Oviduct contraction in Drosophila is modulated by a neural network that is both, octopaminergic and glutamatergic

J Cell Physiol. 2006 Oct;209(1):183-98. doi: 10.1002/jcp.20722.

Abstract

Fertility is a highly complex and regulated phenomenon essential for the survival of any species. To identify Drosophila fertility-specific neural networks, we used a GAL4/UAS enhancer trap genetic screen that selectively inactivates groups of neurons. We identified a GAL4 line (bwktqs) that has a female sterile phenotype only when it expresses the tetanus toxin light chain (TeTxLC). These flies lack oviduct contraction, lay almost no eggs, sperm accumulate in the oviducts, and fewer than normal are seen in the storage organs. In insects, two neuroactive substances are important for oviduct contraction: octopamine (OA), a monoamine that inhibits oviduct contraction, and glutamate (Glu), a neurotransmitter that induces contraction. It is known that octopaminergic neurons of the thoracic abdominal ganglion (TAG) modulate oviduct contraction, however, the glutamatergic neurons that innervate the oviduct have not been identified yet and the interaction between these two neuroactive substances is not well understood. Immunostaining experiments revealed that the bwktqs line trapped an octopaminergic neural network that innervates the genital tract. We show that wt like oviduct contraction in TeTxLC-inactivated flies can only be rescued by simultaneous application of Glu and OA suggesting that the abdominal bwktqs neurons are both octopaminergic and glutamatergic, the use of an agonist and an antagonist for Glu receptors as well as their direct visualization confirmed its participation in this phenomenon. Our work provides the first evidence that adult abdominal type II visceral innervations co-express Glu and OA and allows us to re-evaluate the previous model of neuronal network controlling insect oviduct contraction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Drosophila / embryology*
  • Drosophila / genetics
  • Drosophila Proteins / genetics
  • Female
  • Ganglion Cysts
  • Glutamic Acid / pharmacology*
  • In Vitro Techniques
  • Infertility, Female / etiology
  • Models, Anatomic
  • Models, Biological
  • Models, Neurological
  • Muscle Contraction / genetics*
  • Nerve Net / anatomy & histology
  • Nerve Net / physiology*
  • Neurons / metabolism
  • Octopamine / pharmacology*
  • Oviducts / innervation
  • Oviducts / physiology*
  • Synaptic Transmission
  • Transcription Factors / genetics

Substances

  • BWK protein, Drosophila
  • Drosophila Proteins
  • Transcription Factors
  • Octopamine
  • Glutamic Acid