JAK2/STAT3 signaling mediates IL-6-inhibited neurogenesis of neural stem cells through DNA demethylation/methylation

Brain Behav Immun. 2019 Jul:79:159-173. doi: 10.1016/j.bbi.2019.01.027. Epub 2019 Feb 11.

Abstract

Neuroinflammation, considered as a pathological hallmark of Alzheimer's disease (AD), has been demonstrated to affect hippocampal neurogenesis and cognitive function. Interleukin-6 (IL-6) is a proinflammatory cytokine known to modulate neurogenesis. However, the mechanisms are still largely unknown. Here, we reported that IL-6 suppressed neurogenesis via a JAK2/STAT3 signaling in neural stem cells (NSCs). Importantly, we found that NeuroD1 (Neurogenic differentiation 1) gene expression, which drives NSCs neurodifferentiation, was regulated by TET3 and DNMT1 in a JAK2/STAT3-dependent manner. We further found that JAK2/STAT3 inhibition enhanced demethylation of NeuroD1 regulatory elements in IL-6-treated cells, which is related to the significant upregulation of TET3 expression as well as the decreased expression of DNMT1. Furthermore, Inhibiting JAK2/STAT3 significantly rescued the memory deficits and hippocampal neurogenesis dysfunction in APP/PS1 mice. Our data suggest that JAK2/STAT3 signaling plays a vital role in suppressing neurogenesis of NSCs exposed to IL-6 at the epigenetic level, by regulating DNA methylation/demethylation.

Keywords: Alzheimer disease; DNA demethylation; DNMT1; Interleukin-6; JAK2/STAT3; Neural stem cells; TET3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease / metabolism
  • Alzheimer Disease / physiopathology
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • DNA (Cytosine-5-)-Methyltransferase 1 / genetics
  • DNA (Cytosine-5-)-Methyltransferase 1 / metabolism
  • DNA Demethylation
  • DNA Methylation
  • Dioxygenases / genetics
  • Dioxygenases / metabolism
  • Hippocampus / metabolism
  • Humans
  • Interleukin-6 / metabolism
  • Janus Kinase 2 / metabolism*
  • Male
  • Mice
  • Mice, Transgenic
  • Neural Stem Cells / metabolism
  • Neurogenesis / immunology
  • Neurogenesis / physiology*
  • Neuroimmunomodulation
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction / immunology

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Interleukin-6
  • Neurod1 protein, mouse
  • STAT3 Transcription Factor
  • Dioxygenases
  • Tet3 protein, mouse
  • DNA (Cytosine-5-)-Methyltransferase 1
  • Dnmt1 protein, mouse
  • Jak2 protein, mouse
  • Janus Kinase 2