Golden Goal collaborates with Flamingo in conferring synaptic-layer specificity in the visual system

Hakeda-Suzuki, Satoko; Berger-Müller, Sandra; Tomasi, Tatiana; Usui, Tadao; Horiuchi, Shinya; Uemura, Tadashi; Suzuki, Takashi

doi:10.1038/nn.2756

Cited by 57 publications

(91 citation statements)

References 47 publications

(58 reference statements)

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“…4A). Based on this and other observations, Gogo was proposed to have an adhesive function at the M1 layer during the early pupal stages, when the R8 axons make a temporal stop at the medulla surface (Tomasi et al, 2008;Hakeda-Suzuki et al, 2011). To determine if YYD tripeptide phosphorylation plays a role in M1 layer recognition, we examined whether mutations in the YYD motif interfere with M1 layer targeting.…”

Section: Research Article Development 139 (4)mentioning

confidence: 89%

“…In Drosophila, three cell surface molecules have been implicated in R8 photoreceptor targeting: Capricious (Shinza-Kameda et al, 2006), the seven-transmembrane cadherin Flamingo (Fmi; Starry Night -FlyBase) (Lee et al, 2003;Senti et al, 2003) and Golden goal (Gogo) (Tomasi et al, 2008;Hakeda-Suzuki et al, 2011). Gogo and Fmi participate in both temporary and final layer targeting.…”

Section: Introductionmentioning

confidence: 99%

“…Gogo and Fmi participate in both temporary and final layer targeting. Gogo contributes to anchoring R8 axons in their temporary layer and is necessary for axon extension to the final target layer in the mid-pupa (Tomasi et al, 2008;Hakeda-Suzuki et al, 2011). How does Gogo regulate these sequential targeting steps?…”

Section: Introductionmentioning

confidence: 99%

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A putative tyrosine phosphorylation site of the cell surface receptor Golden goal is involved in synaptic layer selection in the visual system

et al. 2012

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SUMMARYGolden goal (Gogo) is a cell surface protein that is crucial for proper synaptic layer targeting of photoreceptors (R cells) in the Drosophila visual system. In collaboration with the seven-transmembrane cadherin Flamingo (Fmi), Gogo mediates both temporary and final layer targeting of R-cell axons through its cytoplasmic activity. However, it is not known how Gogo activity is regulated. Here, we show that a conserved Tyr-Tyr-Asp (YYD) tripeptide motif in the Gogo cytoplasmic domain is required for photoreceptor axon targeting. Deleting the YYD motif is sufficient to abolish Gogo function. We demonstrate that the YYD motif is a phosphorylation site and that mutations in the YYD tripeptide impair synaptic layer targeting. Gogo phosphorylation results in axon stopping at the temporary targeting layer, and dephosphorylation is crucial for final layer targeting in collaboration with Fmi. Therefore, both temporary and final layer targeting strongly depend on the Gogo phosphorylation status. Drosophila Insulin-like receptor (DInR) has been reported to regulate the wiring of photoreceptors. We show that insulin signaling is a positive regulator, directly or indirectly, of YYD motif phosphorylation. Our findings indicate a novel mechanism for the regulation of Gogo activity by insulin signaling-mediated phosphorylation. We propose the model that a constant phosphorylation signal is antagonized by a presumably temporal dephosphorylation signal, which creates a permissive signal that controls developmental timing in axon targeting.

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Section: Research Article Development 139 (4)mentioning

confidence: 89%

Section: Introductionmentioning

confidence: 99%

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A putative tyrosine phosphorylation site of the cell surface receptor Golden goal is involved in synaptic layer selection in the visual system

et al. 2012

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“…This occurs probably through axonal retraction, because the initial development of the axonal projection is normal. The function of Flamingo in regulating axon-axon and axon-target interactions is best studied in the developing Drosophila eye, as shown in the work of HakedaSuzuki et al [25] . In each ommatidium, the axons of R1-R8 photoreceptor cells terminate in different layers of the optic lobe: R1-R6 synapse in the lamina, R7 terminates in the M6 layer of the medulla, and R8 in the more superficial M3 layer.…”

Section: Flamingo and Neuronal Morphogenesismentioning

confidence: 99%

Planar cell polarity genes, Celsr1-3, in neural development

2012

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flamingo is among the 'core' planar cell-polarity genes, protein of which belongs to a unique cadherin subfamily.In contrast to the classic cadherins, composed of several extracellular cadherin repeats, one transmembrane domain and one cytoplasmic segment linked to catenin binding, Drosophila Flamingo has seven transmembrane segments and a cytoplasmic tail with no catenin-binding sequence. In Drosophila, Flamingo has pleotropic roles in controlling epithelial polarity and neuronal morphogenesis. Three mammalian orthologs of flamingo, Celsr1-3, are widely expressed in the nervous system. Recent work has shown that Celsr1-3 play important roles in neural development, such as in axon guidance, neuronal migration, and cilium polarity. Celsr1-3 single-gene knockout mice exhibit different phenotypes, but there are cooperative interactions among these genes.

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“…In vivo roles of the Fmi family members have been reported in a number of different contexts of neural development in several animal models (Takeichi 2007;Jan and Jan 2010). These include growth control of dendrites in Drosophila and mammals (Gao et al 2000;Sweeney et al 2002;Reuter et al 2003;Shima et al 2004Shima et al , 2007Kimura et al 2006), target selection of Drosophila photoreceptor axons (Lee et al 2003;Senti et al 2003;Chen and Clandinin 2008;Hakeda-Suzuki et al 2011), axonal navigation and tract formation in mouse brains or Caenorhabditis elegans (Tissir et al 2005;Zhou et al 2008;Steimel et al 2010), and restriction of a migrating trajectory of motor neurons in zebrafish (Wada et al 2006;Wada and Okamoto 2009). In spite of all of these and other studies, downstream molecules of these Fmi family members have been poorly understood in neurons, except for indirect connections of mammalian homologs Celsr2 and Celsr3 to trimeric G proteins (Shima et al 2007).…”

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confidence: 99%

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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Golden Goal collaborates with Flamingo in conferring synaptic-layer specificity in the visual system

Cited by 57 publications

References 47 publications

A putative tyrosine phosphorylation site of the cell surface receptor Golden goal is involved in synaptic layer selection in the visual system

A putative tyrosine phosphorylation site of the cell surface receptor Golden goal is involved in synaptic layer selection in the visual system

Planar cell polarity genes, Celsr1-3, in neural development

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

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