Role of CNPase in the oligodendrocytic extracellular 2',3'-cAMP-adenosine pathway

Glia. 2013 Oct;61(10):1595-606. doi: 10.1002/glia.22523. Epub 2013 Aug 6.

Abstract

Extracellular adenosine 3',5'-cyclic monophosphate (3',5'-cAMP) is an endogenous source of localized adenosine production in many organs. Recent studies suggest that extracellular 2',3'-cAMP (positional isomer of 3',5'-cAMP) is also a source of adenosine, particularly in the brain in vivo post-injury. Moreover, in vitro studies show that both microglia and astrocytes can convert extracellular 2',3'-cAMP to adenosine. Here, we examined the ability of primary mouse oligodendrocytes and neurons to metabolize extracellular 2',3'-cAMP and their respective adenosine monophosphates (2'-AMP and 3'-AMP). Cells were also isolated from mice deficient in 2',3'-cyclic nucleotide-3'-phosphodiesterase (CNPase). Oligodendrocytes metabolized 2',3'-cAMP to 2'-AMP with 10-fold greater efficiency than did neurons (and also more than previously examined microglia and astrocytes); whereas, the production of 3'-AMP was minimal in both oligodendrocytes and neurons. The production of 2'-AMP from 2',3'-cAMP was reduced by 65% in CNPase -/- versus CNPase +/+ oligodendrocytes. Oligodendrocytes also converted 2'-AMP to adenosine, and this was also attenuated in CNPase -/- oligodendrocytes. Inhibition of classic 3',5'-cAMP-3'-phosphodiesterases with 3-isobutyl-1-methylxanthine did not block metabolism of 2',3'-cAMP to 2'-AMP and inhibition of classic ecto-5'-nucleotidase (CD73) with α,β-methylene-adenosine-5'-diphosphate did not attenuate the conversion of 2'-AMP to adenosine. These studies demonstrate that oligodendrocytes express the extracellular 2',3'-cAMP-adenosine pathway (2',3'-cAMP → 2'-AMP → adenosine). This pathway is more robustly expressed in oligodendrocytes than in all other CNS cell types because CNPase is the predominant enzyme that metabolizes 2',3'-cAMP to 2-AMP in CNS cells. By reducing levels of 2',3'-cAMP (a mitochondrial toxin) and increasing levels of adenosine (a neuroprotectant), oligodendrocytes may protect axons from injury.

Keywords: 2′,3′-cAMP; 2′,3′-cyclic nucleotide-3′-phosphodiesterase; 2′-AMP; 3′-AMP; adenosine.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 1-Methyl-3-isobutylxanthine / pharmacology
  • 2',3'-Cyclic-Nucleotide Phosphodiesterases / deficiency
  • 2',3'-Cyclic-Nucleotide Phosphodiesterases / metabolism*
  • Adenine Nucleotides / metabolism
  • Adenosine / metabolism*
  • Adenosine Monophosphate / metabolism
  • Adenosine Triphosphate / analogs & derivatives
  • Adenosine Triphosphate / pharmacology
  • Animals
  • Cells, Cultured
  • Embryo, Mammalian
  • Extracellular Fluid / metabolism*
  • Mice
  • Mice, Transgenic
  • Neurons / drug effects
  • Neurons / physiology
  • Oligodendroglia / drug effects
  • Oligodendroglia / metabolism*
  • Phosphodiesterase Inhibitors / pharmacology
  • Signal Transduction / genetics
  • Signal Transduction / physiology*

Substances

  • Adenine Nucleotides
  • Phosphodiesterase Inhibitors
  • Adenosine Monophosphate
  • 2',3'-cyclic AMP
  • Adenosine Triphosphate
  • 2',3'-Cyclic-Nucleotide Phosphodiesterases
  • Adenosine
  • alpha,beta-methyleneadenosine 5'-triphosphate
  • 1-Methyl-3-isobutylxanthine