Engineering-specific pharmacological binding sites for peptidyl inhibitors of potassium channels into KcsA

Biochemistry. 2002 Dec 24;41(51):15369-75. doi: 10.1021/bi026264a.

Abstract

The bacterial potassium channel, KcsA, can be modified to express a high-affinity receptor site for the scorpion toxin kaliotoxin (KTX) by substituting subregion I in the P region of KcsA with the one present in the human voltage-gated potassium channel Kv1.3 [Legros, C., Pollmann, V., Knaus, H. G., Farrell, A. M., Darbon, H., Bougis, P. E., Martin-Eauclaire, M. F., and Pongs, O. (2000) J. Biol. Chem. 275, 16918-16924]. This approach opened the way to investigate whether sequence differences in subregion I of Kv1 channels correlate with the distinct pharmacological profiles of peptide inhibitors. A panel of six chimeras between KcsA and human Kv1.1-6 were constructed, expressed in Escherichia coli, purified to homogeneity, and assessed in filter binding assays using either monoiodo-tyrosine-KTX ([(125)I]KTX) or monoiodo-tyrosine-hongotoxin(1)(A19Y/Y37F) ([(125)I]HgTX(1)(A19Y/Y37F)). The KcsA-Kv1.X chimeras were found to have lower affinities for these ligands than the corresponding mammalian Kv1.X channels, indicating that other parts of the channels may contribute to binding or that subtle structural differences exist between these channels. The properties of the KcsA-Kv1.X chimeras were also characterized in surface plasmon resonance experiments. KcsA-Kv1.3 chimeras were immobilized on the surface of a sensor chip for determining, in real time, binding of the peptides. KTX binding properties to immobilized KcsA-Kv1.3 chimera were similar to those determined by filtration techniques. Taken together, our results demonstrate that the pharmacological profile of peptide toxins can be incorporated into KcsA-Kv1.X chimeras containing the subregion I of the corresponding mammalian Kv1.X channels. This innovative approach may facilitate the high-throughput screening of ligand libraries aimed at the discovery of novel potassium channel modulators.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alanine / genetics
  • Amino Acid Sequence
  • Amino Acid Substitution / genetics*
  • Animals
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Binding Sites / genetics
  • Delayed Rectifier Potassium Channels
  • Humans
  • Kv1.1 Potassium Channel
  • Kv1.2 Potassium Channel
  • Kv1.3 Potassium Channel
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed*
  • Peptide Fragments / chemistry*
  • Peptide Fragments / genetics
  • Peptide Fragments / pharmacology*
  • Phenylalanine / genetics
  • Potassium Channel Blockers / chemistry*
  • Potassium Channel Blockers / pharmacology*
  • Potassium Channels / chemistry*
  • Potassium Channels / genetics
  • Potassium Channels, Voltage-Gated*
  • Protein Structure, Tertiary / genetics
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / genetics
  • Scorpion Venoms / chemistry
  • Scorpion Venoms / pharmacology
  • Surface Plasmon Resonance
  • Tyrosine / genetics

Substances

  • Bacterial Proteins
  • Delayed Rectifier Potassium Channels
  • KCNA1 protein, human
  • KCNA2 protein, human
  • KCNA3 protein, human
  • Kv1.2 Potassium Channel
  • Kv1.3 Potassium Channel
  • Peptide Fragments
  • Potassium Channel Blockers
  • Potassium Channels
  • Potassium Channels, Voltage-Gated
  • Recombinant Fusion Proteins
  • Scorpion Venoms
  • hongotoxin 1
  • prokaryotic potassium channel
  • Kv1.1 Potassium Channel
  • Tyrosine
  • Phenylalanine
  • Alanine