Inositol 1,4,5-Trisphosphate Receptor and dSTIM Function in Drosophila Insulin-Producing Neurons Regulates Systemic Intracellular Calcium Homeostasis and Flight

• Published in: The Journal of neuroscience 2010-01, Vol.30 (4), p.1301-1313
• Main Authors: Agrawal, Neha, Venkiteswaran, Gayatri, Sadaf, Sufia, Padmanabhan, Nisha, Banerjee, Santanu, Hasan, Gaiti
• Format: Article
• Language: English
• Subjects: Animals; Calcium - metabolism; Calcium Signaling - physiology; Cell Membrane - genetics; Cell Membrane - metabolism; Cells, Cultured; Central Nervous System - cytology; Central Nervous System - growth & development; Central Nervous System - metabolism; Drosophila; Drosophila Proteins - genetics; Drosophila Proteins - metabolism; Flight, Animal - physiology; Homeostasis - physiology; Inositol 1,4,5-Trisphosphate Receptors - genetics; Inositol 1,4,5-Trisphosphate Receptors - metabolism; Insulin - metabolism; Insulin Secretion; Intracellular Fluid - metabolism; Membrane Proteins - genetics; Membrane Proteins - metabolism; Mutation - genetics; Neural Pathways - cytology; Neural Pathways - growth & development; Neural Pathways - metabolism; Neurons - cytology; Neurons - metabolism; Pupa - genetics; Pupa - growth & development; Pupa - metabolism; Stromal Interaction Molecule 1
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.3668-09.2010

Calcium (Ca(2+)) signaling is known to regulate the development, maintenance and modulation of activity in neuronal circuits that underlie organismal behavior. In Drosophila, intracellular Ca(2+) signaling by the inositol 1,4,5-trisphosphate receptor and the store-operated channel (dOrai) regulates the formation and function of neuronal circuits that control flight. Here, we show that restoring InsP(3)R activity in insulin-producing neurons of flightless InsP(3)R mutants (itpr) during pupal development can rescue systemic flight ability. Expression of the store operated Ca(2+) entry (SOCE) regulator dSTIM in insulin-producing neurons also suppresses compromised flight ability of InsP(3)R mutants suggesting that SOCE can compensate for impaired InsP(3)R function. Despite restricted expression of wild-type InsP(3)R and dSTIM in insulin-producing neurons, a global restoration of SOCE and store Ca(2+) is observed in primary neuronal cultures from the itpr mutant. These results suggest that restoring InsP(3)R-mediated Ca(2+) release and SOCE in a limited subset of neuromodulatory cells can influence systemic behaviors such as flight by regulating intracellular Ca(2+) homeostasis in a large population of neurons through a non-cell-autonomous mechanism.