Pentameric concatenated (alpha4)(2)(beta2)(3) and (alpha4)(3)(beta2)(2) nicotinic acetylcholine receptors: subunit arrangement determines functional expression

Br J Pharmacol. 2009 Mar;156(6):970-81. doi: 10.1111/j.1476-5381.2008.00104.x.

Abstract

Background and purpose: alpha4 and beta2 nicotinic acetylcholine (ACh) receptor subunits expressed heterologously in Xenopus oocytes assemble into a mixed population of (alpha4)(2)(beta2)(3) and (alpha4)(3)(beta2)(2) receptors. In order to express these receptors separately in heterologous systems, we have engineered pentameric concatenated (alpha4)(2)(beta2)(3) and (alpha4)(3)(beta2)(2) receptors.

Experimental approach: alpha4 and beta2 subunits were concatenated by synthetic linkers into pentameric constructs to produce either (alpha4)(2)(beta2)(3) or (alpha4)(3)(beta2)(2) receptors. Using two-electrode voltage-clamp techniques, we examined the ability of the concatenated constructs to produce functional expression in Xenopus oocytes. Functional constructs were further characterized in respect to agonists, competitive antagonists, Ca2+ permeability, sensitivity to modulation by Zn2+ and sensitivity to up-regulation by chaperone protein 14-3-3.

Key results: We found that pentameric concatamers with a subunit arrangement of beta2_alpha4_beta2_alpha4_beta2 or beta2_alpha4_beta2_alpha4_alpha4 were stable and functional in Xenopus oocytes. By comparison, when alpha4 and beta2 were concatenated with a subunit order of beta2_beta2_alpha4_beta2_alpha4 or beta2_alpha4_alpha4_beta2_alpha4, functional expression in Xenopus oocytes was very low, even though the proteins were synthesized and stable. Both beta2_alpha4_beta2_alpha4_beta2 and beta2_alpha4_beta2_alpha4_alpha4 concatamers recapitulated the ACh concentration response curve, the sensitivity to Zn2+ modulation, Ca2+ permeability and the sensitivity to up-regulation by chaperone protein 14-3-3 of the corresponding non-linked (alpha4)(2)(beta2)(3) and (alpha4)(3)(beta2)(2) receptors respectively. Using these concatamers, we found that most alpha4beta2-preferring compounds studied, including A85380, 5I-A85380, cytisine, epibatidine, TC2559 and dihydro-beta-erythroidine, demonstrate stoichiometry-specific potencies and efficacies.

Conclusions and implications: We concluded that the alpha4beta2 nicotinic ACh receptors produced with beta2_alpha4_beta2_alpha4_beta2 or beta2_alpha4_beta2_alpha4_alpha4 pentameric constructs are valid models of non-linked (alpha4)(2)(beta2)(3) and (alpha4)(3)(beta2)(2) receptors respectively.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / biosynthesis
  • Animals
  • Calcium / metabolism
  • Chlorides / pharmacology
  • DNA, Concatenated / genetics
  • In Vitro Techniques
  • Nicotinic Agonists / pharmacology
  • Nicotinic Antagonists / pharmacology
  • Oocytes / physiology
  • Patch-Clamp Techniques
  • Protein Engineering
  • Protein Multimerization
  • Protein Subunits / biosynthesis
  • Protein Subunits / genetics
  • Protein Subunits / physiology
  • Receptors, Nicotinic / biosynthesis
  • Receptors, Nicotinic / genetics
  • Receptors, Nicotinic / physiology*
  • Up-Regulation
  • Xenopus laevis
  • Zinc Compounds / pharmacology

Substances

  • 14-3-3 Proteins
  • Chlorides
  • DNA, Concatenated
  • Nicotinic Agonists
  • Nicotinic Antagonists
  • Protein Subunits
  • Receptors, Nicotinic
  • Zinc Compounds
  • zinc chloride
  • Calcium