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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 Robos during neural crest migration. Whole mount in situ hybridization with Robo1 and Robo2 probe reveals that the receptor is expressed in the trunk neural tube, on migrating trunk neural crest cells within the somites, and in the dermomyotome, but is not expressed by vagal neural crest cells. (a) In a stage 15 chicken embryo, there is no staining for Robo2 at vagal levels (bracket) though there is staining at truncal levels. (b and c) At stage 18 during the peak of neural crest migration, Robo1 (b) and Robo2 (c) are strongly expressed in neural crest cells at the trunk levels (black arrows) but not in the vagal region (brackets). (d) Robo2 labeling in the head of a stage 15 embryo shows staining on the dorsal half of the otic vesicle (ov), trigeminal placode, and dorsal neurons in the mesencephalon; the posterior part of the second/hyoid branchial arch is also positive for Robo2 (arrowhead). (e–g) At stage 20, when neural crest cells are condensing to form the dorsal root ganglia (arrows), Robo1 (e) and Robo2 (g) are strongly expressed in trunk, but not vagal (brackets), regions. (f) The same stage embryo labeled with HNK-1 shows neural crest cells migrating and beginning to condense into dorsal root ganglia at both vagal and trunk levels.
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fig2: Expression of Robos during neural crest migration. Whole mount in situ hybridization with Robo1 and Robo2 probe reveals that the receptor is expressed in the trunk neural tube, on migrating trunk neural crest cells within the somites, and in the dermomyotome, but is not expressed by vagal neural crest cells. (a) In a stage 15 chicken embryo, there is no staining for Robo2 at vagal levels (bracket) though there is staining at truncal levels. (b and c) At stage 18 during the peak of neural crest migration, Robo1 (b) and Robo2 (c) are strongly expressed in neural crest cells at the trunk levels (black arrows) but not in the vagal region (brackets). (d) Robo2 labeling in the head of a stage 15 embryo shows staining on the dorsal half of the otic vesicle (ov), trigeminal placode, and dorsal neurons in the mesencephalon; the posterior part of the second/hyoid branchial arch is also positive for Robo2 (arrowhead). (e–g) At stage 20, when neural crest cells are condensing to form the dorsal root ganglia (arrows), Robo1 (e) and Robo2 (g) are strongly expressed in trunk, but not vagal (brackets), regions. (f) The same stage embryo labeled with HNK-1 shows neural crest cells migrating and beginning to condense into dorsal root ganglia at both vagal and trunk levels.

Mentions: Trunk, but not vagal, neural crest cells express both Robo1 and Robo2 receptors (Figs. 2 and 3). Whole mount in situ hybridization reveals Robo receptors on neural crest cells as they migrate through the trunk somites (Fig. 2, a–c, e, and g). However, neural crest cells at vagal levels, which can be visualized by their expression of the HNK-1 epitope (Fig. 2 f), lack detectable Robo receptors. Robo1 expression was similar to that of Robo2 but initiated at later stages. By section in situ hybridization, which gives better cellular resolution, we noted that Robo1 (Fig. 3, a and b) and Robo2 (Fig. 3, c and d) were expressed on migrating trunk neural crest cells. In contrast, vagal neural crest cells lacked Robo receptor expression above background (Fig. 3, e–h). Not all HNK-1+ migrating trunk neural crest cells were Robo+ during early stages of migration. With developmental age, the levels of Robos on migrating neural crest cells appeared to increase such that late migrating trunk neural crest cells expressed high levels of both receptors (see Fig. S1, available at http://www.jcb.org/cgi/content/full/jcb.200301041/DC1). In addition to the neural crest, Robo1 is seen in motor neurons. Robo2 appears throughout the neural tube with the exception of the ventral-most region. All Robos are expressed at low levels in the dermomyotome. These observations confirm and extend previous work by others in mouse (Holmes et al., 1998; Yuan et al., 1999) and chick embryos (Li et al., 1999; Holmes and Niswander, 2001; Vargesson et al., 2001).


