The fifth transmembrane domain of angiotensin II Type 1 receptor participates in the formation of the ligand-binding pocket and undergoes a counterclockwise rotation upon receptor activation

J Biol Chem. 2009 Nov 13;284(46):31953-61. doi: 10.1074/jbc.M109.051839. Epub 2009 Sep 22.

Abstract

The octapeptide hormone angiotensin II exerts a wide variety of cardiovascular effects through the activation of the angiotensin II Type 1 (AT(1)) receptor, which belongs to the G protein-coupled receptor superfamily. Like other G protein- coupled receptors, the AT(1) receptor possesses seven transmembrane domains that provide structural support for the formation of the ligand-binding pocket. The role of the fifth transmembrane domain (TMD5) was investigated using the substituted cysteine accessibility method. All of the residues within Thr-190 to Leu-217 region were mutated one at a time to cysteine, and after expression in COS-7 cells, the mutant receptors were treated with the sulfhydryl-specific alkylating agent methanethiosulfonate-ethylammonium (MTSEA). MTSEA reacts selectively with water-accessible, free sulfhydryl groups of endogenous or introduced point mutation cysteines. If a cysteine is found in the binding pocket, the covalent modification will affect the binding kinetics of the ligand. MTSEA substantially decreased the binding affinity of L197C-AT(1), N200C-AT(1), I201C-AT(1), G203C-AT(1), and F204C-AT(1) mutant receptors, which suggests that these residues orient themselves within the water-accessible binding pocket of the AT(1) receptor. Interestingly, this pattern of acquired MTSEA sensitivity was altered for TMD5 reporter cysteines engineered in a constitutively active N111G-AT(1) receptor background. Indeed, mutant I201C-N111G-AT(1) became more sensitive to MTSEA, whereas mutant G203C-N111G-AT(1) lost some sensitivity. Our results suggest that constitutive activation of AT(1) receptor causes an apparent counterclockwise rotation of TMD5 as viewed from the extracellular side.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Substitution
  • Angiotensin II / pharmacology*
  • Animals
  • Binding Sites
  • COS Cells
  • Chlorocebus aethiops
  • Ethyl Methanesulfonate / analogs & derivatives
  • Ethyl Methanesulfonate / pharmacology
  • Humans
  • Indicators and Reagents / pharmacology
  • Kinetics
  • Ligands
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Mutation / genetics
  • Protein Binding
  • Protein Conformation
  • Receptor, Angiotensin, Type 1 / chemistry*
  • Receptor, Angiotensin, Type 1 / genetics
  • Receptor, Angiotensin, Type 1 / metabolism*
  • Transfection
  • Type C Phospholipases / metabolism
  • Vasoconstrictor Agents / pharmacology*

Substances

  • Indicators and Reagents
  • Ligands
  • Receptor, Angiotensin, Type 1
  • Vasoconstrictor Agents
  • methanethiosulfonate ethylammonium
  • Angiotensin II
  • Ethyl Methanesulfonate
  • Type C Phospholipases