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Journal of Neuroscience, Vol 2, 381-393, Copyright © 1982 by Society for Neuroscience
Phenotypic expression in the developing murine enteric nervous system
TP Rothman and MD Gershon
The development of the enteric nervous system was examined in fetal mice.
Synthesis of [3H] acetylcholine ([3H]ACh) from [3H]choline and
acetylcholinesterase histochemistry were used as phenotypic markers for
cholinergic neurons, while the radioautographic detection of the specific
uptake of [3H]serotonin (5-[3H]HT) and immunocytochemical staining with
antiserum to 5-HT marked serotonergic neurons. The gut also was examined by
light and electron microscopy. Development of the gut was studied in situ
and in explants grown in organotypic tissue culture. Neurons were first
detected morphologically in the foregut on embryonic day 12 (E12).
Synthesis of [3H]ACh was detectable on days E10 to E12 but increased
markedly between days E13 and E14. Uptake and radioautographic labeling by
5-[3H]HT was seen first in the foregut on day E12, in the colon on day E13,
and in the terminal colon on day E14. Gut explanted from both distal and
proximal bowel prior to the time when neurons could be detected (days E9 to
E11) nevertheless formed neurons in culture. These cultures of early
explants displayed markers for both cholinergic and serotonergic neurons.
Enhances development of both cholinergic and serotonergic neurons was found
in cultures explanted at day E11 over that found in cultures explanted on
days E9 or E10. The evidence presented indicates (1) that enteric neurons
develop from nonrecognizable precursors, (2) that the proximodistal
gradient in neuronal phenotypic expression probably is not related to a
proximodistal migration of precursor cells down the gut, (3) that the
colonization of the bowel by neuronal precursors may be a prolonged process
continuing from day E9 at least through day E11, (4) that the first pool of
neuronal primordia to colonize the developing bowel can produce both
cholinergic and serotonergic neurons. It is proposed that a sequential
interaction of a long retained pool of dividing precursor cells with a
fetal enteric microenvironment that changes as a function of time during
ontogeny may be involved in producing the phenotypic diversity that
characterized the enteric nervous system.
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