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Published January 1996 | Published
Journal Article Open

Distinct subpopulations of enteric neuronal progenitors defined by time of development, sympathoadrenal lineage markers and Mash-1-dependence

Abstract

Enteric and sympathetic neurons have previously been proposed to be lineally related. We present independent lines of evidence that suggest that enteric neurons arise from at least two lineages, only one of which expresses markers in common with sympathoadrenal cells. In the rat, sympathoadrenal markers are expressed, in the same order as in sympathetic neurons, by a subset of enteric neuronal precursors, which also transiently express tyrosine hydroxylase. If this precursor pool is eliminated in vitro by complement-mediated lysis, enteric neurons continue to develop; however, none of these are serotonergic. In the mouse, the Mash-1−/− mutation, which eliminates sympathetic neurons, also prevents the development of enteric serotonergic neurons. Other enteric neuronal populations, however, including those that contain calcitonin gene related peptide are present. Enteric tyrosine hydroxylase-containing cells co-express Mash-1 and are eliminated by the Mash-1−/− mutation, consistent with the idea that in the mouse, as in the rat, these precursors generate serotonergic neurons. Serotonergic neurons are generated early in development, while calcitonin gene related peptide-containing enteric neurons are generated much later. These data suggest that enteric neurons are derived from at least two progenitor lineages. One transiently expresses sympathoadrenal markers, is Mash-1-dependent, and generates early-born enteric neurons, some of which are serotonergic. The other is Mash-1-independent, does not express sympathoadrenal markers, and generates late-born enteric neurons, some of which contain calcitonin gene related peptide.

Additional Information

© 1996 The Company of Biologists Limited. Accepted 20 September 1995. The authors acknowledge the technical assistance of Ms Mary Schoenebeck and the help provided by Dr Paul Wade in carrying out computer-assisted densitometry (Rothman et al., 1993). We thank Dr Jane Johnson for communicating the sequence of primers for PCR genotyping. The research was supported by NIH grants NS15547, HD17736 and NS23476 to D. J. A. E. Blaugrund was a fellow of the Pharmaceutical Manufacturers Association Foundation. L. Sommer is supported by the Swiss Foundation for Medical and Biological Scholarships. D. J. A. is an Associate Investigator of the Howard Hughes Medical Institute.

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August 22, 2023
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