Loss of Adaptive Myelination Contributes to Methotrexate Chemotherapy-Related Cognitive Impairment

Neuron. 2019 Jul 17;103(2):250-265.e8. doi: 10.1016/j.neuron.2019.04.032. Epub 2019 May 20.

Abstract

Activity-dependent myelination is thought to contribute to adaptive neurological function. However, the mechanisms by which activity regulates myelination and the extent to which myelin plasticity contributes to non-motor cognitive functions remain incompletely understood. Using a mouse model of chemotherapy-related cognitive impairment (CRCI), we recently demonstrated that methotrexate (MTX) chemotherapy induces complex glial dysfunction for which microglial activation is central. Here, we demonstrate that remote MTX exposure blocks activity-regulated myelination. MTX decreases cortical Bdnf expression, which is restored by microglial depletion. Bdnf-TrkB signaling is a required component of activity-dependent myelination. Oligodendrocyte precursor cell (OPC)-specific TrkB deletion in chemotherapy-naive mice results in impaired cognitive behavioral performance. A small-molecule TrkB agonist rescues both myelination and cognitive impairment after MTX chemotherapy. This rescue after MTX depends on intact TrkB expression in OPCs. Taken together, these findings demonstrate a molecular mechanism required for adaptive myelination that is aberrant in CRCI due to microglial activation.

Keywords: BDNF; TrkB; adaptive myelination; chemotherapy-related cognitive impairment; myelin; myelin plasticity; oligodendrocyte; oligodendrocyte precursor cell.

Publication types

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

MeSH terms

  • Animals
  • Brain-Derived Neurotrophic Factor / genetics
  • Brain-Derived Neurotrophic Factor / metabolism
  • Cerebral Cortex / drug effects
  • Cerebral Cortex / metabolism
  • Channelrhodopsins / genetics
  • Channelrhodopsins / metabolism
  • Cognition Disorders / drug therapy*
  • Cognition Disorders / genetics
  • Cognition Disorders / pathology*
  • Disease Models, Animal
  • Humans
  • Immunosuppressive Agents / therapeutic use*
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Methotrexate / therapeutic use*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Myelin Sheath / metabolism*
  • Myelin Sheath / pathology
  • Myelin Sheath / ultrastructure
  • Oligodendrocyte Precursor Cells / drug effects
  • Organic Chemicals / therapeutic use
  • Protein-Tyrosine Kinases / genetics
  • Protein-Tyrosine Kinases / metabolism
  • Recognition, Psychology / drug effects
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Urea / analogs & derivatives
  • Urea / metabolism

Substances

  • 1-(3-dimethylaminopropyl)-3-ethylurea
  • Brain-Derived Neurotrophic Factor
  • Channelrhodopsins
  • Immunosuppressive Agents
  • Luminescent Proteins
  • Membrane Glycoproteins
  • Organic Chemicals
  • PLX5622
  • Urea
  • Ntrk2 protein, mouse
  • Protein-Tyrosine Kinases
  • Methotrexate