Dendrite branching and self-avoidance are controlled by Turtle, a conserved IgSF protein in <i>Drosophila</i>

Hong, Liu; Ou, Yimiao; Rao, Yong; Meyel, Donald J. van

doi:10.1242/dev.040220

Cited by 57 publications

(75 citation statements)

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“…To identify genes that function with raw to regulate terminal dendrite patterning, we assayed for genetic interactions between raw and known regulators of terminal dendrite development, including genes in the Trc signaling pathway, that regulate dendrite-dendrite repulsion and terminal dendrite adhesion: turtle (tutl), which regulates dendrite-dendrite repulsion; Dscam, which regulates dendrite self-avoidance; and myospheroid (mys), which is required for dendrite-extracellular matrix (ECM) interactions (Emoto et al, 2004;Han et al, 2012;Kim et al, 2012;Koike-Kumagai et al, 2009;Long et al, 2009;Matthews et al, 2007;Soba et al, 2007). On its own, heterozygosity for mutation in raw or any of the other genes had no significant effect on the number of terminal dendrite crossing events, but larvae doubly heterozygous for mutations in raw and Trc signaling pathway genes exhibited significant increases in dendrite-dendrite crossing (Fig.…”

Section: Raw May Function Locally In Dendrites To Regulate Terminal Dmentioning

confidence: 99%

Coordinate control of terminal dendrite patterning and dynamics by the membrane protein Raw

et al. 2015

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The directional flow of information in neurons depends on compartmentalization: dendrites receive inputs whereas axons transmit them. Axons and dendrites likewise contain structurally and functionally distinct subcompartments. Axon/dendrite compartmentalization can be attributed to neuronal polarization, but the developmental origin of subcompartments in axons and dendrites is less well understood. To identify the developmental bases for compartment-specific patterning in dendrites, we screened for mutations that affect discrete dendritic domains in Drosophila sensory neurons. From this screen, we identified mutations that affected distinct aspects of terminal dendrite development with little or no effect on major dendrite patterning. Mutation of one gene, raw, affected multiple aspects of terminal dendrite patterning, suggesting that Raw might coordinate multiple signaling pathways to shape terminal dendrite growth. Consistent with this notion, Raw localizes to branch-points and promotes dendrite stabilization together with the Tricornered (Trc) kinase via effects on cell adhesion. Raw independently influences terminal dendrite elongation through a mechanism that involves modulation of the cytoskeleton, and this pathway is likely to involve the RNA-binding protein Argonaute 1 (AGO1), as raw and AGO1 genetically interact to promote terminal dendrite growth but not adhesion. Thus, Raw defines a potential point of convergence in distinct pathways shaping terminal dendrite patterning.

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Section: Raw May Function Locally In Dendrites To Regulate Terminal Dmentioning

confidence: 99%

Coordinate control of terminal dendrite patterning and dynamics by the membrane protein Raw

et al. 2015

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“…IgSF members Dscam1 and Turtle (Tutl) are also required for self-avoidance of da neurons (Hughes et al 2007;Matthews et al 2007;Soba et al 2007;Long et al 2009). Loss of Dscam1 function leads not only to crossing, but also to bundling of branches, which we rarely found in fmi mutants.…”

Section: Fmi Is Required For Self-avoidance Of Dendritic Branches Of mentioning

confidence: 99%

“…For example, unknown are the identities of interbranch signals and their sensors that are connected to the Trc pathway. Genetic interactions have been sought between trc and Dscam1 or tutl, but positive results have not been obtained (Matthews et al 2007;Soba et al 2007;Long et al 2009). We found an interaction between fmi and trc; between fmi and fry, which encodes an activator of Trc; and between fmi and hpo, an upstream kinase.…”

Section: Possibilities Of Functional Interactions Between Fmi-esn Andmentioning

confidence: 99%

“…One is the Dscam immunoglobulin superfamily (IgSF) in Drosophila and mice (Hughes et al 2007;Matthews et al 2007;Soba et al 2007;Fuerst et al 2008Fuerst et al , 2009, and the other is Turtle (Tutl) of the Dasm1 IgSF in Drosophila (Long et al 2009). Relevant signaling molecules downstream from either Dscam1 or Tutl have not been found, and there is as yet no evidence for a functional relationship between Trc and Dscam1 or Tutl (Matthews et al 2007;Soba et al 2007;Long et al 2009). …”

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confidence: 99%

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The seven-pass transmembrane cadherin Flamingo controls dendritic self-avoidance via its binding to a LIM domain protein, Espinas, in Drosophila sensory neurons

Matsubara¹,

Horiuchi²,

Shimono³

et al. 2011

Genes Dev.

