Charge and geometry of residues in the loop 2 β hairpin differentially affect agonist and ethanol sensitivity in glycine receptors

J Pharmacol Exp Ther. 2012 May;341(2):543-51. doi: 10.1124/jpet.111.190942. Epub 2012 Feb 22.

Abstract

Recent studies highlighted the importance of loop 2 of α1 glycine receptors (GlyRs) in the propagation of ligand-binding energy to the channel gate. Mutations that changed polarity at position 52 in the β hairpin of loop 2 significantly affected sensitivity to ethanol. The present study extends the investigation to charged residues. We found that substituting alanine with the negative glutamate at position 52 (A52E) significantly left-shifted the glycine concentration response curve and increased sensitivity to ethanol, whereas the negative aspartate substitution (A52D) significantly right-shifted the glycine EC₅₀ but did not affect ethanol sensitivity. It is noteworthy that the uncharged glutamine at position 52 (A52Q) caused only a small right shift of the glycine EC₅₀ while increasing ethanol sensitivity as much as A52E. In contrast, the shorter uncharged asparagine (A52N) caused the greatest right shift of glycine EC₅₀ and reduced ethanol sensitivity to half of wild type. Collectively, these findings suggest that charge interactions determined by the specific geometry of the amino acid at position 52 (e.g., the 1-Å chain length difference between aspartate and glutamate) play differential roles in receptor sensitivity to agonist and ethanol. We interpret these results in terms of a new homology model of GlyR based on a prokaryotic ion channel and propose that these mutations form salt bridges to residues across the β hairpin (A52E-R59 and A52N-D57). We hypothesize that these electrostatic interactions distort loop 2, thereby changing agonist activation and ethanol modulation. This knowledge will help to define the key physical-chemical parameters that cause the actions of ethanol in GlyRs.

Publication types

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

MeSH terms

  • Alanine / chemistry
  • Animals
  • Aspartic Acid / chemistry
  • Ethanol / chemistry*
  • Female
  • Glutamic Acid / chemistry
  • Glycine / metabolism
  • Humans
  • Ion Channel Gating
  • Ion Channels / genetics
  • Ion Channels / metabolism
  • Mutation
  • Oocytes
  • Protein Binding
  • Protein Structure, Tertiary
  • Receptors, Glycine / agonists*
  • Receptors, Glycine / chemistry*
  • Receptors, Glycine / genetics
  • Receptors, Glycine / metabolism
  • Static Electricity
  • Xenopus laevis

Substances

  • Ion Channels
  • Receptors, Glycine
  • Aspartic Acid
  • Ethanol
  • Glutamic Acid
  • Alanine
  • Glycine