Neuromuscular organization and aminergic modulation of contractions in the Drosophila ovary

Middleton, C. A.; Nongthomba, Upendra; Parry, Katherine; Sweeney, Sean T.; Sparrow, John C.; Elliott, Christopher

doi:10.1186/1741-7007-4-17

Cited by 130 publications

(86 citation statements)

References 40 publications

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“…To investigate, live imaging was used to observe contraction of ovaries when cultured in vitro . The wildtype ovary exhibited smooth and constant rhythmic contraction (Movie S1), as described previously (Middleton et al, 2006). However, in htl KD ovaries, in which htl .RNAi40627 or htl .RNAi6692 was induced in somatic cells by c587 .GAL4 at earlier stages, muscle contractions were present but appeared uncoordinated.…”

Section: Resultsmentioning

confidence: 99%

FGF signaling supports Drosophila fertility by regulating development of ovarian muscle tissues

Irizarry

Stathopoulos

2015

Developmental Biology

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The thisbe (ths) gene encodes a Drosophila fibroblast growth factor (FGF), and mutant females are viable but sterile suggesting a link between FGF signaling and fertility. Ovaries exhibit abnormal morphology including lack of epithelial sheaths, muscle tissues that surround ovarioles. Here we investigated how FGF influences Drosophila ovary morphogenesis and identified several roles. Heartless (Htl) FGF receptor was found expressed within somatic cells at the larval and pupal stages, and phenotypes were uncovered using RNAi. Differentiation of terminal filament cells was affected, but this effect did not alter ovariole number. In addition, proliferation of epithelial sheath progenitors, the apical cells, was decreased in both htl and ths mutants, while ectopic expression of the Ths ligand led to these cells’ over-proliferation suggesting that FGF signaling supports ovarian muscle sheath formation by controlling apical cell number in the developing gonad. Additionally, live imaging of adult ovaries was used to show that htl RNAi mutants, hypomorphic mutants in which epithelial sheaths are present, exhibit abnormal muscle contractions. Collectively, our results demonstrate that proper formation of ovarian muscle tissues is regulated by FGF signaling in the larval and pupal stages through control of apical cell proliferation and is required to support fertility.

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Section: Resultsmentioning

confidence: 99%

FGF signaling supports Drosophila fertility by regulating development of ovarian muscle tissues

Irizarry

Stathopoulos

2015

Developmental Biology

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“…OA relaxes the oviduct muscle when applied to the reproductive system [13], however the OA receptor responsible for this action has not been found in the muscle. Thus, it is tempting to speculate that OA activates Octβ2R and OAMB in the epithelium positioned between the visceral muscle and lumen for dual physiological processes, i.e.…”

Section: Discussionmentioning

confidence: 96%

The Octopamine Receptor Octβ2R Regulates Ovulation in Drosophila melanogaster

et al. 2014

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Oviposition is induced upon mating in most insects. Ovulation is a primary step in oviposition, representing an important target to control insect pests and vectors, but limited information is available on the underlying mechanism. Here we report that the beta adrenergic-like octopamine receptor Octβ2R serves as a key signaling molecule for ovulation and recruits protein kinase A and Ca2+/calmodulin-sensitive kinase II as downstream effectors for this activity. We found that the octβ2r homozygous mutant females are sterile. They displayed normal courtship, copulation, sperm storage and post-mating rejection behavior but were unable to lay eggs. We have previously shown that octopamine neurons in the abdominal ganglion innervate the oviduct epithelium. Consistently, restored expression of Octβ2R in oviduct epithelial cells was sufficient to reinstate ovulation and full fecundity in the octβ2r mutant females, demonstrating that the oviduct epithelium is a major site of Octβ2R’s function in oviposition. We also found that overexpression of the protein kinase A catalytic subunit or Ca2+/calmodulin-sensitive protein kinase II led to partial rescue of octβ2r’s sterility. This suggests that Octβ2R activates cAMP as well as additional effectors including Ca2+/calmodulin-sensitive protein kinase II for oviposition. All three known beta adrenergic-like octopamine receptors stimulate cAMP production in vitro. Octβ1R, when ectopically expressed in the octβ2r’s oviduct epithelium, fully reinstated ovulation and fecundity. Ectopically expressed Octβ3R, on the other hand, partly restored ovulation and fecundity while OAMB-K3 and OAMB-AS that increase Ca2+ levels yielded partial rescue of ovulation but not fecundity deficit. These observations suggest that Octβ2R have distinct signaling capacities in vivo and activate multiple signaling pathways to induce egg laying. The findings reported here narrow the knowledge gap and offer insight into novel strategies for insect control.

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“…We hypothesized that each part of the reproductive tract contains a characteristic combination of neuromodulators that confer unique identities on each region and that post-mating changes in these combinations coordinate subsequent actions. We examined the presence, locations and levels of neuromodulators and related molecules (“signaling molecules”) in the reproductive tract of Drosophila melanogaster females before and after mating: the biogenic amine octopamine, which regulates ovulation rate in Drosophila and locusts [7, 14–20]; serotonin, which regulates muscle contraction in locust oviducts [21]; and the FMRF amide dromyosuppressin (DMS), which regulates contraction of Drosophila heart muscle [22] and may regulate muscle contractions in the reproductive tract, if it is expressed there. We find that separate aspects of mating (sperm, seminal proteins, physical effects) independently modulate the release of signaling molecules.…”

Section: Discussionmentioning

confidence: 99%

Mating Regulates Neuromodulator Ensembles at Nerve Termini Innervating the Drosophila Reproductive Tract

et al. 2014

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Neuromuscular organization and aminergic modulation of contractions in the Drosophila ovary

Cited by 130 publications

References 40 publications

FGF signaling supports Drosophila fertility by regulating development of ovarian muscle tissues

FGF signaling supports Drosophila fertility by regulating development of ovarian muscle tissues

The Octopamine Receptor Octβ2R Regulates Ovulation in Drosophila melanogaster

Mating Regulates Neuromodulator Ensembles at Nerve Termini Innervating the Drosophila Reproductive Tract

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