View the Current Issue

Article

  • The EMBO Journal (2008) 27, 2388 - 2399
  • doi:10.1038/emboj.2008.161

Published online: 14 August 2008

A glial DEG/ENaC channel functions with neuronal channel DEG-1 to mediate specific sensory functions in C. elegans

Ying Wang1,a, Alfonso Apicella Jr2,a, Sun-Kyung Lee2, Marina Ezcurra2, Robert D Slone3, Maya Goldmit4, William R Schafer2, Shai Shaham4, Monica Driscoll3 and Laura Bianchi1

  1. Department of Physiology and Biophysics, Miller School of Medicine, University of Miami, Miami, FL, USA
  2. Cell Biology Division, MRC Laboratory of Molecular Biology, Cambridge, UK
  3. Department of Molecular Biology and Biochemistry, Rutgers University, Piscataway, NJ, USA
  4. Laboratory of Developmental Genetics, The Rockefeller University, New York, NY, USA

Correspondence to:

Laura Bianchi, Department of Physiology and Biophysics, Miller School of Medicine, University of Miami, 1600 NW 10th Avenue, Room 5133, Rosenstiel Building, Miami, FL 33136, USA. Tel.: +1 305 243 1887; Fax: +1 305 243 5931; E-mail: lbianchi@med.miami.edu

aThese authors contributed equally to this work

Received 20 February 2008; Accepted 24 July 2008

Mammalian neuronal DEG/ENaC channels known as ASICs (acid-sensing ion channels) mediate sensory perception and memory formation. ASICS are closed at rest and are gated by protons. Members of the DEG/ENaC family expressed in epithelial tissues are called ENaCs and mediate Na+ transport across epithelia. ENaCs exhibit constitutive activity and strict Na+ selectivity. We report here the analysis of the first DEG/ENaC in Caenorhabditis elegans with functional features of ENaCs that is involved in sensory perception. ACD-1 (acid-sensitive channel, degenerin-like) is constitutively open and impermeable to Ca2+, yet it is required with neuronal DEG/ENaC channel DEG-1 for acid avoidance and chemotaxis to the amino acid lysine. Surprisingly, we document that ACD-1 is required in glia rather than neurons to orchestrate sensory perception. We also report that ACD-1 is inhibited by extracellular and intracellular acidification and, based on the analysis of an acid-hypersensitive ACD-1 mutant, we propose a mechanism of action of ACD-1 in sensory responses based on its sensitivity to protons. Our findings suggest that channels with ACD-1 features may be expressed in mammalian glia and have important functions in controlling neuronal function.

  • Keywords:

    • C. elegans,
    • DEG/ENaC channels,
    • glia,
    • sensory perception