The Journal of Neuroscience, July 15, 2002, 22(14):6005-6018
The Projections of Early Enteric Neurons Are Influenced by the
Direction of Neural Crest Cell Migration
H. M.
Young,
B. R.
Jones, and
S. J.
McKeown
Department of Anatomy and Cell Biology, University of Melbourne,
3010, Victoria, Australia
The enteric nervous system arises from the neural crest. In
embryonic mice, vagal neural crest cells enter the developing foregut
at approximately embryonic day 9.5 (E9.5) and then migrate rostrocaudally to colonize the entire gastrointestinal tract by E14.5.
This study showed that a subpopulation of vagal crest-derived cells,
very close to the migratory wavefront, starts to differentiate into
neurons early, as shown by the expression of neuron-specific proteins
and the absence of Sox10. Many of the early differentiating neurons
transiently exhibited tyrosine hydroxylase (TH) immunoreactivity. The
TH cells were demonstrated to be the progenitors of nitric oxide
synthase (NOS) neurons. Immunohistochemistry, lesions, and DiI tracing
were used to examine the projections of developing enteric neurons. The
axons of first neurons in the gut (the TH-NOS neurons) projected in
the same direction (caudally), and traversed the same pathways through
the mesenchyme, as the migrating, undifferentiated, vagal crest-derived
cells. To examine if the direction of migration and direction of axon
projection are linked, coculture experiments were set up in which vagal
crest-derived cells migrated either rostrocaudally (as they do
in vivo), or caudorostrally (which they do not normally
do), to colonize explants of embryonic aneural hindgut. The direction
in which neurons projected was correlated with the direction of cell
migration, but migration direction appears to be not the only mechanism
influencing axon projection. Peristaltic reflexes involve both orally
(rostrally) projecting neurons and anally (caudally) projecting
neurons. Because few rostrally projecting neurons could be detected
before birth, the full circuitry for peristaltic reflexes appears to
develop after birth.
Key words:
enteric nervous system; nitric oxide synthase; Sox10; axon projection; peristalsis; tyrosine hydroxylase
Copyright © 2002 Society for Neuroscience 0270-6474/02/22146005-14$05.00/0
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