Essential role of the C148-C227 disulphide bridge in the human 5-HT2A homodimeric receptor

Biochem Pharmacol. 2020 Jul:177:113985. doi: 10.1016/j.bcp.2020.113985. Epub 2020 Apr 18.

Abstract

The 5-HT2A receptor is a homodimeric G protein-coupled receptor implied in multiple diseases, including schizophrenia. Recently, its co-crystallisation with the antipsychotic drugs zotepine and risperidone has revealed the importance of its extracellular domains in its pharmacology. Previous studies have shown that the non-specific disruption of extracellular disulphide bridges in the 5-HT2A receptor decreases ligand binding and receptor activation. There is enough evidence to hypothesize that this decrease may be due to a reduction of the disulphide bridge that links transmembrane domain 3 (TM-3) and extracellular loop 2 (ECL-2) of the 5-HT2A receptor via cysteine 148 (C148) and C227. Thus, to study the influence of the C148-C227 disulphide bridge on 5-HT2A receptor pharmacology, we substituted C148 and C227 in the human 5-HT2A receptor (WT) with alanines, to obtain two single mutants (C148A and C227A) and a double mutant (C148A/C227A), and the resultant DNA constructs were used to generate four stable cell lines. These substitutions reduced the binding of the 5-HT2A receptor to [3H]lysergic acid diethylamide ([3H]LSD) and impeded the 5-HT2A receptor-mediated activation of phospholipase C (PLC). Furthermore, bioluminescence resonance energy transfer (BRET) and western blotting analysis revealed that these mutations did not alter the homodimeric nature of the 5-HT2A receptor. However, fluorescence microscopy showed that these mutations hindered receptor trafficking to the cell membrane. These results illustrate the importance of the disulphide bridge between TM-3 and ECL-2 in maintaining the correct 5-HT2A receptor conformation to allow ligand binding and migration of the homodimeric receptor to the cell membrane.

Keywords: Disulfide bridge; Extracellular domains; GPCRs; Ligand binding; Serotonin 2A receptor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Substitution
  • Binding Sites
  • Calcium / metabolism*
  • Cell Line
  • Cell Membrane / chemistry
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism*
  • Disulfides / chemistry*
  • Founder Effect
  • Gene Expression
  • HEK293 Cells
  • Humans
  • Ligands
  • Lysergic Acid Diethylamide / pharmacology
  • Mutation
  • Protein Binding
  • Protein Multimerization
  • Protein Transport
  • Receptor, Serotonin, 5-HT2A / chemistry*
  • Receptor, Serotonin, 5-HT2A / genetics
  • Receptor, Serotonin, 5-HT2A / metabolism
  • Recombinant Proteins
  • Serotonin / pharmacology
  • Type C Phospholipases / genetics
  • Type C Phospholipases / metabolism*

Substances

  • Disulfides
  • Ligands
  • Receptor, Serotonin, 5-HT2A
  • Recombinant Proteins
  • Serotonin
  • Lysergic Acid Diethylamide
  • Type C Phospholipases
  • Calcium