Dual mode of glucagon receptor internalization: role of PKCα, GRKs and β-arrestins

Exp Cell Res. 2011 Dec 10;317(20):2981-94. doi: 10.1016/j.yexcr.2011.10.001. Epub 2011 Oct 6.

Abstract

Glucagon levels are elevated in diabetes and some liver diseases. Increased glucagon secretion leads to abnormal stimulation of glucagon receptors (GRs) and consequent elevated glucose production in the liver. Blocking glucagon receptor signaling has been proposed as a potential treatment option for diabetes and other conditions associated with hyperglycemia. Elucidating mechanisms of GR desensitization and downregulation may help identify new drug targets besides GR itself. The present study explores the mechanisms of GR internalization and the role of PKCα, GPCR kinases (GRKs) and β-arrestins therein. We have reported previously that PKCα mediates GR phosphorylation and desensitization. While the PKC agonist, PMA, did not affect GR internalization when tested alone, it increased glucagon-mediated GR internalization by 25-40% in GR-expressing HEK-293 cells (HEK-GR cells). In both primary hepatocytes and HEK-GR cells, glucagon treatment recruited PKCα to the plasma membrane where it colocalized with GR. We also observed that overexpression of GRK2, GRK3, or GRK5 enhanced GR internalization. In addition, we found that GR utilizes both clathrin- and caveolin-mediated endocytosis in HEK-GR cells. Glucagon triggered translocation of both β-arrestin1 and β-arrestin2 from the cytosol to the perimembrane region, and overexpression of β-arrestin1 and β-arrestin2 increased GR internalization. Furthermore, both β-arrestin1 and β-arrestin2 colocalized with GR and with Cav-1, suggesting the possible involvement of these arrestins in GR internalization.

Publication types

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

MeSH terms

  • Animals
  • Arrestins / metabolism*
  • Caveolins / metabolism
  • Cell Membrane / metabolism
  • Cells, Cultured
  • Clathrin / metabolism
  • Cricetinae
  • Endocytosis / physiology
  • G-Protein-Coupled Receptor Kinases / metabolism*
  • Glucagon / metabolism
  • HEK293 Cells
  • Hepatocytes / metabolism
  • Humans
  • Male
  • Protein Kinase C-alpha / metabolism*
  • Protein Transport
  • Receptors, Glucagon / metabolism*
  • beta-Arrestins

Substances

  • Arrestins
  • Caveolins
  • Clathrin
  • Receptors, Glucagon
  • beta-Arrestins
  • Glucagon
  • Protein Kinase C-alpha
  • G-Protein-Coupled Receptor Kinases