A fundamental role for the nitric oxide-G-kinase signaling pathway in mediating intercellular Ca(2+) waves in glia

J Neurosci. 2000 Mar 1;20(5):1767-79. doi: 10.1523/JNEUROSCI.20-05-01767.2000.

Abstract

In this study, we highlight a role for the nitric oxide-cGMP-dependent protein kinase (NO-G-kinase) signaling pathway in glial intercellular Ca(2+) wave initiation and propagation. Addition of the NO donor molsidomine (100-500 microM) or puffing aqueous NO onto primary glial cell cultures evoked an increase in [Ca(2+)](i) in individual cells and also local intercellular Ca(2+) waves, which persisted after removal of extracellular Ca(2+). High concentrations of ryanodine (100-200 microM) and antagonists of the NO-G-kinase signaling pathway essentially abrogated the NO-induced increase in [Ca(2+)](i), indicating that NO mobilizes Ca(2+) from a ryanodine receptor-linked store, via the NO-G-kinase signaling pathway. Addition of 10 microM nicardipine to cells resulted in a slowing of the molsidomine-induced rise in [Ca(2+)](i), and inhibition of Mn(2+) quench of cytosolic fura-2 fluorescence mediated by a bolus application of 2 microM aqueous NO to cells, indicating that NO also induces Ca(2+) influx in glia. Mechanical stress of individual glial cells resulted in an increase in intracellular NO in target and neighboring cells and intercellular Ca(2+) waves, which were NO, cGMP, and G-kinase dependent, because incubating cells with nitric oxide synthase, guanylate cyclase, and G-kinase inhibitors, or NO scavengers, reduced Delta[Ca(2+)](i) and the rate of Ca(2+) wave propagation in these cultures. Results from this study suggest that NO-G-kinase signaling is coupled to Ca(2+) mobilization and influx in glial cells and that this pathway plays a fundamental role in the generation and propagation of intercellular Ca(2+) waves in glia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aminoquinolines / pharmacology
  • Animals
  • Antineoplastic Agents / pharmacology
  • Apyrase / pharmacology
  • Astrocytes / chemistry
  • Astrocytes / cytology
  • Astrocytes / enzymology*
  • Caenorhabditis elegans Proteins
  • Calcium / metabolism*
  • Calcium Channel Blockers / pharmacology
  • Cells, Cultured
  • Chelating Agents / pharmacology
  • Cyclic GMP / analogs & derivatives
  • Cyclic GMP / pharmacology
  • Cyclic N-Oxides / pharmacology
  • Egtazic Acid / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Estrenes / pharmacology
  • Free Radical Scavengers / pharmacology
  • GTP-Binding Proteins / metabolism*
  • Imidazoles / pharmacology
  • Ionomycin / pharmacology
  • Ionophores / pharmacology
  • Neurons / cytology
  • Nicardipine / pharmacology
  • Nitric Oxide / metabolism*
  • Nitric Oxide Synthase / metabolism
  • Phosphodiesterase Inhibitors / pharmacology
  • Potassium Chloride / pharmacology
  • Prosencephalon / cytology
  • Pyrrolidinones / pharmacology
  • Rats
  • Receptor, Insulin / metabolism
  • Ryanodine / pharmacology
  • Ryanodine Receptor Calcium Release Channel / physiology
  • Signal Transduction / drug effects
  • Signal Transduction / physiology*
  • Suramin / pharmacology
  • Thionucleotides / pharmacology
  • Type C Phospholipases / metabolism
  • omega-N-Methylarginine / pharmacology

Substances

  • 8-(4-chlorophenylthio)guanosine 3',5'-cyclic monophosphorothioate
  • Aminoquinolines
  • Antineoplastic Agents
  • Caenorhabditis elegans Proteins
  • Calcium Channel Blockers
  • Chelating Agents
  • Cyclic N-Oxides
  • Enzyme Inhibitors
  • Estrenes
  • Free Radical Scavengers
  • Imidazoles
  • Ionophores
  • Phosphodiesterase Inhibitors
  • Pyrrolidinones
  • Ryanodine Receptor Calcium Release Channel
  • Thionucleotides
  • 1-(6-((3-methoxyestra-1,3,5(10)-trien-17-yl)amino)hexyl)-1H-pyrrole-2,5-dione
  • Ryanodine
  • 2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide
  • omega-N-Methylarginine
  • Nitric Oxide
  • Egtazic Acid
  • Ionomycin
  • Suramin
  • Potassium Chloride
  • 6-anilino-5,8-quinolinedione
  • Nicardipine
  • Nitric Oxide Synthase
  • DAF-2 protein, C elegans
  • Receptor, Insulin
  • Type C Phospholipases
  • GTP-Binding Proteins
  • Apyrase
  • Cyclic GMP
  • Calcium