Left-right olfactory asymmetry results from antagonistic functions of voltage-activated calcium channels and the Raw repeat protein OLRN-I in C. elegans

Sarah L. Bauer Huang, Yasunori Saheki, Miri K. VanHoven, Ichiro Torayama, Takeshi Ishihara, Isao Katsura, Alexander Van Der Linden, Piali Sengupta, Cornelia I. Bargmann

Research output: Contribution to journalArticle

45 Scopus citations

Abstract

Background: The left and right AWC olfactory neurons in Caenorhabdltis elegans differ in their functions and in their expression of chemosensory receptor genes; in each animal, one AWC randomly takes on one identity, designated AWCOFF, and the contralateral AWC becomes AWC ON. Signaling between AWC neurons induces left-right asymmetry through a gap junction network and a claudin-related protein, which inhibit a calcium-regulated MAP kinase pathway in the neuron that becomes AWC ON. Results: We show here that the asymmetry gene olm-1 acts downstream of the gap junction and claudin genes to inhibit the calcium-MAP kinase pathway in AWCON. OLRN-1, a protein with potential membrane-association domains, is related to the Drosophila Raw protein, a negative regulator of JNK mitogen-activated protein (MAP) kinase signaling, olrn-1 opposes the action of two voltage-activated calcium channel homologs, unc-2 (CaV2) and egl-19 (CaVI), which act together to stimulate the calcium/calmodulin-dependent kinase CaMKII and the MAP kinase pathway. Calcium channel activity is essential in AWCOFF, and the two AWC neurons coordinate left-right asymmetry using signals from the calcium channels and signals from olrn-1. Conclusion: olrn-1 and voltage-activated calcium channels are mediators and targets of AWC signaling that act at the transition between a multicellular signaling network and cell-autonomous execution of the decision. We suggest that the asymmetry decision in AWC results from the intercellular coupling of voltage-regulated channels, whose cross-regulation generates distinct calcium signals in the left and right AWC neurons. The interpretation of these signals by the kinase cascade initiates the sustained difference between the two cells.

Original languageEnglish
Article number24
JournalNeural Development
Volume2
Issue number1
DOIs
StatePublished - Dec 1 2007
Externally publishedYes

Fingerprint Dive into the research topics of 'Left-right olfactory asymmetry results from antagonistic functions of voltage-activated calcium channels and the Raw repeat protein OLRN-I in C. elegans'. Together they form a unique fingerprint.

  • Cite this