Ulk4 deficiency leads to hypomyelination in mice

Glia. 2018 Jan;66(1):175-190. doi: 10.1002/glia.23236. Epub 2017 Oct 16.

Abstract

Brain nerve fibers are insulated by myelin which is produced by oligodendrocytes. Defects in myelination are increasingly recognized as a common pathology underlying neuropsychiatric and neurodevelopmental disorders, which are associated with deletions of the Unc-51-like kinase 4 (ULK4) gene. Key transcription factors have been identified for oligodendrogenesis, but little is known about their associated regulators. Here we report that Ulk4 acts as a key regulator of myelination. Myelination is reduced by half in the Ulk4tm1a/tm1a hypomorph brain, whereas expression of axonal marker genes Tubb3, Nefh, Nefl and Nefm remains unaltered. Transcriptome analyses reveal that 8 (Gfap, Mbp, Mobp, Plp1, Slc1a2, Ttr, Cnp, Scd2) of the 10 most significantly altered genes in the Ulk4tm1a/tm1a brain are myelination-related. Ulk4 is co-expressed in Olig2+ (pan-oligodendrocyte marker) and CC1+ (mature myelinated oligodendrocyte marker) cells during postnatal development. Major oligodendrogeneic transcription factors, including Olig2, Olig1, Myrf, Sox10, Sox8, Sox6, Sox17, Nkx2-2, Nkx6-2 and Carhsp1, are significantly downregulated in the mutants. mRNA transcripts enriched in oligodendrocyte progenitor cells (OPCs), the newly formed oligodendrocytes (NFOs) and myelinating oligodendrocytes (MOs), are significantly attenuated. Expression of stage-specific oligodendrocyte factors including Cspg4, Sox17, Nfasc, Enpp6, Sirt2, Cnp, Plp1, Mbp, Ugt8, Mag and Mog are markedly decreased. Indirect effects of axon caliber and neuroinflammation may also contribute to the hypomyelination, as Ulk4 mutants display smaller axons and increased neuroinflammation. This is the first evidence demonstrating that ULK4 is a crucial regulator of myelination, and ULK4 may therefore become a novel therapeutic target for hypomyelination diseases.

Keywords: Ulk4; hypomyelination; knockout mice; oligodendrogenesis; white matter integrity.

MeSH terms

  • Animals
  • Animals, Newborn
  • Astrocytes / metabolism
  • Astrocytes / ultrastructure
  • Calcium-Binding Proteins / metabolism
  • Cerebral Cortex / pathology
  • Demyelinating Diseases / genetics*
  • Demyelinating Diseases / pathology
  • Disease Models, Animal
  • Gene Expression Regulation, Developmental / genetics*
  • Glial Fibrillary Acidic Protein / metabolism
  • HMGB Proteins / genetics
  • HMGB Proteins / metabolism
  • Homeobox Protein Nkx-2.2
  • Mice
  • Mice, Transgenic
  • Microfilament Proteins / metabolism
  • Microscopy, Electron, Transmission
  • Mutation / genetics
  • Myelin Proteins / genetics
  • Myelin Proteins / metabolism
  • Myelin Sheath / metabolism
  • Myelin Sheath / pathology*
  • Oligodendrocyte Transcription Factor 2 / genetics
  • Oligodendrocyte Transcription Factor 2 / metabolism
  • Oligodendroglia / metabolism
  • Oligodendroglia / ultrastructure
  • Protein Serine-Threonine Kinases / deficiency*
  • Protein Serine-Threonine Kinases / genetics
  • SOXF Transcription Factors / genetics
  • SOXF Transcription Factors / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Aif1 protein, mouse
  • Calcium-Binding Proteins
  • Glial Fibrillary Acidic Protein
  • HMGB Proteins
  • Homeobox Protein Nkx-2.2
  • Microfilament Proteins
  • Myelin Proteins
  • Nkx2-2 protein, mouse
  • Oligodendrocyte Transcription Factor 2
  • SOXF Transcription Factors
  • Sox17 protein, mouse
  • Transcription Factors
  • Ulk4 protein, mouse
  • Protein Serine-Threonine Kinases