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Members of the Flamingo cadherin family are required in a number of different in vivo contexts of neural development. Even so, molecular identities downstream from the family have been poorly understood. Here we show that a LIM domain protein, Espinas (Esn), binds to an intracellular juxtamembrane domain of Flamingo (Fmi), and that this Fmi-Esn interplay elicits repulsion between dendritic branches of Drosophila sensory neurons. In wild-type larvae, branches of the same class IV dendritic arborization neuron achieve efficient coverage of its two-dimensional receptive field with minimum overlap with each other. However, this self-avoidance was disrupted in a fmi hypomorphic mutant, in an esn knockout homozygote, and in the fmi/esn trans-heterozygote. A functional fusion protein, Fmi:3eGFP, was localized at most of the branch tips, and in a heterologous system, assembly of Esn at cell contact sites required its LIM domain and Fmi. We further show that genes controlling epithelial planar cell polarity (PCP), such as Van Gogh (Vang) and RhoA, are also necessary for the self-avoidance, and that fmi genetically interacts with these loci. On the basis of these and other results, we propose that the Fmi-Esn complex, together with the PCP regulators and the Tricornered (Trc) signaling pathway, executes the repulsive interaction between isoneuronal dendritic branches.

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“…5G,H ) (mirr: 143,984 m 2 Ϯ 7870 (mean Ϯ SEM), n ϭ 16; WT: 170,850 m 2 Ϯ 3490, n ϭ 16; p ϭ 0.0083, Student's two-tailed t test). This was not associated with a change in dendritic self-avoidance (Long et al, 2009) (mirr: 2.74 crossing points/ 1000 m dendritic length Ϯ 0.36 (mean Ϯ SEM), n ϭ 12; WT: 2.58 Ϯ 0.34, n ϭ 10; p ϭ 0.76 Student's two-tailed t test). However, it was correlated with a similar reduction of dendritic branching to 86% of WT (mirr: 380 dendrite ends Ϯ 20 (mean Ϯ SEM), n ϭ 12; WT: 443 Ϯ 10, n ϭ 10; p ϭ 0.026, Student's two-tailed t test).…”

Section: Mirror Is a Localized Ventral Promoter Of Class IV Differentmentioning

confidence: 93%

Convergent Local Identity and Topographic Projection of Sensory Neurons

Karim

Moore²

2011

J. Neurosci.

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Development of sensory neural circuits requires concurrent specification of neuron modality, position, and topographic projections. However, little is understood about how controls over these distinct parameters can unify in a single developmental sequence. To address this question, we have used the nociceptive class IV dendritic arborization neurons in the Drosophila larval body wall as an excellent model that allows precise spatiotemporal dissection of developmental-genetic control over sensory neuron positioning and wiring, and subsequent analysis of its functional significance for sensorimotor behavior. The class IV neurogenetic program is intrinsic to the anterior domain of the embryonic parasegment epithelium. Along the ventrolateral axis of this domain, nociceptive neuron induction requirements depend upon location. Near the ventral midline, both Hedgehog and Epithelial growth factor receptor signaling are required for class IV neurogenesis. In addition, close to the ventral midline, class IV neurogenesis is preceded by expression of the Iroquois factor Mirror that promotes local nociceptive neuron differentiation. Remarkably, Mirror is also required for the proper routing of class IV topographic axonal projections across the midline of the CNS. Manipulation of Mirror activity in class IV neurons retargeted axonal projections and caused concordant changes in larval nociceptive escape behavior. These findings indicate that convergent sensory neuron specification, local differentiation, and topographic wiring are mediated by Mirror, and they suggest an integrated paradigm for position-sensitive neural development.

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Dendrite branching and self-avoidance are controlled by Turtle, a conserved IgSF protein in Drosophila

Cited by 57 publications

References 40 publications

Coordinate control of terminal dendrite patterning and dynamics by the membrane protein Raw

Coordinate control of terminal dendrite patterning and dynamics by the membrane protein Raw

The seven-pass transmembrane cadherin Flamingo controls dendritic self-avoidance via its binding to a LIM domain protein, Espinas, in Drosophila sensory neurons

Convergent Local Identity and Topographic Projection of Sensory Neurons

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