Neuroepithelial cells require fucosylated glycans to guide the migration of vagus motor neuron progenitors in the developing zebrafish hindbrain

Ohata, Shinya; Kinoshita, Shigeharu; Aoki, Ryo; Tanaka, Hideomi; Wada, Hironori; Tsuruoka-Kinoshita, Sachiko; Tsuboi, Takashi; Watabe, Shugo; Okamoto, Hitoshi

doi:10.1242/dev.033290

Cited by 39 publications

(46 citation statements)

References 41 publications

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“…S1D). As in previous studies (Ohata et al, 2009), knocking down gmds, the first enzyme in the de novo GDP-Fuc synthetic pathway decreased fucosylation in zebrafish embryos, as assessed by AAL (Fig. 1D).…”

Section: Resultssupporting

confidence: 84%

“…Limiting fucosylation in mice is known to cause developmental defects including early embryonic death (Du et al, 2010; Smith et al, 2002), neuronal migration disorders (Ohata et al, 2009), skeletal abnormalities and other defects (Hayes et al, 2013; Ma et al, 2006). However, the consequence of excess fucosylation has not been examined.…”

Section: Resultsmentioning

confidence: 99%

“…S1C). To independently assess whether mSlc35c1 induced dorsalization was through GDP-Fuc transporter function, we injected mSlc35c1 together with morpholino to knock down GDP-mannose 4,6-dehydratase ( gmds ) (Ohata et al, 2009) (Fig. S1D).…”

Section: Resultsmentioning

confidence: 99%

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Negative feedback regulation of Wnt signaling via N-linked fucosylation in zebrafish

Feng

Jiang

et al. 2014

Developmental Biology

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Summary L-fucose, a monosaccharide widely distributed in eukaryotes and certain bacteria, is a determinant of many functional glycans that play central roles in numerous biological processes. The molecular mechanism, however, by which fucosylation mediates these processes remains largely elusive. To study how changes in fucosylation impact embryonic development, we up-regulated N-linked fucosylation via over-expression of a key GDP-Fucose transporter, Slc35c1, in zebrafish. We show that Slc35c1 overexpression causes elevated N-linked fucosylation and disrupts embryonic patterning in a transporter activity dependent manner. We demonstrate that patterning defects associated with enhanced N-linked fucosylation are due to diminished canonical Wnt signaling. Chimeric analyses demonstrate that elevated Slc35c1 expression in receiving cells decreases the signaling range of Wnt8a during zebrafish embryogenesis. Moreover, we provide biochemical evidence that this decrease is associated with degradation of Wnt8 ligand and elevated Lrp6 coreceptor, which we show are both substrates for N-linked fucosylation in zebrafish embryos. Strikingly, slc35c1 expression is regulated by canonical Wnt signaling. These results suggest that Wnt limits its own signaling activity in part via up-regulation of a transporter, slc35c1 that promotes terminal fucosylation and thereby limits Wnt activity.

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Section: Resultssupporting

confidence: 84%

Section: Resultsmentioning

confidence: 99%

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Negative feedback regulation of Wnt signaling via N-linked fucosylation in zebrafish

Feng

Jiang

et al. 2014

Developmental Biology

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“…However, as informative as those studies are, their conclusions would not be supported if they were found to disagree with in vivo results. Although in vivo observations have been made in zebrafish (31)(32)(33)(34), similar studies have proven far more difficult in mammals. One report showed in vivo analysis of interneuron migration in mouse embryos (35), but analyses in this report were of low resolution, unable to provide detailed description of the dynamics of individual neurons and their organelles.…”

Section: Branch Rather Than the Turning Of A Lp Tip Is Critical Formentioning

confidence: 99%

Dynamics of the leading process, nucleus, and Golgi apparatus of migrating cortical interneurons in living mouse embryos

