Rolling Blackout is required for both phototransduction and synaptic transmission in Drosophila

Abstract

The temperature-sensitive (TS) paralyzed and blind Drosophila mutant rolling blackout (rbo) identifies a gene encoding a protein that pioneers a novel family of membrane-associated putative lipolytic enzymes highly conserved from yeast to human. RBO protein is enriched in synapse-dense neuropil and predominantly localized in presynaptic boutons at neuromuscular junction synapses, but undetectable in central neuronal cell bodies. The protein is also abundant throughout sensory neurons, including retinal photoreceptors. RBO protein is acutely required for both phototransduction and synaptic transmission. rbo TS mutants show a reversible loss of phototransduction in an activity-dependent manner, in correlation with an activity-dependent depletion of diacylglycerol and concomitant accumulation of phosphatidylinositol phosphate (PIP) and phosphatidylinositol 4,5 bisphosphate (PIP2) within minutes at non-permissive temperature. These results suggest a rapid down-regulation of phospholipase C (PLC) activity. rbo TS mutants also show reversible TS paralysis and complete block of both central and peripheral synaptic transmission within minutes at non-permissive temperature. This loss of synaptic transmission, at least partially, is due to a block of synaptic vesicle (SV) exocytosis downstream of SV docking. The conclusion is that RBO putative lipase may regulate the PLC-PIP2 signaling in both phototransduction and synaptic transmission.