Intercellular calcium signaling in a gap junction-coupled cell network establishes asymmetric neuronal fates in C. elegans

Jennifer A. Schumacher, Yi Wen Hsieh, Shiuhwei Chen, Jennifer K. Pirri, Mark J. Alkema, Wen Hong Li, Chieh Chang, Chiou Fen Chuang

Research output: Contribution to journalArticle

28 Scopus citations

Abstract

The C. elegans left and right AWC olfactory neurons specify asymmetric subtypes, one default AWCOFF and one induced AWCON, through a stochastic, coordinated cell signaling event. Intercellular communication between AWCs and non-AWC neurons via a NSY-5 gap junction network coordinates AWC asymmetry. However, the nature of intercellular signaling across the network and how individual non-AWC cells in the network influence AWC asymmetry is not known. Here, we demonstrate that intercellular calcium signaling through the NSY-5 gap junction neural network coordinates a precise 1AWCON/1AWCOFF decision. We show that NSY-5 gap junctions in C. elegans cells mediate small molecule passage. We expressed vertebrate calcium-buffer proteins in groups of cells in the network to reduce intracellular calcium levels, thereby disrupting intercellular communication. We find that calcium in non-AWC cells of the network promotes the AWCON fate, in contrast to the autonomous role of calcium in AWCs to promote the AWCOFF fate. In addition, calcium in specific non-AWCs promotes AWCON side biases through NSY-5 gap junctions. Our results suggest a novel model in which calcium has dual roles within the NSY-5 network: autonomously promoting AWCOFF and non-autonomously promoting AWCON.

Original languageEnglish (US)
Pages (from-to)4191-4201
Number of pages11
JournalDevelopment (Cambridge)
Volume139
Issue number22
DOIs
StatePublished - Nov 15 2012

Keywords

  • C. elegans
  • Calcium signaling
  • Gap junctions
  • Stochastic left-right neuronal asymmetry

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology

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    Schumacher, J. A., Hsieh, Y. W., Chen, S., Pirri, J. K., Alkema, M. J., Li, W. H., Chang, C., & Chuang, C. F. (2012). Intercellular calcium signaling in a gap junction-coupled cell network establishes asymmetric neuronal fates in C. elegans. Development (Cambridge), 139(22), 4191-4201. https://doi.org/10.1242/dev.083428