Stabilization of the human beta2-adrenergic receptor TM4-TM3-TM5 helix interface by mutagenesis of Glu122(3.41), a critical residue in GPCR structure

J Mol Biol. 2008 Mar 7;376(5):1305-19. doi: 10.1016/j.jmb.2007.12.028. Epub 2007 Dec 23.

Abstract

G protein-coupled receptor (GPCR) instability represents one of the most profound obstacles in the structural study of GPCRs that bind diffusible ligands. The introduction of targeted mutations at nonconserved residues that lie proximal to helix interfaces has the potential to enhance the fold stability of the receptor helix bundle while maintaining wild-type receptor function. To test this hypothesis, we studied the effect of amino acid substitutions at Glu122(3.41) in the well-studied beta(2)-adrenergic receptor (beta(2)AR), which was predicted from sequence conservation to lie at a position equivalent to a tryptophan residue in rhodopsin at the 3,4,5 helix interface among transmembrane (TM) domains 3, 4, and 5. Replacement of Glu122(3.41) with bulky hydrophobic residues, such as tryptophan, tyrosine, and phenylalanine, increases the yield of functionally folded beta(2)AR by as much as 5-fold. Receptor stability in detergent solution was studied by isothermal denaturation, and it was found that the E122W and E122Y mutations enhanced the beta(2)AR thermal half-life by 9.3- and 6.7-fold, respectively, at 37 degrees C. The beta(1)AR was also stabilized by the introduction of tryptophan at Glu147(3.41), and the effect on protein behavior was similar to the rescue of the unstable wild-type receptor by the antagonist propranolol. Molecular modeling of the E122W and E122Y mutants revealed that the tryptophan ring edge and tyrosine hydroxyl are positioned proximal to the helical break in TM5 introduced by the conserved Pro211(5.50) and may stabilize the helix by interacting favorably with the unpaired carbonyl oxygen of Val206(5.45). Conformational flexibility of TM5 is likely to be a general property of class A GPCRs; therefore, engineering of the TM4-TM3-TM5 interface at the 3.41 position may provide a general strategy for the stabilization of other receptors.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Substitution
  • Cell Line
  • Humans
  • Microscopy, Confocal
  • Molecular Sequence Data
  • Mutagenesis
  • Protein Structure, Tertiary
  • Receptors, Adrenergic, beta-2 / chemistry
  • Receptors, Adrenergic, beta-2 / genetics*
  • Receptors, Adrenergic, beta-2 / metabolism*
  • Receptors, G-Protein-Coupled / chemistry
  • Receptors, G-Protein-Coupled / genetics
  • Receptors, G-Protein-Coupled / metabolism*
  • Sequence Alignment

Substances

  • Receptors, Adrenergic, beta-2
  • Receptors, G-Protein-Coupled