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Open Access Research article

Colonizing while migrating: how do individual enteric neural crest cells behave?

Heather M Young1*, Annette J Bergner1, Matthew J Simpson2, Sonja J McKeown1, Marlene M Hao1, Colin R Anderson1 and Hideki Enomoto34

Author Affiliations

1 Department of Anatomy & Neuroscience, University of Melbourne, Melbourne 3010 VIC, Australia

2 School of Mathematical Sciences, Queensland University of Technology, GPO Box 2434, Brisbane 4001 QLD, Australia

3 RIKEN Center for Developmental Biology, Laboratory for Neuronal Differentiation and Regeneration, Kobe, Japan

4 Division of Neural Differentiation and Regeneration, Department of Physiology and Cell Biology, Graduate School of Medicine, Kobe University, Kobe 650-0017, Japan

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BMC Biology 2014, 12:23  doi:10.1186/1741-7007-12-23

Published: 26 March 2014

Abstract

Background

Directed cell migration is essential for normal development. In most of the migratory cell populations that have been analyzed in detail to date, all of the cells migrate as a collective from one location to another. However, there are also migratory cell populations that must populate the areas through which they migrate, and thus some cells get left behind while others advance. Very little is known about how individual cells behave to achieve concomitant directional migration and population of the migratory route. We examined the behavior of enteric neural crest-derived cells (ENCCs), which must both advance caudally to reach the anal end and populate each gut region.

Results

The behavior of individual ENCCs was examined using live imaging and mice in which ENCCs express a photoconvertible protein. We show that individual ENCCs exhibit very variable directionalities and speed; as the migratory wavefront of ENCCs advances caudally, each gut region is populated primarily by some ENCCs migrating non-directionally. After populating each region, ENCCs remain migratory for at least 24 hours. Endothelin receptor type B (EDNRB) signaling is known to be essential for the normal advance of the ENCC population. We now show that perturbation of EDNRB principally affects individual ENCC speed rather than directionality. The trajectories of solitary ENCCs, which occur transiently at the wavefront, were consistent with an unbiased random walk and so cell-cell contact is essential for directional migration. ENCCs migrate in close association with neurites. We showed that although ENCCs often use neurites as substrates, ENCCs lead the way, neurites are not required for chain formation and neurite growth is more directional than the migration of ENCCs as a whole.

Conclusions

Each gut region is initially populated by sub-populations of ENCCs migrating non-directionally, rather than stopping. This might provide a mechanism for ensuring a uniform density of ENCCs along the growing gut.

Keywords:
Collective cell migration; Neural crest; Directional migration; Enteric nervous system