Adenosine stimulates depolarization and rise in cytoplasmic [Ca2+] in type I cells of rat carotid bodies

Am J Physiol Cell Physiol. 2006 Jun;290(6):C1592-8. doi: 10.1152/ajpcell.00546.2005. Epub 2006 Jan 25.

Abstract

During hypoxia, the level of adenosine in the carotid bodies increases as a result of ATP catabolism and adenosine efflux via adenosine transporters. Using Ca2+ imaging, we found that adenosine, acting via A2A receptors, triggered a rise in cytoplasmic [Ca2+] ([Ca2+]i) in type I (glomus) cells of rat carotid bodies. The adenosine response could be mimicked by forskolin (but not its inactive analog), and could be abolished by the PKA inhibitor H89. Simultaneous measurements of membrane potential (perforated patch recording) and [Ca2+]i showed that the adenosine-mediated [Ca2+]i rise was accompanied by depolarization. Ni2+, a voltage-gated Ca2+ channel (VGCC) blocker, abolished the adenosine-mediated [Ca2+]i rise. Although adenosine was reported to inhibit a 4-aminopyridine (4-AP)-sensitive K+ current, 4-AP failed to trigger any [Ca2+]i rise, or to attenuate the adenosine response. In contrast, anandamide, an inhibitor of the TWIK-related acid-sensitive K+-1 (TASK-1) channels, triggered depolarization and [Ca2+]i rise. The adenosine response was attenuated by anandamide but not by tetraethylammonium. Our results suggest that adenosine, acting via the adenylate cyclase and PKA pathways, inhibits the TASK-1 K+ channels. This leads to depolarization and activation of Ca2+ entry via VGCC. This excitatory action of adenosine on type I cells may contribute to the chemosensitivity of the carotid body during hypoxia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 4-Aminopyridine / pharmacology
  • Adenosine / metabolism*
  • Adenosine A2 Receptor Antagonists
  • Adenylyl Cyclases / metabolism
  • Animals
  • Calcium / metabolism*
  • Carotid Body / cytology
  • Carotid Body / drug effects
  • Carotid Body / metabolism*
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Cytoplasm / drug effects
  • Cytoplasm / metabolism*
  • Hypoxia / physiopathology
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Nerve Tissue Proteins / drug effects
  • Nerve Tissue Proteins / metabolism
  • Patch-Clamp Techniques
  • Potassium Channel Blockers / pharmacology
  • Potassium Channels, Tandem Pore Domain / drug effects
  • Potassium Channels, Tandem Pore Domain / metabolism
  • Potassium Channels, Voltage-Gated / drug effects
  • Potassium Channels, Voltage-Gated / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Adenosine A2A / metabolism
  • Tetraethylammonium / pharmacology

Substances

  • Adenosine A2 Receptor Antagonists
  • Nerve Tissue Proteins
  • Potassium Channel Blockers
  • Potassium Channels, Tandem Pore Domain
  • Potassium Channels, Voltage-Gated
  • Receptor, Adenosine A2A
  • potassium channel subfamily K member 3
  • Tetraethylammonium
  • 4-Aminopyridine
  • Cyclic AMP-Dependent Protein Kinases
  • Adenylyl Cyclases
  • Adenosine
  • Calcium