Glycosphingolipid metabolic reprogramming drives neural differentiation

EMBO J. 2018 Apr 3;37(7):e97674. doi: 10.15252/embj.201797674. Epub 2017 Dec 27.

Abstract

Neural development is accomplished by differentiation events leading to metabolic reprogramming. Glycosphingolipid metabolism is reprogrammed during neural development with a switch from globo- to ganglio-series glycosphingolipid production. Failure to execute this glycosphingolipid switch leads to neurodevelopmental disorders in humans, indicating that glycosphingolipids are key players in this process. Nevertheless, both the molecular mechanisms that control the glycosphingolipid switch and its function in neurodevelopment are poorly understood. Here, we describe a self-contained circuit that controls glycosphingolipid reprogramming and neural differentiation. We find that globo-series glycosphingolipids repress the epigenetic regulator of neuronal gene expression AUTS2. AUTS2 in turn binds and activates the promoter of the first and rate-limiting ganglioside-producing enzyme GM3 synthase, thus fostering the synthesis of gangliosides. By this mechanism, the globo-AUTS2 axis controls glycosphingolipid reprogramming and neural gene expression during neural differentiation, which involves this circuit in neurodevelopment and its defects in neuropathology.

Keywords: AUTS2; bistability; epigenetics; glycosphingolipids; neural differentiation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Differentiation / drug effects
  • Cell Differentiation / genetics
  • Cell Differentiation / physiology*
  • Cellular Reprogramming / drug effects
  • Cellular Reprogramming / physiology*
  • Cytoskeletal Proteins
  • Epigenomics
  • Gangliosides / metabolism
  • Gene Expression
  • Gene Silencing
  • Glycosphingolipids / metabolism*
  • Glycosphingolipids / pharmacology
  • HeLa Cells
  • Histones / metabolism
  • Humans
  • Neurodevelopmental Disorders
  • Neurogenesis / drug effects
  • Neurogenesis / genetics
  • Neurogenesis / physiology*
  • Neurons / metabolism
  • Promoter Regions, Genetic / drug effects
  • Proteins / genetics
  • Proteins / metabolism
  • Sialyltransferases / genetics
  • Sialyltransferases / metabolism
  • Transcription Factors

Substances

  • AUTS2 protein, human
  • Cytoskeletal Proteins
  • Gangliosides
  • Glycosphingolipids
  • Histones
  • Proteins
  • Transcription Factors
  • Sialyltransferases
  • haematoside synthetase