Tryptophan Scanning Reveals Dense Packing of Connexin Transmembrane Domains in Gap Junction Channels Composed of Connexin32

J Biol Chem. 2015 Jul 10;290(28):17074-84. doi: 10.1074/jbc.M115.650747. Epub 2015 May 12.

Abstract

Tryptophan was substituted for residues in all four transmembrane domains of connexin32. Function was assayed using dual cell two-electrode voltage clamp after expression in Xenopus oocytes. Tryptophan substitution was poorly tolerated in all domains, with the greatest impact in TM1 and TM4. For instance, in TM1, 15 substitutions were made, six abolished coupling and five others significantly reduced function. Only TM2 and TM3 included a distinct helical face that lacked sensitivity to tryptophan substitution. Results were visualized on a comparative model of Cx32 hemichannel. In this model, a region midway through the membrane appears highly sensitive to tryptophan substitution and includes residues Arg-32, Ile-33, Met-34, and Val-35. In the modeled channel, pore-facing regions of TM1 and TM2 were highly sensitive to tryptophan substitution, whereas the lipid-facing regions of TM3 and TM4 were variably tolerant. Residues facing a putative intracellular water pocket (the IC pocket) were also highly sensitive to tryptophan substitution. Although future studies will be required to separate trafficking-defective mutants from those that alter channel function, a subset of interactions important for voltage gating was identified. Interactions important for voltage gating occurred mainly in the mid-region of the channel and focused on TM1. To determine whether results could be extrapolated to other connexins, TM1 of Cx43 was scanned revealing similar but not identical sensitivity to TM1 of Cx32.

Keywords: Cx32; TM domain interactions; comparative model; connexin; gap junction; gating; hemichannel; mutagenesis; transmembrane domain; tryptophan scanning.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amino Acid Substitution
  • Animals
  • Connexin 43 / chemistry
  • Connexin 43 / genetics
  • Connexin 43 / metabolism
  • Connexins / chemistry*
  • Connexins / genetics
  • Connexins / metabolism
  • Female
  • Gap Junction beta-1 Protein
  • Gap Junctions / chemistry*
  • Gap Junctions / metabolism
  • Lipid Bilayers / chemistry
  • Lipid Bilayers / metabolism
  • Models, Molecular
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Oocytes / metabolism
  • Protein Interaction Domains and Motifs
  • Protein Subunits
  • Rats
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Tryptophan / chemistry
  • Xenopus laevis

Substances

  • Connexin 43
  • Connexins
  • Gja1 protein, rat
  • Lipid Bilayers
  • Protein Subunits
  • Recombinant Proteins
  • Tryptophan

Associated data

  • PDB/2zw3