New insights into human prostacyclin receptor structure and function through natural and synthetic mutations of transmembrane charged residues

Br J Pharmacol. 2007 Oct;152(4):513-22. doi: 10.1038/sj.bjp.0707413. Epub 2007 Aug 20.

Abstract

Background and purpose: The human prostacyclin receptor (hIP), a G-protein coupled receptor (GPCR) expressed mainly on platelets and vascular smooth muscle cells, plays important protective roles in the cardiovascular system. We hypothesized that significant insights could be gained into the structure and function of the hIP through mutagenesis of its energetically unfavourably located transmembrane charged residues.

Experimental approach: Within its putative transmembrane helices fourteen hydrophilic residues, both unique and conserved across GPCRs, were systematically mutated to assess for effects on receptor structure and function.

Key results: Mutations of ten of the fourteen charged residues to alanine exhibited defective binding and/or activation. Key potential interactions were identified between 6 core residues; E116(3.49)-R117(3.50) (salt bridge TMIII), D274(7.35)-R279(7.40) (salt bridge TMVII), and D60(2.50)-D288(7.49) (H-bond network TMII-TMVII). Further detailed investigation of E116(3.49) (TMIII) with mutation to a glutamine showed a 2.6-fold increase in agonist-independent basal activity. This increase in activity accounts for a proportion ( approximately 13%) of full agonist induced activation. We further characterized two novel naturally occurring human mutations, R77(2.33)C and R279(7.40)C recently identified in a 1455 human genomic DNA sample screen. The R77(2.33)C variant appeared to exclusively affect expression, while the R279(7.40)C variant, exhibited considerable deficiencies in both agonist binding and activation.

Conclusions and implications: Transmembrane charged residues play important roles in maintaining the hIP binding pocket and ensuring normal activation. The critical nature of these charged residues and the presence of naturally occurring mutations have important implications in the rational design of prostacyclin agonists for treating cardiovascular disease.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alprostadil / pharmacology
  • Amino Acid Sequence
  • Amino Acids / chemistry
  • Amino Acids / genetics
  • Amino Acids / metabolism
  • Animals
  • Binding Sites / genetics
  • Binding, Competitive / drug effects
  • COS Cells
  • Chlorocebus aethiops
  • Cyclic AMP / chemistry
  • Cyclic AMP / metabolism
  • Dose-Response Relationship, Drug
  • Epoprostenol / analogs & derivatives
  • Epoprostenol / pharmacology
  • Humans
  • Hydrophobic and Hydrophilic Interactions
  • Iloprost / pharmacology
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Membrane Proteins / physiology
  • Molecular Sequence Data
  • Mutation*
  • Radioligand Assay
  • Receptors, Epoprostenol
  • Receptors, G-Protein-Coupled / genetics
  • Receptors, G-Protein-Coupled / metabolism*
  • Receptors, G-Protein-Coupled / physiology
  • Receptors, Prostaglandin / genetics
  • Receptors, Prostaglandin / metabolism*
  • Receptors, Prostaglandin / physiology
  • Transfection
  • Tritium

Substances

  • Amino Acids
  • Membrane Proteins
  • PTGIR protein, human
  • Receptors, Epoprostenol
  • Receptors, G-Protein-Coupled
  • Receptors, Prostaglandin
  • Tritium
  • carboprostacyclin
  • Epoprostenol
  • Cyclic AMP
  • Alprostadil
  • Iloprost