Intestinal calcium waves coordinate a behavioral motor program in C. elegans

Takayuki Teramoto, Kouichi Iwasaki

Research output: Contribution to journalArticle

34 Citations (Scopus)

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 languageEnglish
Pages (from-to)319-327
Number of pages9
JournalCell Calcium
Volume40
Issue number3
DOIs
Publication statusPublished - Sep 2006

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Calcium Signaling
Caenorhabditis elegans
Intestines
Inositol 1,4,5-Trisphosphate Receptors
Defecation
Central Pattern Generators
Biological Clocks
Calcium-Calmodulin-Dependent Protein Kinase Type 2
Inositol 1,4,5-Trisphosphate
Motor Neurons
Inositol
Heparin
Temperature
Genes

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 journalArticle

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