Nicotine-induced up regulation of α4β2 neuronal nicotinic receptors is mediated by the protein kinase C-dependent phosphorylation of α4 subunits

Neuroscience. 2010 Nov 24;171(1):12-22. doi: 10.1016/j.neuroscience.2010.09.005. Epub 2010 Sep 17.

Abstract

Sustained exposure to nicotine is well known to increase the cell surface density of α4β2* neuronal nicotinic receptors both in vivo and in vitro, but the cellular mechanisms mediating this effect are equivocal. Using a pharmacological approach to investigate the effects of nicotine on receptor subunit expression and phosphorylation in SH-EP1 cells expressing human α4 and β2 nicotinic receptor subunits, we have demonstrated that incubation with nicotine for 24 h increased the expression of immature and mature forms of both α4 and β2 subunits in a concentration-dependent manner, and that inhibition of protein kinase C (PKC), but not cAMP-dependent protein kinase (PKA) inhibited the nicotine-induced increased expression of subunits. Incubation of cells with nicotine for 24 h also increased the phosphorylation of immature forms of α4 subunits similar to that induced by activation of either PKC or PKA. When cells were preincubated with nicotine, the PKC-mediated increased phosphorylation was inhibited; the PKA-mediated phosphorylation was unaltered. The phosphopeptide maps for immature α4 subunits following nicotine exposure or PKC activation were identical, and phosphoamino acid analyses indicated phosphorylation on serine residues only. Results indicate that nicotine-induced up regulation of α4β2 neuronal nicotinic receptors involves a PKC-dependent mechanism and likely reflects the ability of nicotine to activate PKC, leading to the phosphorylation of immature α4 subunits, promoting subunit assembly and receptor maturation. Because up regulation of these receptors has been implicated to mediate tolerance, locomotor sensitization and addiction to nicotine, results identify a potential new target for modulating the effects of nicotine on the brain.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Analysis of Variance
  • Autoradiography / methods
  • Cell Line, Transformed
  • Colforsin / pharmacology
  • Dose-Response Relationship, Drug
  • Humans
  • Nicotine / pharmacology*
  • Nicotinic Agonists / pharmacology*
  • Phorbol 12,13-Dibutyrate / pharmacology
  • Phosphorus Isotopes / metabolism
  • Phosphorylation / drug effects
  • Protein Kinase C / metabolism*
  • Receptors, Nicotinic / genetics
  • Receptors, Nicotinic / metabolism*
  • Transfection
  • Up-Regulation / drug effects*

Substances

  • Nicotinic Agonists
  • Phosphorus Isotopes
  • Receptors, Nicotinic
  • nicotinic acetylcholine receptor alpha4 subunit
  • nicotinic receptor alpha4beta2
  • Colforsin
  • Phorbol 12,13-Dibutyrate
  • Nicotine
  • Protein Kinase C