Hydrogen bonding between the 17beta-substituent of a neurosteroid and the GABA(A) receptor is not obligatory for channel potentiation

Br J Pharmacol. 2009 Nov;158(5):1322-9. doi: 10.1111/j.1476-5381.2009.00390.x. Epub 2009 Aug 20.

Abstract

Background and purpose: Potentiating neurosteroids are some of the most efficacious modulators of the mammalian GABA(A) receptor. One of the crucial interactions may be between the C20 ketone group (D-ring substituent at C17) of the neurosteroid, and the N407 and Y410 residues in the M4 domain of the receptor. In this study, we examined the contribution of hydrogen bonding between 17beta-substituents on the steroid D-ring and the GABA(A) receptor to potentiation by neurosteroids.

Experimental approach: Whole-cell and single-channel recordings were made from HEK 293 cells transiently expressing wild-type and mutant alpha1beta2gamma2L GABA(A) receptors.

Key results: A steroid with a 17beta-carbonitrile group (3alpha5alpha18nor17betaCN) was a potent and efficacious potentiator of the GABA(A) receptor. Potentiation was also shown by a cyclosteroid in which C21 and the C18 methyl group of (3alpha,5alpha)-3-hydroxypregnan-20-one are connected within a six-membered ring containing a double bond as a hydrogen bond acceptor (3alpha5alphaCDNC12), a steroid containing a 17beta-ethyl group on the D-ring (3alpha5alpha17betaEt) and a steroid lacking a 17beta-substituent on the D-ring (3alpha5alpha17H). Single-channel kinetic analysis indicates that the kinetic mechanism of action is the same for the neurosteroid 3alpha5alphaP, 3alpha5alpha18nor17betaCN, 3alpha5alphaCDNC12, 3alpha5alpha17betaEt and 3alpha5alpha17H. Interestingly, 3alpha5alpha17betaEt, at up to 3 microM, was incapable of potentiating the alpha1N407A/Y410F double mutant receptor.

Conclusions and implications: Hydrogen bonding between the steroid 17beta-substituent and the GABA(A) receptor is not a critical requirement for channel potentiation. The alpha1N407/Y410 residues are important for neurosteroid potentiation for reasons other than hydrogen bonding between steroid and receptor.

Publication types

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

MeSH terms

  • Androstanols / chemistry
  • Androstanols / pharmacology
  • Animals
  • Binding Sites
  • Cell Line
  • GABA-A Receptor Agonists*
  • Humans
  • Hydrogen Bonding
  • Mutation
  • Neurotransmitter Agents / chemistry
  • Neurotransmitter Agents / metabolism*
  • Nitriles / chemistry
  • Nitriles / pharmacology
  • Norandrostanes / chemistry
  • Norandrostanes / pharmacology
  • Patch-Clamp Techniques
  • Rats
  • Receptors, GABA-A / genetics
  • Receptors, GABA-A / metabolism*
  • Structure-Activity Relationship
  • gamma-Aminobutyric Acid / pharmacology

Substances

  • (3alpha,5beta,17beta)-3-hydroxy-18-norandrostane-17-carbonitrile
  • Androstanols
  • GABA-A Receptor Agonists
  • Neurotransmitter Agents
  • Nitriles
  • Norandrostanes
  • Receptors, GABA-A
  • androstan-3-ol
  • gamma-Aminobutyric Acid