Intestinal calcium waves coordinate a behavioral motor program in C. elegans.
Periodic behavioral motor patterns are normally controlled by neural circuits, such as central pattern generators. We here report a novel mechanism of motor pattern generation by non-neural cells. The defecation motor program in Caenorhabditis elegans consists of three stereotyped motor steps with precise timing and this behavior has been studied as a model system of a ultradian biological clock [J.H. Thomas, Genetic analysis of defecation in C. elegans, Genetics 124 (1990) 855-872; D.W. Liu, J.H. Thomas, Regulation of a periodic motor program in C. elegans, J. Neurosci. 14 (1994) 1953-1962; K. Iwasaki, D.W. Liu, J.H. Thomas, Genes that control a temperature-compensated ultradian clock in Caenorhabditis elegans, Proc. Natl. Acad. Sci. USA 92 (1995), 10317-10321]. It was previously implied that the inositol-1,4,5-trisphosphate (IP3) receptor in the intestine was necessary for this periodic behavior [P. Dal Santo, M.A. Logan, A.D. Chisholm, E.M. Jorgensen, The inositol trisphosphate receptor regulates a 50s behavioral rhythm in C. elegans, Cell 98 (1999) 757-767]. Therefore, we developed a new assay system to study a relationship between this behavioral timing and intestinal Ca(2+) dynamics. Using this assay system, we found that the timing between the first and second motor steps is coordinated by intercellular Ca(2+)-wave propagation in the intestine. Lack of the Ca(2+)-wave propagation correlated with no coordination of the motor steps in the CaMKII mutant. Also, when the Ca(2+)-wave propagation was blocked by the IP3 receptor inhibitor heparin at the mid-intestine in wild type, the second/third motor steps were eliminated, which phenocopied ablation of the motor neurons AVL and DVB. These observations suggest that an intestinal Ca(2+)-wave propagation governs the timing of neural activities that controls specific behavioral patterns in C. elegans.
Teramoto
Takayuki
T
Department of Molecular Pharmacology & Biological Chemistry, Institute for Neuroscience, Northwestern University Medical School, 303 E. Chicago Avenue, Searle 5-551, Chicago, IL 60611, USA.
Iwasaki
Kouichi
K
D000818:Animals; D017173:Caenorhabditis elegans / Q000187:drug effects / Q000378:metabolism / Q000502:physiology*; D015220:Calcium Channels; D020013:Calcium Signaling; D003672:Defecation / Q000502:physiology; D006493:Heparin / Q000494:pharmacology; D053496:Inositol 1,4,5-Trisphosphate Receptors; D007413:Intestinal Mucosa / Q000378:metabolism*; D007422:Intestines / Q000502:physiology; D009043:Motor Activity / Q000502:physiology*; D009046:Motor Neurons / Q000502:physiology; D009119:Muscle Contraction; D018160:Receptors, Cytoplasmic and Nuclear / Q000037:antagonists & inhibitors
D015220:Calcium Channels; D053496:Inositol 1,4,5-Trisphosphate Receptors; D018160:Receptors, Cytoplasmic and Nuclear; D006493:Heparin