Simple chordates exhibit a proton-independent function of acid-sensing ion channels

Tatjana Coric, Yale J. Passamaneck, Ping Zhang, Anna Di Gregorio, Cecilia M. Canessa

Research output: Contribution to journalArticle

Abstract

Acid-sensing ion channels (ASICs) constitute a family of neuron-specific voltage-insensitive sodium channels gated by extracellular protons. Functions of ASICs in mammals include nociception, mechanosensation, and modulation of synaptic transmission. However, the role protons play in mediating the effects of ASICs remains elusive. We have examined ASICs from the ascidian Ciona intestinalis, a simple chordate organism whose nervous system in the larval stage exhibits high similarity to that of higher vertebrates. We found that the ascidian genome contains a single ASIC gene that gives rise to two splice forms analogous to the mammalian ASIC1 and ASIC2. CiASIC is expressed in most neurons of the larva but is absent in the adult. Despite high sequence similarity with mammalian counterparts, CiASIC is proton-insensitive when examined in heterologous systems or in larval neurons; the latter rules out the possibility that proton sensitivity is conferred by accessory proteins or particular factors present only in Ciona neurons. Down-regulation of the CiASIC transcript by double-stranded RNA disrupted the regular pattern of larval swimming, implying that proton-independent mechanisms mediate the effects of ASIC in vivo. Together the data identify ASIC as a highly conserved channel distinctive of chordate nervous systems and show that protons are not essential for ASIC function.

Original languageEnglish (US)
Pages (from-to)1914-1923
Number of pages10
JournalFASEB Journal
Volume22
Issue number6
DOIs
StatePublished - Jun 2008

Fingerprint

Acid Sensing Ion Channels
Chordata
ion channels
protons
Protons
acids
Neurons
neurons
Urochordata
Ascidiacea
Neurology
nervous system
Nervous System
Genes
Ciona intestinalis
Voltage-Gated Sodium Channels
nociception
synaptic transmission
sodium channels
Mammals

Keywords

  • Ascidian
  • Ciona
  • Degenerin/epithelial sodium channel (ENaC) family
  • Knockdown expression
  • Proton gating

ASJC Scopus subject areas

  • Agricultural and Biological Sciences (miscellaneous)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Biochemistry
  • Cell Biology

Cite this

Simple chordates exhibit a proton-independent function of acid-sensing ion channels. / Coric, Tatjana; Passamaneck, Yale J.; Zhang, Ping; Di Gregorio, Anna; Canessa, Cecilia M.

In: FASEB Journal, Vol. 22, No. 6, 06.2008, p. 1914-1923.

Research output: Contribution to journalArticle

Coric, Tatjana ; Passamaneck, Yale J. ; Zhang, Ping ; Di Gregorio, Anna ; Canessa, Cecilia M. / Simple chordates exhibit a proton-independent function of acid-sensing ion channels. In: FASEB Journal. 2008 ; Vol. 22, No. 6. pp. 1914-1923.
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