gruber syndrome factors, associated with human ciliopathies, suggesting an important role for cell polarity in nonciliated cells.

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“…First, R8 axons must navigate to the posterior of the eye disk and enter the optic stalk. This process is facilitated, in part, by retinal basal glial cells at the posterior edge of the eye disk (20,21). If glial cells are displaced anteriorly, R-cell axon fascicles project away from the optic stalk rather than toward it (21).…”

Section: Posterior R8 Axon Guidance Plays a Crucial Role In Axon Fascmentioning

confidence: 99%

“…This process is facilitated, in part, by retinal basal glial cells at the posterior edge of the eye disk (20,21). If glial cells are displaced anteriorly, R-cell axon fascicles project away from the optic stalk rather than toward it (21). Although it seems likely that this directional choice relies upon R8, it is not known whether posterior growth requires R8-specific functions or whether all retinal neurons are endowed with this function.…”

Section: Posterior R8 Axon Guidance Plays a Crucial Role In Axon Fascmentioning

confidence: 99%

Robo-3–mediated repulsive interactions guide R8 axons during Drosophila visual system development

Pappu

Morey

Nern

et al. 2011

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

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The formation of neuronal connections requires the precise guidance of developing axons toward their targets. In the Drosophila visual system, photoreceptor neurons (R cells) project from the eye into the brain. These cells are grouped into some 750 clusters comprised of eight photoreceptors or R cells each. R cells fall into three classes: R1 to R6, R7, and R8. Posterior R8 cells are the first to project axons into the brain. How these axons select a specific pathway is not known. Here, we used a microarray-based approach to identify genes expressed in R8 neurons as they extend into the brain. We found that Roundabout-3 (Robo3), an axon-guidance receptor, is expressed specifically and transiently in R8 growth cones. In wild-type animals, posterior-most R8 axons extend along a border of glial cells demarcated by the expression of Slit, the secreted ligand of Robo3. In contrast, robo3 mutant R8 axons extend across this border and fasciculate inappropriately with other axon tracts. We demonstrate that either Robo1 or Robo2 rescues the robo3 mutant phenotype when each is knocked into the endogenous robo3 locus separately, indicating that R8 does not require a function unique to the Robo3 paralog. However, persistent expression of Robo3 in R8 disrupts the layer-specific targeting of R8 growth cones. Thus, the transient cellspecific expression of Robo3 plays a crucial role in establishing neural circuits in the Drosophila visual system by selectively regulating pathway choice for posterior-most R8 growth cones.A striking feature of the insect visual system is the organization of neurons into parallel, interconnected layers and orthogonal columns that contain the axonal and dendritic processes from many neurons (1). Columnar organization preserves the topology of visual space. This organization is achieved, in part, during development by the assembly of axons into discrete fascicles. The fly eye comprises some 750 ommatidia or simple eyes, each containing a cluster of eight photoreceptor neurons (R1-R8). R-cell axons form a topographic map of the visual world in the lamina and medulla. The R1 to R6 axons terminate in the lamina, and R7 and R8 extend through the lamina and terminate in the medulla. Axons from each ommatidium form a discrete fascicle and form connections within columnar units, referred to as cartridges and columns in the lamina and medulla, respectively. The orderly assembly of cartridges and columns relies upon the precise spatiotemporal pattern of R-cell innervation.Two features of early eye development facilitate the orderly assembly of the visual system. First, individual rows of ommatidia are recruited sequentially, following a wave of differentiation beginning at the posterior margin of the eye primordium or eye disk and progressing anteriorly across it. As new ommatidia form, the R cells within them extend axons into the brain. Thus, the wave of ommatidial formation is converted into sequential innervation of the brain (2). Second, R cells in the same developing ommatidium extend axons within a s...

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Temporal Control of Glial Cell Migration in the Drosophila Eye Requires gilgamesh, hedgehog, and Eye Specification Genes

Cited by 90 publications

References 56 publications

Cellular Strategies of Axonal Pathfinding

Cellular Strategies of Axonal Pathfinding

Novel Regulators of Planar Cell Polarity: A Genetic Analysis in Drosophila

Robo-3–mediated repulsive interactions guide R8 axons during Drosophila visual system development

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