Mutationally induced disulfide bond formation within the third extracellular loop causes melanocortin 4 receptor inactivation in patients with obesity

J Biol Chem. 2003 Dec 5;278(49):48666-73. doi: 10.1074/jbc.M309941200. Epub 2003 Sep 22.

Abstract

By screening patients with severe early onset obesity for mutations within the melanocortin 4 receptor (MC4R) gene, we have identified a missense mutation (C271R) that occurs homozygous in two siblings with obesity. In-depth functional characterization of C271R revealed a right-shifted concentration response curve due to lower affinity to natural and synthetic MC4R agonists and a reduced cell surface expression. Cys-271 is located in the third extracellular loop. Here, we provide evidence that Cys-271 forms an intra-loop disulfide bond with Cys-277. Unexpectedly, we found that loss of receptor function is not only caused by the disruption of this disulfide bridge. Our data strongly support a new mechanism in which the receptor malfunction in the C271R mutant is induced by formation of a functionally disastrous disulfide bridge between Cys-277 and a third Cys residue at position 279. Mutational and chemical disruption of this improper disulfide bond was able to restore normal receptor potency. By demonstrating that a loss of a disulfide bond-participating Cys residue can favor a functionally disastrous disulfide bond, we now add a new mechanism of how Cys residues can be involved in G-protein-coupled receptor malfunction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Amino Acid Sequence
  • Child
  • Disulfides / chemistry*
  • Female
  • Humans
  • Male
  • Molecular Sequence Data
  • Mutation, Missense
  • Obesity / metabolism*
  • Pedigree
  • Radioligand Assay
  • Receptor, Melanocortin, Type 4 / antagonists & inhibitors*
  • Receptor, Melanocortin, Type 4 / chemistry
  • Receptor, Melanocortin, Type 4 / genetics
  • Receptor, Melanocortin, Type 4 / metabolism
  • Sequence Homology, Amino Acid

Substances

  • Disulfides
  • Receptor, Melanocortin, Type 4