Tau Pathology Drives Dementia Risk-Associated Gene Networks toward Chronic Inflammatory States and Immunosuppression

Cell Rep. 2020 Nov 17;33(7):108398. doi: 10.1016/j.celrep.2020.108398.

Abstract

To understand how neural-immune-associated genes and pathways contribute to neurodegenerative disease pathophysiology, we performed a systematic functional genomic analysis in purified microglia and bulk tissue from mouse and human AD, FTD, and PSP. We uncover a complex temporal trajectory of microglial-immune pathways involving the type 1 interferon response associated with tau pathology in the early stages, followed by later signatures of partial immune suppression and, subsequently, the type 2 interferon response. We find that genetic risk for dementias shows disease-specific patterns of pathway enrichment. We identify drivers of two gene co-expression modules conserved from mouse to human, representing competing arms of microglial-immune activation (NAct) and suppression (NSupp) in neurodegeneration. We validate our findings by using chemogenetics, experimental perturbation data, and single-cell sequencing in post-mortem brains. Our results refine the understanding of stage- and disease-specific microglial responses, implicate microglial viral defense pathways in dementia pathophysiology, and highlight therapeutic windows.

Keywords: chemical genomics; frontotemporal dementia; gene network; inflammasome; interferon; neurodegeneration; progressive supranuclear palsy; systems biology; transcriptomics.

Publication types

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

MeSH terms

  • Aged
  • Animals
  • Brain / metabolism
  • Dementia / genetics*
  • Female
  • Frontotemporal Dementia / genetics
  • Gene Regulatory Networks / genetics
  • Genetic Predisposition to Disease
  • Genomics / methods
  • Humans
  • Immunosuppression Therapy
  • Inflammation / genetics
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microglia / metabolism
  • Neurodegenerative Diseases / genetics
  • Neurodegenerative Diseases / metabolism
  • Primary Cell Culture
  • Risk Factors
  • Tauopathies / genetics*
  • Tauopathies / metabolism
  • Tauopathies / physiopathology
  • tau Proteins / genetics
  • tau Proteins / metabolism*
  • tau Proteins / physiology

Substances

  • tau Proteins