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The Journal of Neuroscience, July 20, 2005, 25(29):6745-6754; doi:10.1523/JNEUROSCI.1730-05.2005

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Cellular/Molecular
Presynaptic Ryanodine Receptors Are Required for Normal Quantal Size at the Caenorhabditis elegans Neuromuscular Junction

Qiang Liu,¹ Bojun Chen,^1 * Maya Yankova,^2 * D. Kent Morest,¹ Ed Maryon,³ Arthur R. Hand,² Michael L. Nonet,⁴ and Zhao-Wen Wang¹

¹Department of Neuroscience and ²Central Electron Microscope Facility, University of Connecticut Health Center, Farmington, Connecticut 06030-3401, ³Department of Biology, University of Illinois, Chicago, Illinois 60607, and ⁴Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110

Analyses of the effect of ryanodine in vertebrate brain slices have led to the conclusion that presynaptic ryanodine receptors (RYRs) may have several functions in synaptic release, including causing large-amplitude miniature postsynaptic currents (mPSCs) by promoting concerted multivesicular release. However, the role of RYRs in synaptic release is controversial. To better understand the role of RYRs in synaptic release, we analyzed the effect of RYR mutation on mPSCs and evoked postsynaptic currents (ePSCs) at the Caenorhabditis elegans neuromuscular junction (NMJ). Amplitudes of mPSCs varied greatly at the C. elegans NMJ. Loss-of-function mutations of the RYR gene unc-68 (uncoordinated 68) essentially abolished large-amplitude mPSCs. The amplitude of ePSCs was also greatly suppressed. These defects were completely rescued by expressing wild-type UNC-68 specifically in neurons but not in muscle cells, suggesting that RYRs acted presynaptically. A combination of removing extracellular Ca²⁺ and UNC-68 function eliminated mPSCs, suggesting that influx and RYR-mediated release are likely the exclusive sources of Ca²⁺ for synaptic release. Large-amplitude mPSCs did not appear to be caused by multivesicular release, as has been suggested to occur at vertebrate central synapses, because the rise time of mPSCs was constant regardless of the amplitude but distinctive from that of ePSCs, and because large-amplitude mPSCs persisted under conditions that inhibit synchronized synaptic release, including elimination of extracellular Ca²⁺, and mutations of syntaxin and SNAP25 (soluble N-ethylmaleimide-sensitive factor attachment protein 25). These observations suggest that RYRs are essential to normal quantal size and are potential regulators of quantal size.

Key words: ryanodine receptor; quantal size; C. elegans; neuromuscular junction; calcium; presynaptic

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Received May 1, 2005; revised May 31, 2005; accepted May 31, 2005.

This article has been cited by other articles:

				H. Shimizu, M. Fukaya, M. Yamasaki, M. Watanabe, T. Manabe, and H. Kamiya Use-dependent amplification of presynaptic Ca2+ signaling by axonal ryanodine receptors at the hippocampal mossy fiber synapse PNAS, August 19, 2008; 105(33): 11998 - 12003. [Abstract] [Full Text] [PDF]

				Q. Liu, B. Chen, Q. Ge, and Z.-W. Wang Presynaptic Ca2+/Calmodulin-Dependent Protein Kinase II Modulates Neurotransmitter Release by Activating BK Channels at Caenorhabditis elegans Neuromuscular Junction J. Neurosci., September 26, 2007; 27(39): 10404 - 10413. [Abstract] [Full Text] [PDF]

				Q. Liu, B. Chen, E. Gaier, J. Joshi, and Z.-W. Wang Low Conductance Gap Junctions Mediate Specific Electrical Coupling in Body-wall Muscle Cells of Caenorhabditis elegans J. Biol. Chem., March 24, 2006; 281(12): 7881 - 7889. [Abstract] [Full Text] [PDF]

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