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

Ying Wang, Alfonso Apicella, Sun Kyung Lee, Marina Ezcurra, Robert D. Slone, Maya Goldmit, William R. Schafer, Shai Shaham, Monica Driscoll, Laura Bianchi

Research output: Contribution to journalArticle

34 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)2388-2399
Number of pages12
JournalEMBO Journal
Volume27
Issue number18
DOIs
StatePublished - Sep 17 2008

Fingerprint

Neuroglia
Acids
Protons
Degenerin Sodium Channels
Epithelium
Acid Sensing Ion Channels
Acidification
Caenorhabditis elegans
Chemotaxis
Lysine
Neurons
Tissue
Data storage equipment
Amino Acids

Keywords

  • C. elegans
  • DEG/ENaC channels
  • Glia
  • Sensory perception

ASJC Scopus subject areas

  • Genetics
  • Cell Biology

Cite this

A glial DEG/ENaC channel functions with neuronal channel DEG-1 to mediate specific sensory functions in C. elegans. / Wang, Ying; Apicella, Alfonso; Lee, Sun Kyung; Ezcurra, Marina; Slone, Robert D.; Goldmit, Maya; Schafer, William R.; Shaham, Shai; Driscoll, Monica; Bianchi, Laura.

In: EMBO Journal, Vol. 27, No. 18, 17.09.2008, p. 2388-2399.

Research output: Contribution to journalArticle

Wang, Y, Apicella, A, Lee, SK, Ezcurra, M, Slone, RD, Goldmit, M, Schafer, WR, Shaham, S, Driscoll, M & Bianchi, L 2008, 'A glial DEG/ENaC channel functions with neuronal channel DEG-1 to mediate specific sensory functions in C. elegans', EMBO Journal, vol. 27, no. 18, pp. 2388-2399. https://doi.org/10.1038/emboj.2008.161
Wang, Ying ; Apicella, Alfonso ; Lee, Sun Kyung ; Ezcurra, Marina ; Slone, Robert D. ; Goldmit, Maya ; Schafer, William R. ; Shaham, Shai ; Driscoll, Monica ; Bianchi, Laura. / A glial DEG/ENaC channel functions with neuronal channel DEG-1 to mediate specific sensory functions in C. elegans. In: EMBO Journal. 2008 ; Vol. 27, No. 18. pp. 2388-2399.
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