Connectivity and orientation of the seven helical bundle in the tachykinin NK-1 receptor probed by zinc site engineering

EMBO J. 1996 Nov 15;15(22):6213-9.

Abstract

A high affinity, tridentate metal ion site has been constructed previously by His substitutions in an antagonist binding site located between transmembrane segment (TM)-V and TM-VI in the substance P NK-1 receptor. Here, an attempt is made to probe helix-helix interactions systematically in the NK-1 receptor by engineering of bis-His Zn(II) sites. His residues were introduced at selected positions individually and in combinations in the exterior segments of TM-II, III and V in both the wild-type background and after Ala substitution of naturally occurring His residues, and the increase in the affinity for Zn(II) was monitored in competition binding experiments with iodinated substance P or a tritiated non-peptide antagonist. In this way, two high affinity bis-His sites were constructed between position 193 in TM-V (Glu193, G1uV:01) and position 109 in TM-III (Asn1O9, AsnIII:05) as well as between the neighboring, naturally occurring His108 in TM-III (HisIII:04) and position 92 in TM-II (Tyr92, TyrII:24), respectively. Functionally, the coordination of zinc ions at these two sites blocked the receptor as it antagonized the substance P-induced increase in phosphatidylinositol turnover. It is concluded that the bis-His zinc sites from the central TM-III helix to TM-II and -V, respectively, together with the interconnected, previously constructed tridentate site between TM-V and -VI, constitute a basic network of distance constraints for the molecular models of receptors with seven transmembrane segments which, for example, strongly support an anti-clockwise orientation of the seven helical bundle as viewed from the extracellular space.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Binding Sites
  • COS Cells
  • Histidine / genetics
  • Histidine / metabolism
  • Membrane Proteins / chemistry
  • Models, Molecular
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed / genetics
  • Phosphatidylinositols / metabolism
  • Protein Binding / genetics
  • Protein Engineering*
  • Protein Structure, Secondary
  • Receptors, Neurokinin-1 / chemistry*
  • Receptors, Neurokinin-1 / metabolism
  • Substance P
  • Zinc / metabolism*

Substances

  • Membrane Proteins
  • Phosphatidylinositols
  • Receptors, Neurokinin-1
  • Substance P
  • Histidine
  • Zinc