Wnt activity guides facial branchiomotor neuron migration, and involves the PCP pathway and JNK and ROCK kinases

Vivancos, Valérie; Chen, Ping Helen; Spassky, Nathalie; Qian, Dong; Dabdoub, Alain; Kelley, Matthew W.; Studer, Michèle; Guthrie, Sarah

doi:10.1186/1749-8104-4-7

Cited by 83 publications

(135 citation statements)

References 66 publications

(95 reference statements)

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“…We favor a model in which the importance of the second cell is not in having pioneer-like capacity, but rather in being the closest FBMN to the pioneer, serving to link the pioneer to follower FBMNs. Much previous work examining FBMN migration has focused on the PCP pathway; several labs have shown that multiple components of the PCP pathway are crucial for FBMN migration both in zebrafish and in mouse Jessen et al, 2002;Carreira-Barbosa et al, 2003;Bingham et al, 2005;Wada et al, 2005;Wada et al, 2006;Rohrschneider et al, 2007;Vivancos et al, 2009;Qu et al, 2010;Walsh et al, 2011;Glasco et al, 2012). Our analysis of pioneer neurons and the MLF supports a model in which FBMN migration requires additional inputs beyond PCP signaling.…”

Section: Research Articlesupporting

confidence: 67%

Axon tracts guide zebrafish facial branchiomotor neuron migration through the hindbrain

Wanner

Prince

2013

Development

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SUMMARYAppropriate localization of neurons within the brain is a crucial component of the establishment of neural circuitry. In the zebrafish hindbrain, the facial branchiomotor neurons (FBMNs) undergo a chain-like tangential migration from their birthplace in rhombomere (r) 4 to their final destination in r6/r7. Here, we report that ablation of either the cell body or the trailing axon of the leading FBMN, or 'pioneer' neuron, blocks the migration of follower FBMNs into r5. This demonstrates that the pioneer neuron and its axon are crucial to the early migration of FBMNs. Later migration from r5 to r6 is not dependent on pioneer neurons but on the medial longitudinal fasciculus (MLF), a bundle of axons lying ventral to the FBMNs. We find that MLF axons enter r5 only after the pioneer neuron has led several followers into this region; the MLF is then contacted by projections from the FBMNs. The interactions between FBMNs and the MLF are important for migration from r5 to r6, as blocking MLF axons from entering the hindbrain can stall FBMN migration in r5. Finally, we have found that the adhesion molecule Cdh2 (N-cadherin) is important for interactions between the MLF and FBMNs, as well as for interactions between the trailing axon of the pioneer neuron and follower FBMNs. Interestingly, migration of pioneer neurons is independent of both the MLF and Cdh2, suggesting pioneer migration relies on independent cues.

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Section: Research Articlesupporting

confidence: 67%

Axon tracts guide zebrafish facial branchiomotor neuron migration through the hindbrain

Wanner

Prince

2013

Development

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“…In the nervous system, Fz receptors mediate a range of functions from neuronal differentiation (Van Raay et al, 2005) to cell survival Wang et al, 2001), cell polarity (Prasad and Clark, 2006), cell migration (Pan et al, 2006;Vivancos et al, 2009), axon guidance (Lyuksyutova et al, 2003;Wang et al, 2002) and synapse formation (Varela-Nallar et al, 2009;Klassen and Shen, 2007). Here, we focus our attention on Fz5, previously shown to regulate neuronal development .…”

Section: Discussionmentioning

confidence: 99%

“…In the nervous system, Fzs mediate a range of functions from neuronal differentiation (Van Raay et al, 2005) to cell polarity (Prasad and Clark, 2006), cell migration (Pan et al, 2006;Vivancos et al, 2009), axon guidance (Lyuksyutova et al, 2003;Wang et al, 2002) and cell survival . In Drosophila, the Wnt protein Wingless (Wg) activates the Fz2 receptor, present at both sides of the neuromuscular synapse, to regulate pre-and postsynaptic signalling (Ataman et al, 2008;Packard et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Frizzled-5, a receptor for the synaptic organizer Wnt7a, regulates activity-mediated synaptogenesis

