The migratory behavior of immature enteric neurons

Hao, Marlene M; Anderson, Richard B.; Kobayashi, Kazuto; Whitington, Paul M.; Young, Heather M.

doi:10.1002/dneu.20683

Cited by 49 publications

(34 citation statements)

References 66 publications

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“…Most neuron-like ENCCs in the E11.5 and E12.5 gut project caudally [37,38]. Four of the movies of the E12.5 colon contained photoconverted ENCCs undergoing neuritogenesis.…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2014

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BackgroundDirected 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.ResultsThe 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.ConclusionsEach 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.

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“…Most neuron-like ENCCs in the E11.5 and E12.5 gut project caudally [37,38]. Four of the movies of the E12.5 colon contained photoconverted ENCCs undergoing neuritogenesis.…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2014

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“…This has led to the suggestion that enteric neural crest-derived cell migration is retarded by neuronal differentiation Wu et al, 1999). It has recently been shown that around 50% of immature enteric neurons continue to migrate within the developing gut, although the speed at which they migrate is considerably slower than that of enteric neural crest-derived cells (Hao et al, 2008). We have previously shown that the migration of enteric neural crest-derived cell migration is significantly delayed in E11.5 L1 Ϫ/y embryos compared with littermate controls (Anderson et al, 2006b).…”

Section: Cgrpmentioning

confidence: 86%

Cell adhesion molecule L1 affects the rate of differentiation of enteric neurons in the developing gut

Turner

Schachner

Anderson

2009

Developmental Dynamics

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The enteric nervous system arises predominantly from vagal level neural crest cells that migrate into and along the developing gut. As the neural crest-derived cells migrate within the gut, a subpopulation begins to differentiate into enteric neurons. Here, we show that the differentiation of neural crest-derived cells into enteric neurons is delayed in L1-deficient mice, compared with littermate controls. However, glial cell differentiation is not affected in L1-deficient mice. These mice also show a delay in the differentiation of a neurotransmitter-specific subtype of enteric neuron within the gastrointestinal tract. Together, these results suggest a role for the cell adhesion molecule, L1, in the differentiation of neural crestderived cells into enteric neurons within the developing enteric nervous system. Developmental Dynamics 238:708 -715, 2009.

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“…To identify cells expressing pan-neuronal markers in E11.5 cultures, cells from TH-GFP mice were used, as the subpopulation of ENCCs that expresses pan-neuronal markers transiently express TH at this age (Sawamoto et al, 2001;Hao et al, 2009). By E12.5, TH is downregulated in cells expressing pan-neuronal markers.…”

Section: Electrophysiological Properties Of Embryonic Early Postnatamentioning

confidence: 99%

Early Development of Electrical Excitability in the Mouse Enteric Nervous System

Hao

Lomax

McKeown³

et al. 2012

J. Neurosci.

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Neural activity is integral to the development of the enteric nervous system (ENS). A subpopulation of neural crest-derived cells expresses pan-neuronal markers at early stages of ENS development (at E10.5 in the mouse). However, the electrical activity of these cells has not been previously characterized, and it is not known whether all cells expressing neuronal markers are capable of firing action potentials (APs). In this study, we examined the activity of "neuron"-like cells (expressing pan-neuronal markers or with neuronal morphology) in the gut of E11.5 and E12.5 mice using whole-cell patch-clamp electrophysiology and compared them to the activity of neonatal and adult enteric neurons. Around 30 -40% of neuron-like cells at E11.5 and E12.5 fired APs, some of which were very similar to those of adult enteric neurons. All APs were sensitive to tetrodotoxin (TTX), indicating that they were driven by voltage-gated Na ϩ currents. Expression of mRNA encoding several voltage-gated Na ϩ channels by the E11.5 gut was detected using RT-PCR. The density of voltage-gated Na ϩ currents increased from E11.5 to neonates. Immature active responses, mediated in part by TTX-and lidocaine-insensitive channels, were observed in most cells at E11.5 and E12.5, but not in P0/P1 or adult neurons. However, some cells expressing neuronal markers at E11.5 or E12.5 did not exhibit an active response to depolarization. Spontaneous depolarizations resembling excitatory postsynaptic potentials were observed at E12.5. The ENS is one of the earliest parts of the developing nervous system to exhibit mature forms of electrical activity.

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The migratory behavior of immature enteric neurons

Cited by 49 publications

References 66 publications

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

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

Cell adhesion molecule L1 affects the rate of differentiation of enteric neurons in the developing gut

Early Development of Electrical Excitability in the Mouse Enteric Nervous System

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