C9orf72 promoter hypermethylation is neuroprotective: Neuroimaging and neuropathologic evidence

Neurology. 2015 Apr 21;84(16):1622-30. doi: 10.1212/WNL.0000000000001495. Epub 2015 Mar 20.

Abstract

Objective: To use in vivo neuroimaging and postmortem neuropathologic analysis in C9orf72 repeat expansion patients to investigate the hypothesis that C9orf72 promoter hypermethylation is neuroprotective and regionally selective.

Methods: Twenty patients with a C9orf72 repeat expansion participating in a high-resolution MRI scan and a clinical examination and a subset of patients (n = 11) were followed longitudinally with these measures. Gray matter (GM) density was related to C9orf72 promoter hypermethylation using permutation-based testing. Regional neuronal loss was measured in an independent autopsy series (n = 35) of C9orf72 repeat expansion patients.

Results: GM analysis revealed that hippocampus, frontal cortex, and thalamus are associated with hypermethylation and thus appear to be relatively protected from mutant C9orf72. Neuropathologic analysis demonstrated an association between reduced neuronal loss and hypermethylation in hippocampus and frontal cortex. Longitudinal neuroimaging revealed that hypermethylation is associated with reduced longitudinal decline in GM regions protected by hypermethylation and longitudinal neuropsychological assessment demonstrated that longitudinal decline in verbal recall is protected by hypermethylation.

Conclusions: These cross-sectional and longitudinal neuroimaging studies, along with neuropathologic validation studies, provide converging evidence for neuroprotective properties of C9orf72 promoter hypermethylation. These findings converge with prior postmortem studies suggesting that C9orf72 promoter hypermethylation may be a neuroprotective target for drug discovery.

Publication types

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

MeSH terms

  • Amyotrophic Lateral Sclerosis* / genetics
  • Amyotrophic Lateral Sclerosis* / pathology
  • Amyotrophic Lateral Sclerosis* / physiopathology
  • C9orf72 Protein
  • Cerebral Cortex / metabolism
  • Cerebral Cortex / pathology
  • Cerebral Cortex / physiopathology
  • Cross-Sectional Studies
  • DNA Methylation*
  • DNA Repeat Expansion / genetics
  • Female
  • Frontal Lobe / metabolism
  • Frontal Lobe / pathology
  • Frontal Lobe / physiopathology
  • Frontotemporal Lobar Degeneration* / genetics
  • Frontotemporal Lobar Degeneration* / pathology
  • Frontotemporal Lobar Degeneration* / physiopathology
  • Gray Matter* / metabolism
  • Gray Matter* / pathology
  • Gray Matter* / physiopathology
  • Hippocampus / metabolism
  • Hippocampus / pathology
  • Hippocampus / physiopathology
  • Humans
  • Longitudinal Studies
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Promoter Regions, Genetic
  • Proteins / genetics*
  • Thalamus / metabolism
  • Thalamus / pathology
  • Thalamus / physiopathology

Substances

  • C9orf72 Protein
  • C9orf72 protein, human
  • Proteins