Abstract
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.
| Original language | English |
|---|---|
| Pages (from-to) | 319-327 |
| Number of pages | 9 |
| Journal | Cell Calcium |
| Volume | 40 |
| Issue number | 3 |
| DOIs | |
| Publication status | Published - Sep 2006 |
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All Science Journal Classification (ASJC) codes
- Physiology
- Molecular Biology
- Cell Biology
Cite this
Intestinal calcium waves coordinate a behavioral motor program in C. elegans. / Teramoto, Takayuki; Iwasaki, Kouichi.
In: Cell Calcium, Vol. 40, No. 3, 09.2006, p. 319-327.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Intestinal calcium waves coordinate a behavioral motor program in C. elegans
AU - Teramoto, Takayuki
AU - Iwasaki, Kouichi
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.
UR - http://www.scopus.com/inward/record.url?scp=33745970486&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=33745970486&partnerID=8YFLogxK
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 -