Mdm2 directs the ubiquitination of beta-arrestin-sequestered cAMP phosphodiesterase-4D5

J Biol Chem. 2009 Jun 12;284(24):16170-16182. doi: 10.1074/jbc.M109.008078. Epub 2009 Apr 16.

Abstract

Beta-arrestin plays a key role in regulating beta2-adrenoreceptor signaling by interdicting activation of adenylyl cyclase and selectively sequestering cAMP phosphodiesterase-4D5 (PDE4D5) for delivery of an active cAMP degrading system to the site of cAMP synthesis. Here we show that the beta-agonist, isoprenaline, triggers the rapid and transient ubiquitination of PDE4D5 in primary cardiomyocytes, mouse embryo fibroblasts, and HEK293B2 cells constitutively expressing beta2-adrenoceptors. Reconstitution analyses in beta-arrestin1/2 double knockout cells plus small interference RNA knockdown studies indicate that a beta-arrestin-scaffolded pool of the E3-ubiquitin ligase, Mdm2, mediates PDE4D5 ubiquitination. Critical for this is the ubiquitin-interacting motif located in the extreme C terminus of PDE4D5, which is specific to the PDE4D sub-family. In vitro ubiquitination [corrected] of a PDE4D5 spot-immobilized peptide array, followed by a mutagenesis strategy, showed that PDE4D5 ubiquitination occurs at Lys-48, Lys-53, and Lys-78, which are located within its isoform-specific N-terminal region, as well as at Lys-140 located within its regulatory UCR1 module. We suggest that mono-ubiquitination at Lys-140 primes PDE4D5 for a subsequent cascade of polyubiquitination occurring within its isoform-specific N-terminal region at Lys-48, Lys-53, and Lys-78. PDE4D5 interacts with a non-ubiquitinated beta-arrestin sub-population that is likely to be protected from Mdm2-mediated ubiquitination due to steric hindrance caused by sequestered PDE4D5. Ubiquitination of PDE4D5 elicits an increase in the fraction of PDE4D5 sequestered by beta-arrestin in cells, thereby contributing to the fidelity of PDE4D5-beta-arrestin interaction, as well as decreasing the fraction of PDE4D5 sequestered by the scaffolding protein, RACK1.

Publication types

  • Research Support, Non-U.S. Gov't
  • Retracted Publication

MeSH terms

  • Adrenergic beta-Agonists / pharmacology
  • Animals
  • Arrestins / metabolism*
  • Cells, Cultured
  • Consensus Sequence
  • Cyclic Nucleotide Phosphodiesterases, Type 3
  • Cyclic Nucleotide Phosphodiesterases, Type 4
  • Fibroblasts / cytology
  • GTP-Binding Proteins / metabolism
  • Gene Knockout Techniques
  • Humans
  • Isoproterenol / pharmacology
  • Kidney / cytology
  • Lysine / metabolism
  • Mice
  • Myocytes, Cardiac / cytology
  • Neoplasm Proteins / metabolism
  • Phosphoric Diester Hydrolases / chemistry
  • Phosphoric Diester Hydrolases / genetics*
  • Phosphoric Diester Hydrolases / metabolism*
  • Protein Structure, Tertiary
  • Proto-Oncogene Proteins c-mdm2 / genetics
  • Proto-Oncogene Proteins c-mdm2 / metabolism*
  • Rats
  • Receptors for Activated C Kinase
  • Receptors, Cell Surface / metabolism
  • Transfection
  • Ubiquitin / metabolism*
  • Ubiquitination / drug effects
  • Vasopressins / pharmacology
  • beta-Arrestins

Substances

  • Adrenergic beta-Agonists
  • Arrestins
  • Neoplasm Proteins
  • RACK1 protein, human
  • Receptors for Activated C Kinase
  • Receptors, Cell Surface
  • Ubiquitin
  • beta-Arrestins
  • Vasopressins
  • MDM2 protein, human
  • Mdm2 protein, mouse
  • Proto-Oncogene Proteins c-mdm2
  • Phosphoric Diester Hydrolases
  • Cyclic Nucleotide Phosphodiesterases, Type 3
  • Cyclic Nucleotide Phosphodiesterases, Type 4
  • PDE4D protein, human
  • GTP-Binding Proteins
  • Lysine
  • Isoproterenol