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The Journal of Neuroscience, March 1, 2006, 26(9):2369-2379; doi:10.1523/JNEUROSCI.3770-05.2006

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Cellular/Molecular
Rolling Blackout Is Required for Synaptic Vesicle Exocytosis

Fu-De Huang, Elvin Woodruff, Ralf Mohrmann, and Kendal Broadie

Department of Biological Sciences, Vanderbilt Kennedy Center for Research on Human Development, Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee 37235-1634

Correspondence should be addressed to Prof. Kendal S. Broadie, Department of Biological Sciences, Vanderbilt University, VU Station B, Nashville, TN 37235-1634. Email: kendal.broadie{at}vanderbilt.edu

Rolling blackout (RBO) is a putative transmembrane lipase required for phospholipase C-dependent phosphatidylinositol 4,5-bisphosphate–diacylglycerol signaling in Drosophila neurons. Conditional temperature-sensitive (TS) rbo mutants display complete, reversible paralysis within minutes, demonstrating that RBO is acutely required for movement. RBO protein is localized predominantly in presynaptic boutons at neuromuscular junction (NMJ) synapses and throughout central synaptic neuropil, and rbo TS mutants display a complete, reversible block of both central and peripheral synaptic transmission within minutes. This phenotype appears limited to adults, because larval NMJs do not manifest the acute blockade. Electron microscopy of adult rbo TS mutant boutons reveals an increase in total synaptic vesicle (SV) content, with a concomitant shrinkage of presynaptic bouton size and an accumulation of docked SVs at presynaptic active zones within minutes. Genetic tests reveal a synergistic interaction between rbo and syntaxin1A TS mutants, suggesting that RBO is required in the mechanism of N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE)-mediated SV exocytosis, or in a parallel pathway necessary for SV fusion. The rbo TS mutation does not detectably alter SNARE complex assembly, suggesting a downstream requirement in SV fusion. We conclude that RBO plays an essential role in neurotransmitter release, downstream of SV docking, likely mediating SV fusion.

Key words: Drosophila; temperature-sensitive paralysis; giant fiber circuit; neurotransmission; synapse; membrane lipase; syntaxin

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Received Sept. 6, 2005; revised Jan. 12, 2006; accepted Jan. 17, 2006.

Correspondence should be addressed to Prof. Kendal S. Broadie, Department of Biological Sciences, Vanderbilt University, VU Station B, Nashville, TN 37235-1634. Email: kendal.broadie{at}vanderbilt.edu

This article has been cited by other articles:

				N. Vijayakrishnan, E. A. Woodruff III, and K. Broadie Rolling blackout is required for bulk endocytosis in non-neuronal cells and neuronal synapses J. Cell Sci., January 1, 2009; 122(1): 114 - 125. [Abstract] [Full Text] [PDF]

				D. Baird, C. Stefan, A. Audhya, S. Weys, and S. D. Emr Assembly of the PtdIns 4-kinase Stt4 complex at the plasma membrane requires Ypp1 and Efr3 J. Cell Biol., December 15, 2008; 183(6): 1061 - 1074. [Abstract] [Full Text] [PDF]

				A. A. Long, E. Kim, H.-T. Leung, E. Woodruff III, L. An, R. W. Doerge, W. L. Pak, and K. Broadie Presynaptic Calcium Channel Localization and Calcium-Dependent Synaptic Vesicle Exocytosis Regulated by the Fuseless Protein J. Neurosci., April 2, 2008; 28(14): 3668 - 3682. [Abstract] [Full Text] [PDF]

				F. Darios, E. Connell, and B. Davletov Phospholipases and fatty acid signalling in exocytosis J. Physiol., December 15, 2007; 585(3): 699 - 704. [Abstract] [Full Text] [PDF]

				J. Rohrbough, E. Rushton, E. Woodruff III, T. Fergestad, K. Vigneswaran, and K. Broadie Presynaptic establishment of the synaptic cleft extracellular matrix is required for post-synaptic differentiation Genes & Dev., October 15, 2007; 21(20): 2607 - 2628. [Abstract] [Full Text] [PDF]

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