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 Robos during neural crest migration. Whole mount in situ hybridization with Robo1 and Robo2 probe reveals that the receptor is expressed in the trunk neural tube, on migrating trunk neural crest cells within the somites, and in the dermomyotome, but is not expressed by vagal neural crest cells. (a) In a stage 15 chicken embryo, there is no staining for Robo2 at vagal levels (bracket) though there is staining at truncal levels. (b and c) At stage 18 during the peak of neural crest migration, Robo1 (b) and Robo2 (c) are strongly expressed in neural crest cells at the trunk levels (black arrows) but not in the vagal region (brackets). (d) Robo2 labeling in the head of a stage 15 embryo shows staining on the dorsal half of the otic vesicle (ov), trigeminal placode, and dorsal neurons in the mesencephalon; the posterior part of the second/hyoid branchial arch is also positive for Robo2 (arrowhead). (e–g) At stage 20, when neural crest cells are condensing to form the dorsal root ganglia (arrows), Robo1 (e) and Robo2 (g) are strongly expressed in trunk, but not vagal (brackets), regions. (f) The same stage embryo labeled with HNK-1 shows neural crest cells migrating and beginning to condense into dorsal root ganglia at both vagal and trunk levels.
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fig2: Expression of Robos during neural crest migration. Whole mount in situ hybridization with Robo1 and Robo2 probe reveals that the receptor is expressed in the trunk neural tube, on migrating trunk neural crest cells within the somites, and in the dermomyotome, but is not expressed by vagal neural crest cells. (a) In a stage 15 chicken embryo, there is no staining for Robo2 at vagal levels (bracket) though there is staining at truncal levels. (b and c) At stage 18 during the peak of neural crest migration, Robo1 (b) and Robo2 (c) are strongly expressed in neural crest cells at the trunk levels (black arrows) but not in the vagal region (brackets). (d) Robo2 labeling in the head of a stage 15 embryo shows staining on the dorsal half of the otic vesicle (ov), trigeminal placode, and dorsal neurons in the mesencephalon; the posterior part of the second/hyoid branchial arch is also positive for Robo2 (arrowhead). (e–g) At stage 20, when neural crest cells are condensing to form the dorsal root ganglia (arrows), Robo1 (e) and Robo2 (g) are strongly expressed in trunk, but not vagal (brackets), regions. (f) The same stage embryo labeled with HNK-1 shows neural crest cells migrating and beginning to condense into dorsal root ganglia at both vagal and trunk levels.
Mentions: Trunk, but not vagal, neural crest cells express both Robo1 and Robo2 receptors (Figs. 2 and 3). Whole mount in situ hybridization reveals Robo receptors on neural crest cells as they migrate through the trunk somites (Fig. 2, a–c, e, and g). However, neural crest cells at vagal levels, which can be visualized by their expression of the HNK-1 epitope (Fig. 2 f), lack detectable Robo receptors. Robo1 expression was similar to that of Robo2 but initiated at later stages. By section in situ hybridization, which gives better cellular resolution, we noted that Robo1 (Fig. 3, a and b) and Robo2 (Fig. 3, c and d) were expressed on migrating trunk neural crest cells. In contrast, vagal neural crest cells lacked Robo receptor expression above background (Fig. 3, e–h). Not all HNK-1+ migrating trunk neural crest cells were Robo+ during early stages of migration. With developmental age, the levels of Robos on migrating neural crest cells appeared to increase such that late migrating trunk neural crest cells expressed high levels of both receptors (see Fig. S1, available at http://www.jcb.org/cgi/content/full/jcb.200301041/DC1). In addition to the neural crest, Robo1 is seen in motor neurons. Robo2 appears throughout the neural tube with the exception of the ventral-most region. All Robos are expressed at low levels in the dermomyotome. These observations confirm and extend previous work by others in mouse (Holmes et al., 1998; Yuan et al., 1999) and chick embryos (Li et al., 1999; Holmes and Niswander, 2001; Vargesson et al., 2001).

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