The timing of initial neuropeptide expression by an identified insect neuron does not depend on interactions with its normal peripheral target

John B. Wall, Paul H. Taghert

Research output: Contribution to journalArticle

16 Scopus citations

Abstract

To study the developmental regulation of a neuropeptide phenotype, we have analyzed the biochemical and morphological differentiation of two identifiable neurons in embryos of the moth, Manduca sexta. The central cell, CF, and the peripheral cell, L1, are both neuroendocrine neurons that express neuropeptides related to the molluscan tetrapeptide FMRFamide. Both neurons project axons to the transvers nerve in each thoracic segment. Within the CF and L1 cells, neuropeptide‐like immunoreactivity was localized to secretory granules that had cell specific morphologies and sizes. The onset of neuropeptide expression in the two cell types displayed a similar pattern: immunoreactivity was first detected in distal processes and soon after within cells bodies. However, the onsets occurred at different times: for the CF cell, neuropeptides were first seen at 60%‐63% of embryonic development, after the neuron had extended a long axon into the periphery, while L1 neuropeptide expression began at ∼42%, as it first extended its growth cone. These times were related in that they corresponded to the arrival times of the respective growth cones at a similar position in the developing peripheral nerve. Withinthis region of the nerve, the growth cones of both cell typesexhibited a transient and cell‐specific interaction with an identified mesodermal cell, called the Syncytium. Like the L1 and B neurons (Carr and Taghert, 1988b), the CF growth cones typically grew past this cell, yet remained attached to it by lamellipodial and filopodial processes of the axon. Ultrastructurally, the interaction involved filopodial adhesion to and insertion within the Syncytial cell. Two other nonneuroendocrine cell types grew axons past this same region, but showed no such tendencies. To test the hypothesis that the morphological and biochemical differentiation of these cells was somehow linked, central ganglia were isolated (as individuals or connected as ganglionic chains) in tissue culture, prior to the time when CF growth cones entered the periphery and prior to the development of CF neuropeptide expression. In the majority of cases, CF neurons nevertheless displayed their neuropeptide phenotype at a normal and cell‐specific stage. We conclude that the initiation of neuropeptide expression is highly correlated with schedules of morphological differentiation in these neurons, but that, in the case of the CF neuron, it is not regulated by interactions of the growth cone with peripheral structures.

Original languageEnglish
Pages (from-to)935-956
Number of pages22
JournalJournal of Neurobiology
Volume22
Issue number9
DOIs
StatePublished - Dec 1991

Keywords

  • FMRFamide
  • Manduca
  • cell differentiation
  • growth cones
  • insect embryo
  • neuroendocrine neurons
  • neuropeptide

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