Proteopathic tau primes and activates interleukin-1β via myeloid-cell-specific MyD88- and NLRP3-ASC-inflammasome pathway

Cell Rep. 2021 Sep 21;36(12):109720. doi: 10.1016/j.celrep.2021.109720.

Abstract

Pathological hyperphosphorylation and aggregation of tau (pTau) and neuroinflammation, driven by interleukin-1β (IL-1β), are the major hallmarks of tauopathies. Here, we show that pTau primes and activates IL-1β. First, RNA-sequence analysis suggests paired-helical filaments (PHFs) from human tauopathy brain primes nuclear factor κB (NF-κB), chemokine, and IL-1β signaling clusters in human primary microglia. Treating microglia with pTau-containing neuronal media, exosomes, or PHFs causes IL-1β activation, which is NLRP3, ASC, and caspase-1 dependent. Suppression of pTau or ASC reduces tau pathology and inflammasome activation in rTg4510 and hTau mice, respectively. Although the deletion of MyD88 prevents both IL-1β expression and activation in the hTau mouse model of tauopathy, ASC deficiency in myeloid cells reduces pTau-induced IL-1β activation and improves cognitive function in hTau mice. Finally, pTau burden co-exists with elevated IL-1β and ASC in autopsy brains of human tauopathies. Together, our results suggest pTau activates IL-1β via MyD88- and NLRP3-ASC-dependent pathways in myeloid cells, including microglia.

Keywords: ASC; IL-1β; MAPT; MyD88; NLRP3; inflammasomes; microglia; neuroinflammation; tau; tauopathies.

Publication types

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

MeSH terms

  • Animals
  • CARD Signaling Adaptor Proteins / genetics
  • CARD Signaling Adaptor Proteins / metabolism
  • Caspase 1 / metabolism
  • Cells, Cultured
  • Disease Models, Animal
  • Down-Regulation / drug effects
  • Doxorubicin / pharmacology
  • Humans
  • Inflammasomes / metabolism*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Microglia / cytology
  • Microglia / metabolism
  • Myeloid Cells / cytology
  • Myeloid Cells / metabolism
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / metabolism
  • NF-kappa B / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Signal Transduction*
  • Tauopathies / metabolism
  • Tauopathies / pathology*
  • tau Proteins / genetics
  • tau Proteins / metabolism*

Substances

  • CARD Signaling Adaptor Proteins
  • Inflammasomes
  • Interleukin-1beta
  • Myeloid Differentiation Factor 88
  • NF-kappa B
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • tau Proteins
  • Doxorubicin
  • Caspase 1