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

• Published in: The EMBO journal Vol. 27; no. 18; pp. 2388 - 2399
• Main Authors: Wang, Ying, Apicella Jr, Alfonso, Lee, Sun-Kyung, Ezcurra, Marina, Slone, Robert D, Goldmit, Maya, Schafer, William R, Shaham, Shai, Driscoll, Monica, Bianchi, Laura
• Format: Journal Article
• Language: English
• Published: Chichester, UK John Wiley & Sons, Ltd 17.09.2008; Nature Publishing Group UK; Blackwell Publishing Ltd; Nature Publishing Group
• Subjects: Acid Sensing Ion Channels; Acidification; Amino Acid Sequence; Amino acids; Animals; C. elegans; Caenorhabditis elegans; Caenorhabditis elegans Proteins - metabolism; Calcium - metabolism; Cellular biology; DEG/ENaC channels; EMBO11; EMBO37; Epithelial Sodium Channels - metabolism; glia; Mammals; Membrane Proteins - metabolism; Models, Biological; Molecular Sequence Data; Nerve Tissue Proteins - metabolism; Neuroglia - metabolism; Neurons - metabolism; Perception; Phylogeny; Protons; Sensory perception; Sequence Homology, Amino Acid; Signal transduction; Sodium Channels - metabolism; Worms; Xenopus laevis; sensory perception; DEG/ENaC channels; glia
• ISSN: 0261-4189; 1460-2075
• DOI: 10.1038/emboj.2008.161

Mammalian neuronal DEG/ENaC channels known as ASICs ( a cid‐ s ensing i on c hannels) 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 ( a cid‐sensitive c hannel, d egenerin‐like) is constitutively open and impermeable to Ca 2+ , 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.