7-Dehydrocholesterol-derived oxysterols cause neurogenic defects in Smith-Lemli-Opitz syndrome

Elife. 2022 Sep 16:11:e67141. doi: 10.7554/eLife.67141.

Abstract

Defective 3β-hydroxysterol-Δ7 -reductase (DHCR7) in the developmental disorder, Smith-Lemli-Opitz syndrome (SLOS), results in a deficiency in cholesterol and accumulation of its precursor, 7-dehydrocholesterol (7-DHC). Here, we show that loss of DHCR7 causes accumulation of 7-DHC-derived oxysterol metabolites, premature neurogenesis from murine or human cortical neural precursors, and depletion of the cortical precursor pool, both in vitro and in vivo. We found that a major oxysterol, 3β,5α-dihydroxycholest-7-en-6-one (DHCEO), mediates these effects by initiating crosstalk between glucocorticoid receptor (GR) and neurotrophin receptor kinase TrkB. Either loss of DHCR7 or direct exposure to DHCEO causes hyperactivation of GR and TrkB and their downstream MEK-ERK-C/EBP signaling pathway in cortical neural precursors. Moreover, direct inhibition of GR activation with an antagonist or inhibition of DHCEO accumulation with antioxidants rescues the premature neurogenesis phenotype caused by the loss of DHCR7. These results suggest that GR could be a new therapeutic target against the neurological defects observed in SLOS.

Keywords: 7-dehydrocholesterol; cortical development; glucocorticoid receptor; human; mouse; neurogenesis; neuroscience; oxysterol; smith-lemli-opitz syndrome.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antioxidants
  • Cholesterol
  • Dehydrocholesterols
  • Disease Models, Animal
  • Humans
  • Mice
  • Mitogen-Activated Protein Kinase Kinases
  • Neurogenesis
  • Oxidoreductases
  • Oxidoreductases Acting on CH-CH Group Donors* / genetics
  • Oxysterols* / therapeutic use
  • Receptors, Glucocorticoid
  • Receptors, Nerve Growth Factor
  • Smith-Lemli-Opitz Syndrome* / drug therapy
  • Smith-Lemli-Opitz Syndrome* / genetics
  • Smith-Lemli-Opitz Syndrome* / metabolism

Substances

  • Antioxidants
  • Dehydrocholesterols
  • Oxysterols
  • Receptors, Glucocorticoid
  • Receptors, Nerve Growth Factor
  • Cholesterol
  • 7-dehydrocholesterol
  • Oxidoreductases
  • Oxidoreductases Acting on CH-CH Group Donors
  • Mitogen-Activated Protein Kinase Kinases

Associated data

  • Dryad/10.5061/dryad.zw3r2287f