Two kinases mediate agonist-dependent phosphorylation and desensitization of the beta 2-adrenergic receptor

Symp Soc Exp Biol. 1990:44:225-40.

Abstract

Binding of the catecholamine agonists epinephrine and norepinephrine to the beta-adrenergic receptor (BAR) rapidly activates adenylate cyclase via the stimulatory guanine nucleotide regulatory protein Gs, and results in rises in cellular levels of cAMP. However, continuous exposure to these agonists leads within minutes to a dampening of the enzymatic response. Both in vivo and in vitro studies have implicated agonist-induced phosphorylation of BAR in this process. These results include the isolation of a novel beta-adrenergic receptor kinase (BARK), which has been shown to preferentially phosphorylate receptors that are occupied by agonist when assessed in vitro. Recent studies in our laboratory have examined the desensitization process in intact cells to determine where on the receptor molecule functionally relevant phosphorylation occurs, and to identify the kinase(s) involved. In one set of studies, site-specific mutagenic techniques with the cloned gene for the human beta 2-adrenergic receptor were utilized to delete putative sites of phosphorylation by BARK and/or the cAMP-dependent protein kinase (PKA). Following expression of the mutated receptors in mammalian cells, the cells were challenged with different concentrations of agonist for 10-15 min and the functional and phosphorylation properties of the mutant receptors were then assessed. In another set of studies human A431 cells were permeabilized with low concentrations of digitonin and treated with selective inhibitors of both BARK and PKA. The cells were then exposed to desensitizing concentrations of agonist, and similar measurements performed. Taken together, the results from both sets of studies suggest that exposure of cells to low (nanomolar) concentrations of agonist leads to phosphorylation of the receptor on one or both consensus sites for PKA, and that the predominant effect of this phosphorylation on the adenylyl cyclase response is a loss in sensitivity of the receptor to further stimulation by the agonist. In contrast, exposure of cells to higher (micromolar) concentrations of agonist leads to BAR phosphorylation by both PKA and BARK, the latter on the carboxyl terminal region of the receptor. Phosphorylation of the receptor by both kinases appears to be required for the full desensitization effect seen with the high concentration of agonist, which includes both losses in sensitivity and in the maximal responsiveness of the adenylyl cyclase response upon subsequent challenge with the agonist. Such a dual kinase control of BAR phosphorylation may have important implications for understanding the regulation of desensitization under different physiological circumstances.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adenylyl Cyclases / metabolism
  • Adrenergic beta-Agonists / metabolism*
  • Animals
  • Cells, Cultured
  • Cloning, Molecular
  • Cyclic AMP / biosynthesis
  • Cyclic AMP-Dependent Protein Kinases*
  • Down-Regulation / physiology
  • Epinephrine / pharmacology
  • Humans
  • Mammals / metabolism*
  • Norepinephrine / pharmacology
  • Phosphorylation
  • Protein Kinases / metabolism*
  • Receptors, Adrenergic, beta / genetics
  • Receptors, Adrenergic, beta / metabolism*
  • beta-Adrenergic Receptor Kinases

Substances

  • Adrenergic beta-Agonists
  • Receptors, Adrenergic, beta
  • Cyclic AMP
  • Protein Kinases
  • Cyclic AMP-Dependent Protein Kinases
  • beta-Adrenergic Receptor Kinases
  • Adenylyl Cyclases
  • Norepinephrine
  • Epinephrine