TREM2 variant p.R47H as a risk factor for sporadic amyotrophic lateral sclerosis

JAMA Neurol. 2014 Apr;71(4):449-53. doi: 10.1001/jamaneurol.2013.6237.

Abstract

Importance: Amyotrophic lateral sclerosis (ALS) is a fatal neurodegenerative disease in which microglia play a significant and active role. Recently, a rare missense variant (p.R47H) in the microglial activating gene TREM2 was found to increase the risk of several neurodegenerative diseases, including Alzheimer disease. Whether the p.R47H variant is a risk factor for ALS is not known.

Objectives: To determine whether p.R47H (rs75932628) in TREM2 is a risk factor for ALS and assess whether TREM2 expression is dysregulated in disease.

Design, setting, and participants: Samples of DNA from 923 individuals with sporadic ALS and 1854 healthy control individuals self-reported as non-Hispanic white were collected from ALS clinics in the United States and genotyped for the p.R47H variant in TREM2. Clinical data were obtained on ALS participants for genotype/phenotype correlations. Expression of TREM2 was measured by quantitative polymerase chain reaction and compared in spinal cord samples from 18 autopsied patients with ALS and 12 neurologically healthy controls, as well as from wild-type and transgenic SOD1G93A mice.

Main outcomes and measures: Minor allele frequency of rs75932628 and relative expression of TREM2.

Results: The TREM2 variant p.R47H was more common in patients with ALS than in the controls and is therefore a significant risk factor for ALS (odds ratio, 2.40; 95% CI, 1.29-4.15; P = 4.1×10-3). Furthermore, TREM2 expression was increased in spinal cord samples from ALS patients and SOD1G93A mice (P = 2.8×10-4 and P = 2.8×10-9, respectively), confirming dysregulated TREM2 in disease. Expression of TREM2 in the human spinal cord was negatively correlated with survival (P = .04) but not with other phenotypic aspects of disease.

Conclusions and relevance: This study demonstrates that the TREM2 p.R47H variant is a potent risk factor for sporadic ALS. To our knowledge, these findings identify the first genetic influence on neuroinflammation in ALS and highlight the TREM2 signaling pathway as a therapeutic target in ALS and other neurodegenerative diseases.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • Amyotrophic Lateral Sclerosis / diagnosis*
  • Amyotrophic Lateral Sclerosis / genetics*
  • Amyotrophic Lateral Sclerosis / pathology
  • Animals
  • Case-Control Studies
  • Cohort Studies
  • Disease Models, Animal
  • Female
  • Gene Expression Regulation / genetics
  • Genetic Predisposition to Disease / genetics*
  • Genetic Variation / genetics*
  • Humans
  • Inflammation / diagnosis
  • Inflammation / genetics
  • Inflammation / pathology
  • Male
  • Membrane Glycoproteins / biosynthesis
  • Membrane Glycoproteins / genetics*
  • Mice
  • Mice, Transgenic
  • Microglia / metabolism
  • Microglia / pathology
  • Middle Aged
  • Phenotype
  • Receptors, Immunologic / biosynthesis
  • Receptors, Immunologic / genetics*
  • Risk Factors
  • Signal Transduction / genetics
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase-1

Substances

  • Membrane Glycoproteins
  • Receptors, Immunologic
  • SOD1 protein, human
  • TREM2 protein, human
  • Sod1 protein, mouse
  • Superoxide Dismutase
  • Superoxide Dismutase-1

Supplementary concepts

  • Amyotrophic lateral sclerosis 1