lncRNA Functional Networks in Oligodendrocytes Reveal Stage-Specific Myelination Control by an lncOL1/Suz12 Complex in the CNS

Neuron. 2017 Jan 18;93(2):362-378. doi: 10.1016/j.neuron.2016.11.044. Epub 2016 Dec 29.

Abstract

Long noncoding RNAs (lncRNAs) are emerging as important regulators of cellular functions, but their roles in oligodendrocyte myelination remain undefined. Through de novo transcriptome reconstruction, we establish dynamic expression profiles of lncRNAs at different stages of oligodendrocyte development and uncover a cohort of stage-specific oligodendrocyte-restricted lncRNAs, including a conserved chromatin-associated lncOL1. Co-expression network analyses further define the association of distinct oligodendrocyte-expressing lncRNA clusters with protein-coding genes and predict lncRNA functions in oligodendrocyte myelination. Overexpression of lncOL1 promotes precocious oligodendrocyte differentiation in the developing brain, whereas genetic inactivation of lncOL1 causes defects in CNS myelination and remyelination following injury. Functional analyses illustrate that lncOL1 interacts with Suz12, a component of polycomb repressive complex 2, to promote oligodendrocyte maturation, in part, through Suz12-mediated repression of a differentiation inhibitory network that maintains the precursor state. Together, our findings reveal a key lncRNA epigenetic circuitry through interaction with chromatin-modifying complexes in control of CNS myelination and myelin repair.

Keywords: EZH2; OPC; chromatin remodeling; functional genomics; long noncoding RNA; myelination; neural precursors; oligodendrocyte differentiation; polycomb repressive complex; remyelination.

MeSH terms

  • Animals
  • Blotting, Western
  • Brain / cytology
  • Brain / embryology*
  • Cell Differentiation / genetics*
  • Drosophila Proteins / genetics*
  • Epigenesis, Genetic
  • Gene Expression Regulation, Developmental*
  • Gene Regulatory Networks
  • Immunohistochemistry
  • Mice
  • Myelin Sheath / metabolism*
  • Neural Stem Cells / cytology
  • Neural Stem Cells / metabolism*
  • Oligodendroglia / cytology
  • Oligodendroglia / metabolism*
  • Polycomb Repressive Complex 2 / metabolism*
  • RNA, Long Noncoding / genetics*
  • RNA, Long Noncoding / metabolism
  • Rats
  • Real-Time Polymerase Chain Reaction
  • Receptors, Ionotropic Glutamate / genetics*

Substances

  • Drosophila Proteins
  • IR75b protein, Drosophila
  • RNA, Long Noncoding
  • Receptors, Ionotropic Glutamate
  • Suz12 protein, mouse
  • Polycomb Repressive Complex 2