Gap junctions synchronize action potentials and Ca2+ transients in Caenorhabditis elegans body wall muscle.
The sinusoidal locomotion of Caenorhabditis elegans requires synchronous activities of neighboring body wall muscle cells. However, it is unknown whether the synchrony results from muscle electrical coupling or neural inputs. We analyzed the effects of mutating gap junction proteins and blocking neuromuscular transmission on the synchrony of action potentials (APs) and Ca2+ transients among neighboring body wall muscle cells. In wild-type worms, the percentage of synchronous APs between two neighboring cells varied depending on the anatomical relationship and junctional conductance (Gj) between them, and Ca2+ transients were synchronous among neighboring muscle cells. Compared with the wild type, knock-out of the gap junction gene unc-9 resulted in greatly reduced coupling coefficient and asynchronous APs and Ca2+ transients. Inhibition of unc-9 expression specifically in muscle by RNAi also reduced the synchrony of APs and Ca2+ transients, whereas expression of wild-type UNC-9 specifically in muscle rescued the synchrony defect. Loss of the stomatin-like protein UNC-1, which is a regulator of UNC-9-based gap junctions, similarly impaired muscle synchrony as unc-9 mutant did. The blockade of muscle ionotropic acetylcholine receptors by (+)-tubocurarine decreased the frequencies of APs and Ca2+ transients, whereas blockade of muscle GABAA receptors by gabazine had opposite effects. However, both APs and Ca2+ transients remained synchronous after the application of (+)-tubocurarine and/or gabazine. These observations suggest that gap junctions in C. elegans body wall muscle cells are responsible for synchronizing muscle APs and Ca2+ transients.
Department of Neuroscience, University of Connecticut Health Center, Farmington, Connecticut 06030.
Ping
P
Liu
Department of Neuroscience, University of Connecticut Health Center, Farmington, Connecticut 06030.
Bojun
B
Chen
Department of Neuroscience, University of Connecticut Health Center, Farmington, Connecticut 06030. Electronic address: zwwang@uchc.edu.
Zhao-Wen
ZW
Wang
D000200:Action Potentials; D000818:Animals; D017173:Caenorhabditis elegans; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism; D002118:Calcium / Q000378:metabolism*; D020013:Calcium Signaling; D004594:Electrophysiology / Q000379:methods; D017629:Gap Junctions / Q000378:metabolism*; D008954:Models, Biological; D009132:Muscles / Q000378:metabolism; D003473:Neuromuscular Nondepolarizing Agents / Q000494:pharmacology; D011724:Pyridazines / Q000494:pharmacology; D034622:RNA Interference; D009435:Synaptic Transmission; D014403:Tubocurarine / Q000494:pharmacology
D029742:Caenorhabditis elegans Proteins; D003473:Neuromuscular Nondepolarizing Agents; D011724:Pyridazines; C049853:gabazine; D002118:Calcium; D014403:Tubocurarine