Loss of the sphingolipid desaturase DEGS1 causes hypomyelinating leukodystrophy

J Clin Invest. 2019 Mar 1;129(3):1240-1256. doi: 10.1172/JCI123959. Epub 2019 Feb 11.

Abstract

Sphingolipid imbalance is the culprit in a variety of neurological diseases, some affecting the myelin sheath. We have used whole-exome sequencing in patients with undetermined leukoencephalopathies to uncover the endoplasmic reticulum lipid desaturase DEGS1 as the causative gene in 19 patients from 13 unrelated families. Shared features among the cases include severe motor arrest, early nystagmus, dystonia, spasticity, and profound failure to thrive. MRI showed hypomyelination, thinning of the corpus callosum, and progressive thalamic and cerebellar atrophy, suggesting a critical role of DEGS1 in myelin development and maintenance. This enzyme converts dihydroceramide (DhCer) into ceramide (Cer) in the final step of the de novo biosynthesis pathway. We detected a marked increase of the substrate DhCer and DhCer/Cer ratios in patients' fibroblasts and muscle. Further, we used a knockdown approach for disease modeling in Danio rerio, followed by a preclinical test with the first-line treatment for multiple sclerosis, fingolimod (FTY720, Gilenya). The enzymatic inhibition of Cer synthase by fingolimod, 1 step prior to DEGS1 in the pathway, reduced the critical DhCer/Cer imbalance and the severe locomotor disability, increasing the number of myelinating oligodendrocytes in a zebrafish model. These proof-of-concept results pave the way to clinical translation.

Keywords: Neurodegeneration; Neuroscience.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified* / genetics
  • Animals, Genetically Modified* / metabolism
  • Brain* / enzymology
  • Brain* / pathology
  • Disease Models, Animal
  • Fatty Acid Desaturases / genetics
  • Fatty Acid Desaturases / metabolism
  • Fingolimod Hydrochloride / pharmacology*
  • Hereditary Central Nervous System Demyelinating Diseases* / drug therapy
  • Hereditary Central Nervous System Demyelinating Diseases* / enzymology
  • Hereditary Central Nervous System Demyelinating Diseases* / genetics
  • Hereditary Central Nervous System Demyelinating Diseases* / pathology
  • Humans
  • Locomotion / drug effects
  • Oligodendroglia / enzymology
  • Oligodendroglia / pathology
  • Zebrafish Proteins* / genetics
  • Zebrafish* / genetics
  • Zebrafish* / metabolism

Substances

  • Zebrafish Proteins
  • Fatty Acid Desaturases
  • DEGS1 protein, human
  • Fingolimod Hydrochloride