Respective roles of the DRL receptor and its ligand WNT5 in<i>Drosophila</i>mushroom body development

Grillenzoni, Nicola; Flandre, Adrien; Lasbleiz, Christelle; Dura, Jean-Maurice

doi:10.1242/dev.02876

Cited by 33 publications

(36 citation statements)

References 40 publications

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“…We searched for ligands of the PCP components that could participate in the axonal development of the MB. Wnt5, which functions as a repulsive guidance cue for Derailed (Drl) in the embryonic CNS (Yoshikawa et al, 2003), has been previously shown to be required for the development of the MB (Grillenzoni et al, 2007). As reported by Grillenzoni et al (2007), we also observed that Wnt5 D7 mutants showed a loss of the ␣/␤ lobes in D21 and dsh 1 mutants, respectively (***p Ͻ 0.001, Fisher's exact test).…”

Section: Drosophila Pcp Components Are Expressed In the Mbsupporting

confidence: 83%

“…in the rescue experiments of the PCP mutants. Because it was reported that the Wnt5 mutant phenotype was rescued by restoring Wnt5 expression using MB-specific Gal4 lines (Grillenzoni et al, 2007), we confirmed this result with a different mutant allele of Wnt5 (Wnt5 D7 ) than was used by Grillenzoni et al (Wnt5 400 ). Whereas the Wnt5 mutant showed the posterior aggregation, the lobe loss and the lobe reduction phenotype with a penetrance of 3.13, 64.4, and 0.00%, respectively, the MB-specific expression of Wnt5 suppressed these phenotypes to 0.00, 5.00, and 36.0% using OK107-Gal4, 0.00, 24.0, and 21.0% using 247-Gal4, and 0.00, 35.7, and 21.4% using c739-Gal4 (Fig.…”

Section: Wnt5 Is Broadly Expressed In the Developing Brainsupporting

confidence: 77%

“…In this study, we demonstrated that the PCP genes regulated axonal morphogenesis of the MB and genetically interacted during this process. Moreover, we found that Wnt5, which has been previously reported to be required for the development of the MB (Grillenzoni et al, 2007), genetically interacted with the PCP components. These findings emphasize the importance of Wnt5 and its downstream PCP signal in the axonal development of the MB.…”

Section: Discussionmentioning

confidence: 51%

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The Wnt5/Planar Cell Polarity Pathway Regulates Axonal Development of theDrosophilaMushroom Body Neuron

Shimizu¹,

Sato²,

Tabata³

2011

J. Neurosci.

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Axonal development is a fundamental process for circuit formation in the nervous system and is dependent on many cellular events, including axon initiation, elongation, guidance, and branching. The molecular mechanisms underlying these events have been well studied, especially for axon guidance. In the presence of a guidance cue, the polarization of a growth cone precedes the turning response, which is one example of the diverse forms of cell polarity. Planar cell polarity (PCP) is another example of cell polarity. Although some PCP genes are required for axonal tract formation in vertebrates, it remains elusive whether these genes participate in a common PCP pathway concertedly. Here, we show that essential PCP signaling components, encoded by frizzled ( fz), strabismus (stbm), flamingo ( fmi), and dishevelled (dsh), are cooperatively required for axonal targeting and branching of the Drosophila mushroom body (MB) neurons. A detailed analysis of these mutants revealed that these components were required for the correct targeting and bifurcation of axons. In addition, we suggest that Wnt5 functions as a ligand in the PCP pathway in this process. Wnt5 mutants showed similar phenotypes to PCP mutants at the single-cell level and genetically interacted with PCP genes. Wnt5 was broadly expressed in the developing brain. We propose that Wnt5 and the PCP pathway concertedly regulate axonal development of the MB.

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Section: Drosophila Pcp Components Are Expressed In the Mbsupporting

confidence: 83%

Section: Wnt5 Is Broadly Expressed In the Developing Brainsupporting

confidence: 77%

Section: Discussionmentioning

confidence: 51%

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The Wnt5/Planar Cell Polarity Pathway Regulates Axonal Development of theDrosophilaMushroom Body Neuron

Shimizu¹,

Sato²,

Tabata³

2011

J. Neurosci.

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“…Ryk is important for establishing planar polarity during neural tube formation [13][14][15], differentiation of mouse cortical and dopaminergic midbrain progenitors [16,17], and specification and migration of GABAergic interneurons during cortical development [18,19]. Derailed is also required for mushroom body development, glomerular patterning, neuromuscular junction formation, synaptogenesis and memory and learning in the fly [20][21][22][23]. These other facets of Ryk function have been comprehensively covered in several recent reviews [24][25][26].…”

Section: Ryk a Novel Wnt Receptormentioning

confidence: 99%

The Yin and Yang of Wnt/Ryk axon guidance in development and regeneration

Clark

Liu

Cooper

2014

Sci. China Life Sci.

