Neurofilament expression in vagal neural crest-derived precursors of enteric neurons

doi:10.1016/0012-1606(84)90285-9

Developmental Biology

Volume 105, Issue 2, October 1984, Pages 273-287

https://doi.org/10.1016/0012-1606(84)90285-9 Get rights and content

Abstract

In order to gain insight into the potential role of the enteric microenvironment in the neuronal determination of the neural crest-derived precursor cells of enteric neurons, an attempt was made to ascertain when and where along the migratory route of these cells that they first express neuronal properties. The immunocytochemical detection of the 160-kDa component of the triplet of the chick neurofilament peptides served as a neuronal marker. In addition, neurogenic potential was assessed by growing explants of tissue suspected of containing presumptive neuroblasts in culture or as grafts on the chorioallantoic membrane of chick embryonic hosts. Neurofilament immunoreactivity was first detected in the foregut by Day 4 of development and spread to the hindgut by Day 7. Within the hindgut, development was more advanced within the colorectum than within the more proximal terminal ileum and caecal appendages. This probably reflects the distal-proximal migration of sacral neural crest cells in the postumbilical bowel. The ability of enteric explants to show neuronal development in vitro correlated with whether or not cells containing neurofilament immunoreactivity had reached that segment of gut at the age of explantation. These data suggest that enteric neuronal precursors have already begun to differentiate as neurons by the time they colonize the gut. Prior to the appearance of fibrillar neurofilament immunoreactivity in the foregut, cells that express this marker were found transiently within the mesenchyme of branchial arches 3, 4, and 5. These cells had disappeared from this region by developmental Day 6. The neurogenic potential of branchial arches 3 and 4 was demonstrated by the correlation that was found between the ability of explants of these arches to show neuronal development in vitro and the presence within them of cells that display neurofilament immunoreactivity. No similar neurogenic potential was found in the more rostral branchial arches which lacked the masses of neurofilament-immunoreactive cells. The location of the caudal branchial arches below the migrating vagal neural crest, the transience of the neurofilament immunoreactivity in them, and the coincident transience of their neurogenic potential in vitro, suggested that the masses of neurofilament immunoreactive cells in the caudal branchial arches might be vagal neural crest-derived neuronal precursor cells en route to the pharynx and the rest of the gut. This possibility was supported by the observation of neurofilament immunoreactivity in a subset of cells of the premigratory and early migratory neural crest in the vagal, but not other, regions of the neuraxis prior to the appearance of neurofilament immunoreactivity in the branchial arches. Proliferative expansion of cells with neurofilament immunoreactivity was indicated by the observation of mitotic figures in them. It is suggested that the vagal neural crest cells that populate the ENS are already committed to the neuronal lineage while still in the vagal region of the neuraxis. It is therefore not likely that the enteric microenvironment plays a role in this process.

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^☆: This research was supported by Grants BNS-83-09156 from the National Science Foundation, NS15547 from the National Institutes of Health, The Jurzykowski Foundation, and by a fellowship to R.F.P. from the John A. Hartford Foundation.

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Full paperNeurofilament expression in vagal neural crest-derived precursors of enteric neurons☆

Abstract

Brain Res

Dev. Biol

Dev. Biol

Brain Res

Dev. Biol

Neuroscience

Dev. Biol

Dev. Biol

Dev. Biol

Dev. Biol

Dev. Biol

Cell Differ

Dev. Biol

Brain Res

Dev. Brain Res

The origin and differentiation of enteric neurons of the intestine of the fowl embryo

Amer. J. Anat

Different proteins associated with 10 nm filaments in cultured chick neurons and non-neuronal cells

Science

Patterns of neurofilament protein expression in replicating neuroepithelial cells of the embryonic chick spinal cord and brain

J. Cell Biol

Use of formaldehyde solutions at variable pH for the localization of tyrosine hydroxylase

J. Histochem. Cytochem

Nature and nurture in development of the autonomic neuron

Science

Enteric neurogenesis by neural crest-derived branchial arch mesenchymal cells

Nature (London)

The ultrastructure of Auerbach's plexus in the guinea pig. I. Neuronal elements

J. Neurocytol

The ultrastructure of Auerbach's plexus in the guinea pig. II. Non-neuronal elements

J. Neurocytol

Glial fibrillary acidic protein in Schwann cells: Fact or artifact

J. Histochem. Cytochem

Contributions of placodal and neural crest cells to avian cranial peripheral ganglia

Amer. J. Anat

Histochemical methods for separate, consecutive and simultaneous demonstration of acetylcholinesterase and norepinephrine in cryostat sections

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Full paper
Neurofilament expression in vagal neural crest-derived precursors of enteric neurons☆