Differential beta-arrestin trafficking and endosomal sorting of somatostatin receptor subtypes

J Biol Chem. 2004 May 14;279(20):21374-82. doi: 10.1074/jbc.M313522200. Epub 2004 Mar 4.

Abstract

The physiological responses of somatostatin are mediated by five different G protein-coupled receptors. Although agonist-induced endocytosis of the various somatostatin receptor subtypes (sst(1)-sst(5)) has been studied in detail, little is known about their postendocytic trafficking. Here we show that somatostatin receptors profoundly differ in patterns of beta-arrestin mobilization and endosomal sorting. The beta-arrestin-dependent trafficking of the sst(2A) somatostatin receptor resembled that of a class B receptor in that upon receptor activation, beta-arrestin and the receptor formed stable complexes and internalized together into the same endocytic vesicles. This pattern was dependent on GRK2 (G protein-coupled receptor kinase 2)-mediated phosphorylation of a cluster of phosphate acceptor sites within the cytoplasmic tail of the sst(2A) receptor. Unlike other class B receptors, however, the sst(2A) receptor was rapidly resensitized and recycled to the plasma membrane. The beta-arrestin mobilization of the sst(3) and the sst(5) somatostatin receptors resembled that of a class A receptor in that upon receptor activation, beta-arrestin and the receptor formed relatively unstable complexes that dissociated at or near the plasma membrane. Consequently, beta-arrestin was excluded from sst(3)-containing vesicles. Unlike other class A receptors, a large proportion of sst(3) receptors was subject to ubiquitin-dependent lysosomal degradation and did not rapidly recycle to the plasma membrane. The sst(4) somatostatin receptor is unique in that it did not exhibit agonist-dependent receptor phosphorylation and beta-arrestin recruitment. Together, these findings may provide important clues about the regulation of receptor responsiveness during long-term administration of somatostatin analogs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Arrestins / chemistry
  • Arrestins / genetics
  • Arrestins / physiology*
  • Cell Line
  • Cyclic AMP-Dependent Protein Kinases / metabolism*
  • Endosomes / physiology*
  • G-Protein-Coupled Receptor Kinase 2
  • G-Protein-Coupled Receptor Kinase 3
  • Humans
  • Kidney
  • Mice
  • Molecular Sequence Data
  • Phosphorylation
  • Rabbits
  • Rats
  • Receptors, Somatostatin / physiology*
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • beta-Adrenergic Receptor Kinases
  • beta-Arrestins

Substances

  • Arrestins
  • Receptors, Somatostatin
  • beta-Arrestins
  • Cyclic AMP-Dependent Protein Kinases
  • G-Protein-Coupled Receptor Kinase 3
  • GRK3 protein, human
  • GRK3 protein, mouse
  • Grk2 protein, rat
  • Grk3 protein, rat
  • beta-Adrenergic Receptor Kinases
  • G-Protein-Coupled Receptor Kinase 2