Yanagida

Miyoshi

Toyokuni

et al. 2012

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

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Precisely arranged cytoarchitectures such as layers and nuclei depend on neuronal migration, of which many in vitro studies have revealed the mode and underlying mechanisms. However, how neuronal migration is achieved in vivo remains unknown. Here we established an imaging system that allows direct visualization of cortical interneuron migration in living mouse embryos. We found that during nucleokinesis, translocation of the Golgi apparatus either precedes or occurs in parallel to that of the nucleus, suggesting the existence of both a Golgi/centrosome-dependent and -independent mechanism of nucleokinesis. Changes in migratory direction occur when the nucleus enters one of the leading process branches, which is accompanied by the retraction of other branches. The nucleus occasionally swings between two branches before translocating into one of them, the occurrence of which is most often preceded by Golgi apparatus translocation into that branch. These in vivo observations provide important insight into the mechanisms of neuronal migration and demonstrate the usefulness of our system for studying dynamic events in living animals.cortex | GABAergic interneuron | in utero electroporation | in vivo imaging N euronal migration is a critical step in the construction of the nervous system. During development, neurons migrate from the sites of their birth to their final destinations, where they form neuronal architectures, such as laminated structures and nuclei, that are necessary for information processing in the nervous system.Because neuronal migration is a dynamic phenomenon, realtime imaging could provide important insight into its mechanisms. Studies using real-time imaging of neurons in dissociated culture have demonstrated various aspects of neuronal migration, including the fact that radial fibers (1) and neighboring cells (2) act as the substrate for migration and the molecular mechanisms driving nucleokinesis (3, 4). Real-time imaging has also helped reveal the dynamics and roles of cytoplasmic organelles and cytoskeletal components, such as the centrosome (5-9), microtubules (9), and even of some molecules like calcium (10) and actin (7,11,12) during migration. In addition, slice and explant preparations have demonstrated aspects of migratory behaviors, including locomotion and translocation (13), branch-induced changes in migratory direction (14), multidirectional migration (15), random-walk-like behavior (16), pausing behavior, and the transition from tangential to radial migration (17).However, as informative as these neural migration studies are, they are limited because they are all in vitro and do not necessarily show neuronal behaviors in vivo. Here, we observed migrating neurons in the brain of living mouse embryos and analyzed their behavior, including the dynamics of the nucleus and the Golgi apparatus. We took advantage of the fact that cortical interneurons tangentially migrate near the surface of the cortex. These neurons are generated in the ganglionic eminences (GEs) in the basal forebrain a...

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“…Mutagenesis was carried out as described previously (Ohata et al, 2009;Solnica-Krezel et al, 1994;Tanaka et al, 2007;Wada et al, 2005Wada et al, , 2006. Mutation was induced in the male germ cells using N-ethyl-Nnitrosourea (ENU, Sigma-Aldrich, St. Louis, MO).…”

Section: Mutagenesismentioning

confidence: 99%

Islet1 selectively promotes peripheral axon outgrowth in Rohon‐Beard primary sensory neurons

Tanaka

Nojima

Watanabe

et al. 2010

Developmental Dynamics

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We isolated a novel zebrafish mutant, lullaby (llb), and showed that the llb locus encodes the zebrafish orthologue of isl1. Rohon-Beard (RB) primary sensory neurons are multipolar neurons that extend their central axons longitudinally within the spinal cord and also extend their peripheral axons under the skin. In llb embryos, the outgrowth of the peripheral axons of RB neurons was selectively impaired, which correlated with down-regulation of the expression of dihydropyrimidinase-like 3 (dpysl3, also known as collapsin response mediator protein 4, crmp4). Antisense morpholino oligonucleotide (AMO)-mediated knockdown of dpysl3 inhibited the outgrowth of the peripheral axons of RB neurons, and semaphorin 3d (sema3d) AMO enhanced this effect. These data indicate that Dpysl3 is cooperating with Sema3d in the peripheral axon outgrowth, and Isl1 is required for the selective outgrowth of the peripheral axons of RB neurons by maintaining the expression of dpysl3. Developmental Dynamics 240:9-22,

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Neuroepithelial cells require fucosylated glycans to guide the migration of vagus motor neuron progenitors in the developing zebrafish hindbrain

Cited by 39 publications

References 41 publications

Negative feedback regulation of Wnt signaling via N-linked fucosylation in zebrafish

Negative feedback regulation of Wnt signaling via N-linked fucosylation in zebrafish

Dynamics of the leading process, nucleus, and Golgi apparatus of migrating cortical interneurons in living mouse embryos

Islet1 selectively promotes peripheral axon outgrowth in Rohon‐Beard primary sensory neurons

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