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In the developing embryo, nascent axons navigate towards their specific targets to establish the intricate network of axonal connections linking neurons within the mature nervous system. Molecular navigational systems comprising repulsive and attractive guidance cues form chemotactic gradients along the pathway of the exploring growth cone. Axon-bound receptors detect these gradients and determine the trajectory of the migrating growth cone. In contrast to their benevolent role in the developing nervous system, repulsive guidance receptors are detrimental to the axon's ability to regenerate after injury in the adult. In this review we explore the essential and beneficial role played by the chemorepulsive Wnt receptor, Ryk/Derailed in axon navigation in the embryonic nervous system (the Yin function). Specifically, we focus on the role of Wnt5a/Rykmediated guidance in the establishment of two major axon tracts in the mammalian central nervous system, the corticospinal tract and the corpus callosum. Recent studies have also identified Ryk as a major suppressor of axonal regeneration after spinal cord injury. Thus, we also discuss this opposing aspect of Ryk function in axonal regeneration where its activity is a major impediment to axon regrowth (the Yang function).Ryk, Derailed, Wnt, Wnt signalling, axon guidance, axonal regeneration, spinal cord injury Citation:Clark CEJ, Liu YB, Cooper HM. The Yin and Yang of Wnt/Ryk axon guidance in development and regeneration.

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“…Although apparently lacking kinase activity, a human TRKA (NTRK1)-RYK fusion protein was shown to activate the MAPK pathway when bound by NGF (Katso et al, 1999), suggesting that RYKs transduce extracellular signals to downstream targets within the cell. Recent studies (Grillenzoni et al, 2007;Yao et al, 2007) have shown that DRL can also act to antagonize WNT5 function in the Drosophila post-embryonic CNS. These functions require the WIF domain, but not the intracellular region of DRL.…”

Section: Introductionmentioning

confidence: 99%

Src family kinases are required for WNT5 signaling through the Derailed/RYK receptor in theDrosophilaembryonic central nervous system

et al. 2008

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Members of the RYK/Derailed family have recently been shown to regulate axon guidance in both Drosophila and mammals by acting as Wnt receptors. Little is known about how the kinase activity-deficient RYKs transduce Wnt signals. Here, we show that the non-receptor Src family tyrosine kinases, SRC64B and SRC42A, are involved in WNT5-mediated signaling through Derailed in the Drosophila embryonic central nervous system. Analysis of animals lacking SRC64B and SRC42A reveals defects in commissure formation similar to those observed in Wnt5 and derailed mutants. Reductions in SRC64B expression levels suppress a Wnt5/derailed-dependent dominant gain-of-function phenotype, and increased levels of either SRC64B or SRC42A enhance Wnt5/derailed-mediated axon commissure switching. Derailed and SRC64B form a complex, which contains catalytically active SRC64B, the formation or stability of which requires SRC64B kinase activity. Furthermore, Derailed is phosphorylated in a SRC64B-dependent manner and coexpression of Derailed and SRC64B results in the activation of SRC64B. The mammalian orthologs of Derailed and SRC64B also form complexes, suggesting that Src roles in RYK signaling are conserved. Finally, we show that coexpression of WNT5 and Derailed has no apparent effect upon TCF/LEF-dependent transcription, suggesting that the WNT5/Derailed signaling pathway is unlikely to directly regulate canonical Wnt pathway targets. Together, these findings indicate that the Src family kinases play novel roles in WNT5/Derailed-mediated signaling.

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Respective roles of the DRL receptor and its ligand WNT5 inDrosophilamushroom body development

Cited by 33 publications

References 40 publications

The Wnt5/Planar Cell Polarity Pathway Regulates Axonal Development of theDrosophilaMushroom Body Neuron

The Wnt5/Planar Cell Polarity Pathway Regulates Axonal Development of theDrosophilaMushroom Body Neuron

The Yin and Yang of Wnt/Ryk axon guidance in development and regeneration

Src family kinases are required for WNT5 signaling through the Derailed/RYK receptor in theDrosophilaembryonic central nervous system

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