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

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.

Dispensable, Redundant, Complementary, and Cooperative Roles of Dopamine, Octopamine, and Serotonin inDrosophila melanogaster

“…We also find that feeding OA but not TA or DA rescues the egg retention phenotype in the dVMAT mutant ( Figure S6). These results are consistent with previous reports showing that mutation of the biosynthetic enzyme for OA causes egg retention (Monastirioti 2003) and that OA receptors are likely to mediate passage of eggs through the oviduct as well (Lee et al 2003(Lee et al , 2009Middleton et al 2006;Rodríguez-Valentín et al 2006). Our data further indicate that the vesicular storage and release of OA rather than other signaling mechanisms are important for female fertility and egg laying.…”

“…Previous genetic studies have demonstrated a critical role for OA in female fertility (Monastirioti et al 1996;Neckameyer 1996;Lee et al 2003;Monastirioti 2003;Willard et al 2006;Gruntenko et al 2007;Hardie et al 2007). OA is likely to act at several sites in the female reproductive system to enable egg laying, and activation of different types of OA receptors may mediate contraction of the musculo-epithelial net surrounding the ovary, relaxation of the oviduct, and lubrication of the oviduct via epithelial cells that line the lumen (Lee et al 2003(Lee et al , 2009Middleton et al 2006;Rodríguez-Valentín et al 2006).…”

Drosophila Vesicular Monoamine Transporter Mutants Can Adapt to Reduced or Eliminated Vesicular Stores of Dopamine and Serotonin

“…Fertility: Mutations in either of the biosynthetic enzymes for octopamine, tyramine b-hydroxylase (TbH), and tyrosine decarboxylase (Tdc2), or the octopamine receptor (OAMB) result in egg retention without defects in oocyte development, most likely secondary to altered ovarian and oviduct contractions (Monastirioti et al 1996;Lee et al 2003;Monastirioti 2003;Cole et al 2005;Middleton et al 2006;Rodríguez-Valentín et al 2006). Octopamine may also act as a neurohormone in controlling the metabolism of gonadotropins (juvenile hormone and 20-H ecdysone; Gruntenko et al 2007).…”

Roles of ecdysteroids for progression of reproductive cycle in the fresh water crustacean Daphnia magna

“…In Drosophila, neural signalling with octopamine, which causes oviduct-muscle contraction, controls ovulation [38,39]. In decapod crustaceans, octopamine in the lobster Homarus americanus also stimulates muscle contraction of ovarian walls [3].…”