Activation of the neurokinin-1 receptor in rat spinal astrocytes induces Ca2+ release from IP3-sensitive Ca2+ stores and extracellular Ca2+ influx through TRPC3

Neurochem Int. 2010 Dec;57(8):923-34. doi: 10.1016/j.neuint.2010.09.012. Epub 2010 Oct 7.

Abstract

Substance P (SP) plays an important role in pain transmission through the stimulation of the neurokinin (NK) receptors expressed in neurons of the spinal cord, and the subsequent increase in the intracellular Ca(2+) concentration ([Ca(2+)](i)) as a result of this stimulation. Recent studies suggest that spinal astrocytes also contribute to SP-related pain transmission through the activation of NK receptors. However, the mechanisms involved in the SP-stimulated [Ca(2+)](i) increase by spinal astrocytes are unclear. We therefore examined whether (and how) the activation of NK receptors evoked increase in [Ca(2+)](i) in rat cultured spinal astrocytes using a Ca(2+) imaging assay. Both SP and GR73632 (a selective agonist of the NK1 receptor) induced both transient and sustained increases in [Ca(2+)](i) in a dose-dependent manner. The SP-induced increase in [Ca(2+)](i) was significantly attenuated by CP-96345 (an NK1 receptor antagonist). The GR73632-induced increase in [Ca(2+)](i) was completely inhibited by pretreatment with U73122 (a phospholipase C inhibitor) or xestospongin C (an inositol 1,4,5-triphosphate (IP(3)) receptor inhibitor). In the absence of extracellular Ca(2+), GR73632 induced only a transient increase in [Ca(2+)](i). In addition, H89, an inhibitor of protein kinase A (PKA), decreased the GR73632-mediated Ca(2+) release from intracellular Ca(2+) stores, while bisindolylmaleimide I, an inhibitor of protein kinase C (PKC), enhanced the GR73632-induced influx of extracellular Ca(2+). RT-PCR assays revealed that canonical transient receptor potential (TRPC) 1, 2, 3, 4 and 6 mRNA were expressed in spinal astrocytes. Moreover, BTP2 (a general TRPC channel inhibitor) or Pyr3 (a TRPC3 inhibitor) markedly blocked the GR73632-induced sustained increase in [Ca(2+)](i). These findings suggest that the stimulation of the NK-1 receptor in spinal astrocytes induces Ca(2+) release from IP(3-)sensitive intracellular Ca(2+) stores, which is positively modulated by PKA, and subsequent Ca(2+) influx through TRPC3, which is negatively regulated by PKC.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Astrocytes / drug effects
  • Astrocytes / metabolism*
  • Calcium Signaling / drug effects
  • Calcium Signaling / physiology*
  • Cells, Cultured
  • Cyclic AMP-Dependent Protein Kinases / antagonists & inhibitors
  • Cyclic AMP-Dependent Protein Kinases / physiology
  • Feedback, Physiological / drug effects
  • Feedback, Physiological / physiology
  • Inositol 1,4,5-Trisphosphate / pharmacology*
  • Inositol 1,4,5-Trisphosphate Receptors / antagonists & inhibitors
  • Inositol 1,4,5-Trisphosphate Receptors / physiology
  • Intracellular Fluid / drug effects
  • Intracellular Fluid / metabolism
  • Neurokinin-1 Receptor Antagonists
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase C / physiology
  • Rats
  • Rats, Wistar
  • Receptors, Neurokinin-1 / agonists
  • Receptors, Neurokinin-1 / physiology*
  • Spinal Cord / cytology
  • Spinal Cord / metabolism*
  • TRPC Cation Channels / drug effects
  • TRPC Cation Channels / physiology*

Substances

  • Inositol 1,4,5-Trisphosphate Receptors
  • Neurokinin-1 Receptor Antagonists
  • Receptors, Neurokinin-1
  • TRPC Cation Channels
  • TRPC3 cation channel
  • Inositol 1,4,5-Trisphosphate
  • Cyclic AMP-Dependent Protein Kinases
  • Protein Kinase C