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Dual function of Slit2 in repulsion and enhanced migration of trunk, but not vagal, neural crest cells.

De Bellard ME, Rao Y, Bronner-Fraser M - J. Cell Biol. (2003)

Bottom Line: Accordingly, only trunk neural crest cells express Robo receptors.Conversely, exposure to soluble Slit2 significantly increases the distance traversed by trunk neural crest cells.These results suggest that Slit2 can act bifunctionally, both repulsing and stimulating the motility of trunk neural crest cells.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA.

ABSTRACT
Neural crest precursors to the autonomic nervous system form different derivatives depending upon their axial level of origin; for example, vagal, but not trunk, neural crest cells form the enteric ganglia of the gut. Here, we show that Slit2 is expressed at the entrance of the gut, which is selectively invaded by vagal, but not trunk, neural crest. Accordingly, only trunk neural crest cells express Robo receptors. In vivo and in vitro experiments demonstrate that trunk, not vagal, crest cells avoid cells or cell membranes expressing Slit2, thereby contributing to the differential ability of neural crest populations to invade and innervate the gut. Conversely, exposure to soluble Slit2 significantly increases the distance traversed by trunk neural crest cells. These results suggest that Slit2 can act bifunctionally, both repulsing and stimulating the motility of trunk neural crest cells.

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Effects of Slit2-expressing cells on neural crest migration in vivo. Cells expressing Slit2 or control HEK cells were labeled with the lipophilic dye DiI and implanted onto vagal and/or trunk neural crest migratory pathways. Left panel shows flattened confocal Z-series of whole mounts of embryos stained with the HNK-1 antibody (green) to recognize neural crest cells, and the right panel shows both the neural crest and the injected cells (red) at both vagal and trunk levels. Embryos were analyzed one day after injection. (a–d) At vagal levels, neural crest cells intermixed with both control and Slit2-expressing cells. (g–l) In contrast, at trunk levels, neural crest cells overlapped with control cells (g and h) but appeared to stop (white arrowhead) some distance away from Slit2 cells (i–l). Notice also how trunk neural crest cells circumvent Slit2-expressing cells (white arrow in j). (e and f) Sections through embryos injected with Slit2 show that vagal neural crest freely intermix with Slit2 cells, whereas trunk neural crest cells avoid (white arrowhead) Slit2 cells.
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fig4: Effects of Slit2-expressing cells on neural crest migration in vivo. Cells expressing Slit2 or control HEK cells were labeled with the lipophilic dye DiI and implanted onto vagal and/or trunk neural crest migratory pathways. Left panel shows flattened confocal Z-series of whole mounts of embryos stained with the HNK-1 antibody (green) to recognize neural crest cells, and the right panel shows both the neural crest and the injected cells (red) at both vagal and trunk levels. Embryos were analyzed one day after injection. (a–d) At vagal levels, neural crest cells intermixed with both control and Slit2-expressing cells. (g–l) In contrast, at trunk levels, neural crest cells overlapped with control cells (g and h) but appeared to stop (white arrowhead) some distance away from Slit2 cells (i–l). Notice also how trunk neural crest cells circumvent Slit2-expressing cells (white arrow in j). (e and f) Sections through embryos injected with Slit2 show that vagal neural crest freely intermix with Slit2 cells, whereas trunk neural crest cells avoid (white arrowhead) Slit2 cells.

Mentions: Cells expressing Slit2 were introduced onto neural crest migratory pathways. HEK293 cells transfected either with human Slit2 or control vectors (Li et al., 1999) were labeled with DiI and microinjected onto trunk and/or vagal neural crest migratory pathways in early chick embryos. Vagal level injections were performed into somites 1–7 of stage 10–12 chicken embryos (Hamburger and Hamilton, 1951). When injected into this location, the labeled cells appeared to localize in ventral sites around the dorsal aorta, as has been previously described for injections of cells or latex beads (Bronner-Fraser and Cohen, 1980; Bronner-Fraser, 1982). Vagal neural crest cells migrate from the neural tube and proceed ventrally to populate the dorsal root and sympathetic ganglia. Other vagal crest cells migrate further ventrally to penetrate the gut. When encountering Slit2-secreting cells at the level of the aorta, the vagal neural crest cells appeared to mix and closely associate with Slit2-secreting cells (Fig. 4, c–e). Their distribution pattern was similar to that observed after injection of parental control cells (Figs. 4, a and b). Little or no avoidance behavior was observed after either injection of Slit2 cells (n = 1/8 embryos) or control cells (n = 0/6 embryos) at vagal levels.


