TY - JOUR
T1 - Intestinal calcium waves coordinate a behavioral motor program in C. elegans
AU - Teramoto, Takayuki
AU - Iwasaki, Kouichi
N1 - Funding Information:
We thank K. Bray, R. Toyonaga, and K. Nagasaka for technical assistance, A. Miyawaki, K. Kimura, and H. Suzuki for cameleon constructs, M. Doriscoll for mec-4(d) vectors, E. Jorgensen and M. Peters for collaboration of the innexin project, A. Fire for GFP vectors, T. Nagai and M. Doi for discussion, M. Prakriya, E. Mugnaini, K. Nishiwaki for comments on this manuscript, K. Matsumoto, Y. Kohara, Y. Iino, and K. Nishiwaki for enthusiastic supports. This work was supported by funds from Northwestern University to KI. KI is a Kyakuin Kenkyuin Scientist of AIST. Some strains were obtained from the Caenorhabditis Genetics Center, which is funded by the National Institutes of Health, National Center for Research Resources of the US.
PY - 2006/9
Y1 - 2006/9
N2 - 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 50 s 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 Ca2+ dynamics. Using this assay system, we found that the timing between the first and second motor steps is coordinated by intercellular Ca2+-wave propagation in the intestine. Lack of the Ca2+-wave propagation correlated with no coordination of the motor steps in the CaMKII mutant. Also, when the Ca2+-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 Ca2+-wave propagation governs the timing of neural activities that controls specific behavioral patterns in C. elegans.
AB - 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 50 s 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 Ca2+ dynamics. Using this assay system, we found that the timing between the first and second motor steps is coordinated by intercellular Ca2+-wave propagation in the intestine. Lack of the Ca2+-wave propagation correlated with no coordination of the motor steps in the CaMKII mutant. Also, when the Ca2+-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 Ca2+-wave propagation governs the timing of neural activities that controls specific behavioral patterns in C. elegans.
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U2 - 10.1016/j.ceca.2006.04.009
DO - 10.1016/j.ceca.2006.04.009
M3 - Article
C2 - 16780946
AN - SCOPUS:33745970486
VL - 40
SP - 319
EP - 327
JO - Cell Calcium
JF - Cell Calcium
SN - 0143-4160
IS - 3
ER -