An identified set of visceral muscle bands is essential for the guidance of migratory neurons in the enteric nervous system of Manduca serta

P. F. Copenhaver, A. M. Morgan, S. Combes

Research output: Contribution to journalArticle

21 Scopus citations

Abstract

During the formation of the enteric nervous system (ENS) in Manduca, a population of ~300 enteric neurons (the EP cells) become distributed along the foregut and midgut by migrating onto specific sets of visceral muscle bands. Only after their migration is complete do the neurons express a variety of position-specific phenotypes, including a peptidergic phenotype that is usually restricted to a subset of EP cells on the midgut. To investigate whether direct interactions between the EP cells and these pathways are necessary for either neuronal migration or differentiation, we have investigated the developmental origins and functional role of the muscle bands in embryonic culture. Using scanning electron microscopy, immunohistochemistry, and mitotic labeling with bromodeoxyuridine, we found that the eight major muscle bands of the midgut form by the coalescence of longitudinal muscle fibers on the midgut surface, apparently in response to regional cues associated with the underlying epithelium. These bands then serve as migratory pathways for the EP cells, which travel rapidly along the bands (but not onto adjacent interband musculature) and then complete their differentiation. Dye labeling of individual EP cells revealed that prior to migration onset, each neuron extended widely distributed filopodia onto both the band and interband regions of the midgut surface. As the muscle bands coalesced, however, the leading process of each EP cell became increasingly confined to a specific band, onto which it subsequently migrated. In a series of surgical manipulations of both the muscle bands and the migratory neurons, we demonstrated that these pathways are both necessary and sufficient to support the migratory behavior of the EP cells. Surgical interventions that prevented the neurons from contacting the muscle bands inhibited migration, while contact between isolated EP cells and a muscle band supported both their migration and differentiation. However, the acquisition of mature phenotypes by the EP cells was not strictly dependent on the migration of these neurons to their expected positions. In particular, the onset of neuropeptide expression could be detected in at least some of the neurons whose migration onto the midgut had been blocked. Thus, in the embryonic ENS, the migration and delayed differentiation of the EP cells represent precisely coordinated aspects of development that are nevertheless regulated in an independent manner.

Original languageEnglish (US)
Pages (from-to)412-426
Number of pages15
JournalDevelopmental Biology
Volume179
Issue number2
DOIs
StatePublished - Nov 1 1996

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology
  • Cell Biology

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