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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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Expression of Slits during neural crest migration. In situ hybridization of Slit2, 1, and 3 demonstrates that Slits are expressed in the mesenchyme at the entry to the gut as well as in the neural tube and somites. (a–c) Whole mounts of stage 17 chicken embryos. (a) Whole mount in situ hybridization with a Slit2 probe reveals that it is expressed in the dorsal neural tube (black arrow), ventral neural tube (white arrow), and gut mesenchyme (black arrowhead). (b and c) Whole mount in situ hybridization with a Slit1 probe reveals that it is expressed in the dorsal neural tube, dorsomedial dermomyotome (red arrow), and gut mesenchyme. (b) A higher magnification of c. (d) Transverse section in situ hybridization through the lumbar level of a stage 17 chick embryo shows Slit2 in the floor plate and developing motor neurons (white arrow), the roof plate of the neural tube (black arrow), and the mesenchyme immediately dorsal to the gut (black arrowhead); the Slit1 pattern (not depicted) looked identical. (e) A similar expression pattern for Slit2 and Slit1 (not depicted) was observed at the hindlimb level of a stage 19 embryo. (f) Slit3 in a stage 16 embryo appeared similar to the other Slits, except that staining was reduced or absent in the floor plate and dorsal neural tube.
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fig1: Expression of Slits during neural crest migration. In situ hybridization of Slit2, 1, and 3 demonstrates that Slits are expressed in the mesenchyme at the entry to the gut as well as in the neural tube and somites. (a–c) Whole mounts of stage 17 chicken embryos. (a) Whole mount in situ hybridization with a Slit2 probe reveals that it is expressed in the dorsal neural tube (black arrow), ventral neural tube (white arrow), and gut mesenchyme (black arrowhead). (b and c) Whole mount in situ hybridization with a Slit1 probe reveals that it is expressed in the dorsal neural tube, dorsomedial dermomyotome (red arrow), and gut mesenchyme. (b) A higher magnification of c. (d) Transverse section in situ hybridization through the lumbar level of a stage 17 chick embryo shows Slit2 in the floor plate and developing motor neurons (white arrow), the roof plate of the neural tube (black arrow), and the mesenchyme immediately dorsal to the gut (black arrowhead); the Slit1 pattern (not depicted) looked identical. (e) A similar expression pattern for Slit2 and Slit1 (not depicted) was observed at the hindlimb level of a stage 19 embryo. (f) Slit3 in a stage 16 embryo appeared similar to the other Slits, except that staining was reduced or absent in the floor plate and dorsal neural tube.

Mentions: We found that the patterns of expression for Slit2 (Fig. 1, a, d, and e), Slit1 (Fig. 1, b and c), and Slit3 (Fig. 1 f) largely overlapped. All were expressed prominently in the splanchnic mesoderm that marks the entrance to the gut. In addition, there was marked expression in the ventral neural tube, notochord, and dorsomedial dermomyotome. Slit1 and Slit2 were expressed strongly in the roof plate, whereas Slit3 had little or no expression in this site. Interestingly, Slit1 and Slit2 were expressed in both the floor plate and in forming motor neuron pools. In contrast, Slit3 was expressed in motor neurons but had low expression in the floor plate. These expression patterns are similar to those noted previously in the mouse (Yuan et al., 1999).


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)

Expression of Slits during neural crest migration. In situ hybridization of Slit2, 1, and 3 demonstrates that Slits are expressed in the mesenchyme at the entry to the gut as well as in the neural tube and somites. (a–c) Whole mounts of stage 17 chicken embryos. (a) Whole mount in situ hybridization with a Slit2 probe reveals that it is expressed in the dorsal neural tube (black arrow), ventral neural tube (white arrow), and gut mesenchyme (black arrowhead). (b and c) Whole mount in situ hybridization with a Slit1 probe reveals that it is expressed in the dorsal neural tube, dorsomedial dermomyotome (red arrow), and gut mesenchyme. (b) A higher magnification of c. (d) Transverse section in situ hybridization through the lumbar level of a stage 17 chick embryo shows Slit2 in the floor plate and developing motor neurons (white arrow), the roof plate of the neural tube (black arrow), and the mesenchyme immediately dorsal to the gut (black arrowhead); the Slit1 pattern (not depicted) looked identical. (e) A similar expression pattern for Slit2 and Slit1 (not depicted) was observed at the hindlimb level of a stage 19 embryo. (f) Slit3 in a stage 16 embryo appeared similar to the other Slits, except that staining was reduced or absent in the floor plate and dorsal neural tube.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2172792&req=5

fig1: Expression of Slits during neural crest migration. In situ hybridization of Slit2, 1, and 3 demonstrates that Slits are expressed in the mesenchyme at the entry to the gut as well as in the neural tube and somites. (a–c) Whole mounts of stage 17 chicken embryos. (a) Whole mount in situ hybridization with a Slit2 probe reveals that it is expressed in the dorsal neural tube (black arrow), ventral neural tube (white arrow), and gut mesenchyme (black arrowhead). (b and c) Whole mount in situ hybridization with a Slit1 probe reveals that it is expressed in the dorsal neural tube, dorsomedial dermomyotome (red arrow), and gut mesenchyme. (b) A higher magnification of c. (d) Transverse section in situ hybridization through the lumbar level of a stage 17 chick embryo shows Slit2 in the floor plate and developing motor neurons (white arrow), the roof plate of the neural tube (black arrow), and the mesenchyme immediately dorsal to the gut (black arrowhead); the Slit1 pattern (not depicted) looked identical. (e) A similar expression pattern for Slit2 and Slit1 (not depicted) was observed at the hindlimb level of a stage 19 embryo. (f) Slit3 in a stage 16 embryo appeared similar to the other Slits, except that staining was reduced or absent in the floor plate and dorsal neural tube.
Mentions: We found that the patterns of expression for Slit2 (Fig. 1, a, d, and e), Slit1 (Fig. 1, b and c), and Slit3 (Fig. 1 f) largely overlapped. All were expressed prominently in the splanchnic mesoderm that marks the entrance to the gut. In addition, there was marked expression in the ventral neural tube, notochord, and dorsomedial dermomyotome. Slit1 and Slit2 were expressed strongly in the roof plate, whereas Slit3 had little or no expression in this site. Interestingly, Slit1 and Slit2 were expressed in both the floor plate and in forming motor neuron pools. In contrast, Slit3 was expressed in motor neurons but had low expression in the floor plate. These expression patterns are similar to those noted previously in the mouse (Yuan et al., 1999).

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