2010

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SUMMARYWnt proteins play a crucial role in several aspects of neuronal circuit formation. Wnts can signal through different receptors including Frizzled, Ryk and Ror2. In the hippocampus, Wnt7a stimulates the formation of synapses; however, its receptor remains poorly characterized. Here, we demonstrate that Frizzled-5 (Fz5) is expressed during the peak of synaptogenesis in the mouse hippocampus. Fz5 is present in synaptosomes and colocalizes with the pre-and postsynaptic markers vGlut1 and PSD-95. Expression of Fz5 during early stages of synaptogenesis increases the number of presynaptic sites in hippocampal neurons. Conversely, Fz5 knockdown or the soluble Fz5-CRD domain (Fz5CRD), which binds to Wnt7a, block the ability of Wnt7a to stimulate synaptogenesis. Increased neuronal activity induced by K + depolarization or by high-frequency stimulation (HFS), known to induce synapse formation, raises the levels of Fz5 at the cell surface. Importantly, both stimuli increase the localization of Fz5 at synapses, an effect that is blocked by Wnt antagonists or Fz5CRD. Conversely, low-frequency stimulation, which reduces the number of synapses, decreases the levels of surface Fz5 and the percentage of synapses containing the receptor. Interestingly, Fz5CRD abolishes HFS-induced synapse formation. Our results indicate that Fz5 mediates the synaptogenic effect of Wnt7a and that its localization to synapses is regulated by neuronal activity, a process that depends on endogenous Wnts. These findings support a model where neuronal activity and Wnts increase the responsiveness of neurons to Wnt signalling by recruiting Fz5 receptor at synaptic sites.

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“…This finding stems primarily from studies of mouse and zebrafish facial branchiomotor neurons (FBMNs), which originate ventrally in hindbrain rhombomere (r)4 and undergo highly stereotypical posterior migration along the floorplate to r6 and r7 (Wanner et al, 2013). Mutations in the genes encoding Vangl2, Pk1, Fz3 and Celsr2 all prevent FBMN migration in zebrafish and mice, as do Scrib and Ptk7 mutations Glasco et al, 2012;Mapp et al, 2011;Qu et al, 2010;Vivancos et al, 2009;Wada et al, 2005Wada et al, , 2006Yang et al, 2014) (Table 1). The role of Wnt ligands in FBMN migration is uncertain: mice lacking Wnt5a have a mild defect whereas Wnt4a, Wnt5a and Wnt11r mutants in zebrafish all exhibit normal FBMN migration (Vivancos et al, 2009) (our unpublished results).…”

Section: Pcp Signaling In Neuronal Migrationmentioning

confidence: 99%

Planar cell polarity in moving cells: think globally, act locally

2017

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The planar cell polarity (PCP) pathway is best known for its role in polarizing epithelial cells within the plane of a tissue but it also plays a role in a range of cell migration events during development. The mechanism by which the PCP pathway polarizes stationary epithelial cells is well characterized, but how PCP signaling functions to regulate more dynamic cell behaviors during directed cell migration is much less understood. Here, we review recent discoveries regarding the localization of PCP proteins in migrating cells and their impact on the cell biology of collective and individual cell migratory behaviors.

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Wnt activity guides facial branchiomotor neuron migration, and involves the PCP pathway and JNK and ROCK kinases

Cited by 83 publications

References 66 publications

Axon tracts guide zebrafish facial branchiomotor neuron migration through the hindbrain

Axon tracts guide zebrafish facial branchiomotor neuron migration through the hindbrain

Frizzled-5, a receptor for the synaptic organizer Wnt7a, regulates activity-mediated synaptogenesis

Planar cell polarity in moving cells: think globally, act locally

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