Developmental expression of G proteins in a migratory population of embryonic neurons

A. M. Horgan, M. T. Lagrange, P. F. Copenhaver

Research output: Contribution to journalArticlepeer-review

18 Scopus citations

Abstract

Directed neuronal migration contributes to the formation of many developing systems, but the molecular mechanisms that control the migratory process are still poorly understood. We have examined the role of heterotrimeric G proteins (guanyl nucleotide binding proteins) in regulating the migratory behavior of embryonic neurons in the enteric nervous system of the moth, Manduca sexta. During the formation of the enteric nervous system, a group of approx. 300 enteric neurons (the EP cells) participate in a precise migratory sequence, during which the undifferentiated cells populate a branching nerve plexus that lies superficially on the visceral musculature. Once migration is complete, the cells then acquire a variety of position-specific neuronal phenotypes. Using affinity-purified antisera against different G protein subtypes, we found no apparent staining for any G protein in the EP cells prior to their migration. Coincident with the onset of migration, however, the EP cells commenced the expression of one particular G protein, Go(α). The intensity of immunostaining continued to increase as migration progressed, with Go(α) immunoreactivity being detectable in the leading processes of the neurons as well as their somata. The identity of the Go(α)-related proteins was confirmed by protein immunoblot analysis and by comparison with previously described forms of Go(α) from Drosophila. When cultured embryos were treated briefly with aluminium fluoride, a compound known to stimulate the activity of heterotrimeric G proteins, both EP cell migration and process outgrowth were inhibited. The effects of aluminium fluoride were potentiated by alpha toxin, a pore-forming compound that by itself caused no significant perturbations of migration. In preliminary experiments, intracellular injections of the non-hydrolyzable nucleotide GTPγ-S also inhibited the migration of individual EP cells, supporting the hypothesis that G proteins play a key role in the control of neuronal motility in this system. In addition, once migration was complete, the expression of Go(α)-related proteins in the EP cells underwent a subsequent phase of regulation, so that only certain phenotypic classes among the differentiated EP cells retained detectable levels of Go(α) immunoreactivity. Thus Go may perform multiple functions within the same population of migratory neurons in the course of embryonic development.

Original languageEnglish (US)
Pages (from-to)729-742
Number of pages14
JournalDevelopment
Volume120
Issue number4
StatePublished - Apr 1 1994

Keywords

  • Cell migration
  • Enteric nervous system
  • G protein
  • Invertebrate embryogenesis
  • Manduca sexta
  • Migratory pathway
  • Neuronal motility

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology

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