Neuron-glia communication via nitric oxide is essential in establishing antennal-lobe structure in Manduca sexta

Nicholas J. Gibson, Wolfgang Rössler, Alan J. Nighorn, Lynne A. Oland, John G. Hildebrand, Leslie P. Tolbert

Research output: Contribution to journalArticle

40 Scopus citations

Abstract

Nitric oxide synthase recently has been shown to be present in olfactory receptor cells throughout development of the adult antennal (olfactory) lobe of the brain of the moth Manduca sexta. Here, we investigate the possible involvement of nitric oxide (NO) in antennal-lobe morphogenesis. Inhibition of NO signaling with a NO synthase inhibitor or a NO scavenger early in development results in abnormal antennal lobes in which neuropil-associated glia fail to migrate. A more subtle effect is seen in the arborization of dendrites of a serotonin-immunoreactive neuron, which grow beyond their normal range. The effects of NO signaling in these types of cells do not appear to be mediated by activation of soluble guanylyl cyclase to produce cGMP, as these cells do not exhibit cGMP immunoreactivity following NO stimulation and are not affected by infusion of a soluble guanylyl cyclase inhibitor. Treatment with Novobiocin, which blocks ADP-ribosylation of proteins, results in a phenotype similar to those seen with blockade of NO signaling. Thus, axons of olfactory receptor cells appear to trigger glial cell migration and limit arborization of serotonin-immunoreactive neurons via NO signaling. The NO effect may be mediated in part by ADP-ribosylation of target cell proteins.

Original languageEnglish (US)
Pages (from-to)326-339
Number of pages14
JournalDevelopmental biology
Volume240
Issue number2
DOIs
StatePublished - Dec 15 2001

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Keywords

  • Development
  • Glia
  • Glomerulus.
  • Manduca sexta
  • Nitric oxide
  • Olfaction
  • Olfactory receptor

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology
  • Cell Biology

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