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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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Slit2 enhances neural crest cell migration. Trunk neural crest cells exposed to Slit2 migrate for longer distances compared with control exposed neural crest cells. Trunk and vagal neural tubes were cultured overnight on fibronectin. After one day, media was changed to one conditioned by control or Slit2-secreting cells 1 h before video microscopy in a confocal microscope for 3 h. (a) The total path length was determined and normalized to a 2.5-h time period and binned in groups of 100-μm distances traveled. (b) Total path length (total distance traveled, including the various turns made by the cells) of neural crest cells was plotted as cumulative percentages of the distance traveled. (c) Net path length (net distance from starting point) of neural crest cells was plotted as cumulative percentages of the distance traveled.
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fig9: Slit2 enhances neural crest cell migration. Trunk neural crest cells exposed to Slit2 migrate for longer distances compared with control exposed neural crest cells. Trunk and vagal neural tubes were cultured overnight on fibronectin. After one day, media was changed to one conditioned by control or Slit2-secreting cells 1 h before video microscopy in a confocal microscope for 3 h. (a) The total path length was determined and normalized to a 2.5-h time period and binned in groups of 100-μm distances traveled. (b) Total path length (total distance traveled, including the various turns made by the cells) of neural crest cells was plotted as cumulative percentages of the distance traveled. (c) Net path length (net distance from starting point) of neural crest cells was plotted as cumulative percentages of the distance traveled.

Mentions: Fig. 9 a, which illustrates by groups the total path length of all cells normalized to a total of 2.5 h, shows that the Slit2-exposed neural crest cells tend to move further than control-treated cells, with twice as many within the range of 100–200 μm from the neural tube (n = 74 experimental and 65 control cells analyzed from five separate experiments). We also noted a significant difference in both the total distance traveled (i.e., including the various turns made by the cells) and the net distance away from the neural tube of neural crest cells exposed to soluble Slit2 compared with control CM (Fig. 9, b and c). Accordingly, the net path length was 36% longer in the Slit2-exposed cells compared with control-treated length (38 ± 3 μm in Slit2 compared with 28 ± 3 μm in control medium, P < 0.02, Mann-Whitney test), as was the total path length (139 ± 15 μm for control and 167 ± 14 μm for Slit2, P < 0.005, Mann-Whitney test; Fig. 9 b). We analyzed the speed of movement in groups of cells assayed for similar lengths of time and found an average increase in speed of 52% in Slit2-containing medium relative to the control (P < 0.009, t test). Interestingly, the persistence and directionality were not significantly different between control and Slit2 exposed. Thus, the cells change directions with the same frequency but move further in the same time in the presence of Slit2.


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)

Slit2 enhances neural crest cell migration. Trunk neural crest cells exposed to Slit2 migrate for longer distances compared with control exposed neural crest cells. Trunk and vagal neural tubes were cultured overnight on fibronectin. After one day, media was changed to one conditioned by control or Slit2-secreting cells 1 h before video microscopy in a confocal microscope for 3 h. (a) The total path length was determined and normalized to a 2.5-h time period and binned in groups of 100-μm distances traveled. (b) Total path length (total distance traveled, including the various turns made by the cells) of neural crest cells was plotted as cumulative percentages of the distance traveled. (c) Net path length (net distance from starting point) of neural crest cells was plotted as cumulative percentages of the distance traveled.
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fig9: Slit2 enhances neural crest cell migration. Trunk neural crest cells exposed to Slit2 migrate for longer distances compared with control exposed neural crest cells. Trunk and vagal neural tubes were cultured overnight on fibronectin. After one day, media was changed to one conditioned by control or Slit2-secreting cells 1 h before video microscopy in a confocal microscope for 3 h. (a) The total path length was determined and normalized to a 2.5-h time period and binned in groups of 100-μm distances traveled. (b) Total path length (total distance traveled, including the various turns made by the cells) of neural crest cells was plotted as cumulative percentages of the distance traveled. (c) Net path length (net distance from starting point) of neural crest cells was plotted as cumulative percentages of the distance traveled.
Mentions: Fig. 9 a, which illustrates by groups the total path length of all cells normalized to a total of 2.5 h, shows that the Slit2-exposed neural crest cells tend to move further than control-treated cells, with twice as many within the range of 100–200 μm from the neural tube (n = 74 experimental and 65 control cells analyzed from five separate experiments). We also noted a significant difference in both the total distance traveled (i.e., including the various turns made by the cells) and the net distance away from the neural tube of neural crest cells exposed to soluble Slit2 compared with control CM (Fig. 9, b and c). Accordingly, the net path length was 36% longer in the Slit2-exposed cells compared with control-treated length (38 ± 3 μm in Slit2 compared with 28 ± 3 μm in control medium, P < 0.02, Mann-Whitney test), as was the total path length (139 ± 15 μm for control and 167 ± 14 μm for Slit2, P < 0.005, Mann-Whitney test; Fig. 9 b). We analyzed the speed of movement in groups of cells assayed for similar lengths of time and found an average increase in speed of 52% in Slit2-containing medium relative to the control (P < 0.009, t test). Interestingly, the persistence and directionality were not significantly different between control and Slit2 exposed. Thus, the cells change directions with the same frequency but move further in the same time in the presence of Slit2.

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