Dual function of Slit2 in repulsion and enhanced migration of trunk, but not vagal, neural crest cells.

De Bellard ME, Rao Y, Bronner-Fraser M - J. Cell Biol. (2003)

Effects of Slit2-expressing cells on neural crest migration in vivo. Cells expressing Slit2 or control HEK cells were labeled with the lipophilic dye DiI and implanted onto vagal and/or trunk neural crest migratory pathways. Left panel shows flattened confocal Z-series of whole mounts of embryos stained with the HNK-1 antibody (green) to recognize neural crest cells, and the right panel shows both the neural crest and the injected cells (red) at both vagal and trunk levels. Embryos were analyzed one day after injection. (a–d) At vagal levels, neural crest cells intermixed with both control and Slit2-expressing cells. (g–l) In contrast, at trunk levels, neural crest cells overlapped with control cells (g and h) but appeared to stop (white arrowhead) some distance away from Slit2 cells (i–l). Notice also how trunk neural crest cells circumvent Slit2-expressing cells (white arrow in j). (e and f) Sections through embryos injected with Slit2 show that vagal neural crest freely intermix with Slit2 cells, whereas trunk neural crest cells avoid (white arrowhead) Slit2 cells.
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Related In: Results  -  Collection

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fig4: Effects of Slit2-expressing cells on neural crest migration in vivo. Cells expressing Slit2 or control HEK cells were labeled with the lipophilic dye DiI and implanted onto vagal and/or trunk neural crest migratory pathways. Left panel shows flattened confocal Z-series of whole mounts of embryos stained with the HNK-1 antibody (green) to recognize neural crest cells, and the right panel shows both the neural crest and the injected cells (red) at both vagal and trunk levels. Embryos were analyzed one day after injection. (a–d) At vagal levels, neural crest cells intermixed with both control and Slit2-expressing cells. (g–l) In contrast, at trunk levels, neural crest cells overlapped with control cells (g and h) but appeared to stop (white arrowhead) some distance away from Slit2 cells (i–l). Notice also how trunk neural crest cells circumvent Slit2-expressing cells (white arrow in j). (e and f) Sections through embryos injected with Slit2 show that vagal neural crest freely intermix with Slit2 cells, whereas trunk neural crest cells avoid (white arrowhead) Slit2 cells.
Mentions: Cells expressing Slit2 were introduced onto neural crest migratory pathways. HEK293 cells transfected either with human Slit2 or control vectors (Li et al., 1999) were labeled with DiI and microinjected onto trunk and/or vagal neural crest migratory pathways in early chick embryos. Vagal level injections were performed into somites 1–7 of stage 10–12 chicken embryos (Hamburger and Hamilton, 1951). When injected into this location, the labeled cells appeared to localize in ventral sites around the dorsal aorta, as has been previously described for injections of cells or latex beads (Bronner-Fraser and Cohen, 1980; Bronner-Fraser, 1982). Vagal neural crest cells migrate from the neural tube and proceed ventrally to populate the dorsal root and sympathetic ganglia. Other vagal crest cells migrate further ventrally to penetrate the gut. When encountering Slit2-secreting cells at the level of the aorta, the vagal neural crest cells appeared to mix and closely associate with Slit2-secreting cells (Fig. 4, c–e). Their distribution pattern was similar to that observed after injection of parental control cells (Figs. 4, a and b). Little or no avoidance behavior was observed after either injection of Slit2 cells (n = 1/8 embryos) or control cells (n = 0/6 embryos) at vagal levels.

Bottom Line: Accordingly, only trunk neural crest cells express Robo receptors.Conversely, exposure to soluble Slit2 significantly increases the distance traversed by trunk neural crest cells.These results suggest that Slit2 can act bifunctionally, both repulsing and stimulating the motility of trunk neural crest cells.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA.

ABSTRACT
Neural crest precursors to the autonomic nervous system form different derivatives depending upon their axial level of origin; for example, vagal, but not trunk, neural crest cells form the enteric ganglia of the gut. Here, we show that Slit2 is expressed at the entrance of the gut, which is selectively invaded by vagal, but not trunk, neural crest. Accordingly, only trunk neural crest cells express Robo receptors. In vivo and in vitro experiments demonstrate that trunk, not vagal, crest cells avoid cells or cell membranes expressing Slit2, thereby contributing to the differential ability of neural crest populations to invade and innervate the gut. Conversely, exposure to soluble Slit2 significantly increases the distance traversed by trunk neural crest cells. These results suggest that Slit2 can act bifunctionally, both repulsing and stimulating the motility of trunk neural crest cells.

Show MeSH
Related in: MedlinePlus