Experimental determination of the vertical alignment between the second and third transmembrane segments of muscle nicotinic acetylcholine receptors

J Neurochem. 2013 Jun;125(6):843-54. doi: 10.1111/jnc.12260. Epub 2013 Apr 30.

Abstract

Nicotinic acetylcholine receptors (nAChR) are members of the Cys-loop ligand-gated ion channel superfamily. Muscle nAChR are heteropentamers that assemble from two α, and one each of β, γ, and δ subunits. Each subunit is composed of three domains, extracellular, transmembrane and intracellular. The transmembrane domain consists of four α-helical segments (M1-M4). Pioneering structural information was obtained using electronmicroscopy of Torpedo nAChR. The recently solved X-ray structure of the first eukaryotic Cys-loop receptor, a truncated (intracellular domain missing) glutamate-gated chloride channel α (GluClα) showed the same overall architecture. However, a significant difference with regard to the vertical alignment between the channel-lining segment M2 and segment M3 was observed. Here, we used functional studies utilizing disulfide trapping experiments in muscle nAChR to determine the spatial orientation between M2 and M3. Our results are in agreement with the vertical alignment as obtained when using the GluClα structure as a template to homology model muscle nAChR, however, they cannot be reconciled with the current Torpedo nAChR model. The vertical M2-M3 alignments as observed in X-ray structures of prokaryotic Gloeobacter violaceus ligand-gated ion channel and GluClα are in agreement. Our results further confirm that this alignment in Cys-loop receptors is conserved between prokaryotes and eukaryotes.

Publication types

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

MeSH terms

  • Animals
  • Caenorhabditis elegans Proteins / chemistry
  • Caenorhabditis elegans Proteins / genetics
  • Chloride Channels / chemistry
  • Chloride Channels / genetics
  • Disulfides / chemistry
  • Female
  • Mice
  • Muscles / metabolism
  • Mutation
  • Oocytes / metabolism
  • Patch-Clamp Techniques
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Receptors, Nicotinic / chemistry*
  • Receptors, Nicotinic / genetics
  • Receptors, Nicotinic / physiology
  • Species Specificity
  • Torpedo
  • Xenopus laevis

Substances

  • Caenorhabditis elegans Proteins
  • Chloride Channels
  • Disulfides
  • Receptors, Nicotinic
  • glutamate-gated chloride channels