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MEMBRANE TRANSPORTERS, ION CHANNELS, AND PUMPS

Intestinal Ca²⁺ wave dynamics in freely moving C. elegans coordinate execution of a rhythmic motor program

²Departments of Anesthesiology and Pharmacology, Digestive Disease Research Center, Vanderbilt University Medical Center, Nashville, Tennessee; and ³Interdepartmental Graduate Program in Neuroscience, Center for Aging and Developmental Biology and ¹Nephrology Division, Department of Medicine, University of Rochester Medical Center, Rochester, New York

Submitted 19 July 2007 ; accepted in final form 13 October 2007

Defecation in the nematode worm Caenorhabditis elegans is a highly rhythmic behavior that is regulated by a Ca²⁺ wave generated in the 20 epithelial cells of the intestine, in part through activation of the inositol 1,4,5-trisphosphate receptor. Execution of the defecation motor program (DMP) can be modified by external cues such as nutrient availability or mechanical stimulation. To address the likelihood that environmental regulation of the DMP requires integrating distinct cellular and organismal processes, we have developed a method for studying coordinate Ca²⁺ oscillations and defecation behavior in intact, freely behaving animals. We tested this technique by examining how mutations in genes known to alter Ca²⁺ handling [including egl-8/phospholipase C (PLC)-β, kqt-3/KCNQ1, sca-1/sarco(endo)plasmic reticulum Ca²⁺ ATPase, and unc-43/Ca²⁺-CaMKII] contribute to shaping the Ca²⁺ wave and asked how Ca²⁺ wave dynamics in the mutant backgrounds altered execution of the DMP. Notably, we find that Ca²⁺ waves in the absence of PLCβ initiate ectopically, often traveling in reverse, and fail to trigger a complete DMP. These results suggest that the normal supremacy of the posterior intestinal cells is not obligatory for Ca²⁺ wave occurrence but instead helps to coordinate the DMP. Furthermore, we present evidence suggesting that an underlying pacemaker appears to oscillate at a faster frequency than the defecation cycle and that arrhythmia may result from uncoupling the pacemaker from the DMP rather than from disrupting the pacemaker itself. We also show that chronic elevations in Ca²⁺ have limited influence on the defecation period but instead alter the interval between successive steps of the DMP. Finally, our results demonstrate that it is possible to assess Ca²⁺ dynamics and muscular contractions in a completely unrestrained model organism.

calcium; oscillation; Caenorhabditis elegans; biosensor

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