Vanishing white matter: deregulated integrated stress response as therapy target

Ann Clin Transl Neurol. 2019 Aug;6(8):1407-1422. doi: 10.1002/acn3.50826. Epub 2019 Jul 18.

Abstract

Objective: Vanishing white matter (VWM) is a fatal, stress-sensitive leukodystrophy that mainly affects children and is currently without treatment. VWM is caused by recessive mutations in eukaryotic initiation factor 2B (eIF2B) that is crucial for initiation of mRNA translation and its regulation during the integrated stress response (ISR). Mutations reduce eIF2B activity. VWM pathomechanisms remain unclear. In contrast with the housekeeping function of eIF2B, astrocytes are selectively affected in VWM. One study objective was to test our hypothesis that in the brain translation of specific mRNAs is altered by eIF2B mutations, impacting primarily astrocytes. The second objective was to investigate whether modulation of eIF2B activity could ameliorate this altered translation and improve the disease.

Methods: Mice with biallelic missense mutations in eIF2B that recapitulate human VWM were used to screen for mRNAs with altered translation in brain using polysomal profiling. Findings were verified in brain tissue from VWM patients using qPCR and immunohistochemistry. The compound ISRIB (for "ISR inhibitor") was administered to VWM mice to increase eIF2B activity. Its effect on translation, neuropathology, and clinical signs was assessed.

Results: In brains of VWM compared to wild-type mice we observed the most prominent changes in translation concerning ISR mRNAs; their expression levels correlated with disease severity. We substantiated these findings in VWM patients' brains. ISRIB normalized expression of mRNA markers, ameliorated brain white matter pathology and improved motor skills in VWM mice.

Interpretation: The present findings show that ISR deregulation is central in VWM pathomechanisms and a viable target for therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetamides / pharmacology*
  • Activating Transcription Factor 4 / metabolism
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Astrocytes / metabolism
  • Brain / metabolism
  • Cell Cycle Proteins / metabolism
  • Cerebellum / drug effects
  • Corpus Callosum / drug effects
  • Cyclohexylamines / pharmacology*
  • Eukaryotic Initiation Factor-2B / genetics*
  • Eukaryotic Initiation Factor-2B / metabolism
  • Humans
  • Leukoencephalopathies / drug therapy*
  • Leukoencephalopathies / genetics
  • Leukoencephalopathies / pathology*
  • Mice
  • Mutation
  • Protein Biosynthesis
  • Protein Serine-Threonine Kinases / metabolism
  • White Matter / pathology

Substances

  • 2-(4-chlorophenoxy)-N-(4-(2-(4-chlorophenoxy)acetamido)cyclohexyl)acetamide
  • Acetamides
  • Adaptor Proteins, Signal Transducing
  • Atf4 protein, mouse
  • Cell Cycle Proteins
  • Cyclohexylamines
  • EIF4EBP1 protein, human
  • Eif4ebp1 protein, mouse
  • Eukaryotic Initiation Factor-2B
  • Activating Transcription Factor 4
  • Protein Serine-Threonine Kinases
  • eIF2alpha kinase, mouse