Visualizing pregnenolone sulfate-like modulators of NMDA receptor function reveals intracellular and plasma-membrane localization

Neuropharmacology. 2019 Jan:144:91-103. doi: 10.1016/j.neuropharm.2018.10.015. Epub 2018 Oct 15.

Abstract

Positive modulators of NMDA receptors are important candidates for therapeutic development to treat psychiatric disorders including autism and schizophrenia. Sulfated neurosteroids have been studied as positive allosteric modulators of NMDA receptors for years, but we understand little about the cellular fate of these compounds, an important consideration for drug development. Here we focus on a visualizable sulfated neurosteroid analogue, KK-169. As expected of a pregnenolone sulfate analogue, the compound strongly potentiates NMDA receptor function, is an antagonist of GABAA receptors, exhibits occlusion with pregnenolone sulfate potentiation, and requires receptor domains important for pregnenolone sulfate potentiation. KK-169 exhibits somewhat higher potency than the natural parent, pregnenolone sulfate. The analogue contains a side-chain alkyne group, which we exploited for retrospective click labeling of neurons. Although the anionic sulfate group is expected to hinder cell entry, we detected significant accumulation of KK-169 in neurons with even brief incubations. Adding a photolabile diazirine group revealed that the expected plasma membrane localization of KK-169 is likely lost during fixation. Overall, our studies reveal new facets of the structure-activity relationship of neurosteroids at NMDA receptors, and their intracellular distribution suggests that sulfated neurosteroids could have unappreciated targets in addition to plasma membrane receptors.

Keywords: Click chemistry; GABA; Glutamate; NMDA; Photolabeling; Pregnenolone sulfate.

Publication types

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

MeSH terms

  • Allosteric Regulation
  • Animals
  • Cell Membrane / drug effects*
  • Cell Membrane / metabolism
  • Cells, Cultured
  • Click Chemistry
  • Cytoplasm / drug effects*
  • Cytoplasm / metabolism
  • Excitatory Amino Acid Agonists / chemistry
  • Excitatory Amino Acid Agonists / pharmacology*
  • Glutamic Acid / metabolism
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Humans
  • Mice
  • Oocytes
  • Rats, Sprague-Dawley
  • Receptors, N-Methyl-D-Aspartate / agonists*
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Structure-Activity Relationship
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology
  • Xenopus laevis

Substances

  • Excitatory Amino Acid Agonists
  • Receptors, N-Methyl-D-Aspartate
  • Glutamic Acid