MicroRNA-125b induces tau hyperphosphorylation and cognitive deficits in Alzheimer's disease

EMBO J. 2014 Aug 1;33(15):1667-80. doi: 10.15252/embj.201387576. Epub 2014 Jul 7.

Abstract

Sporadic Alzheimer's disease (AD) is the most prevalent form of dementia, but no clear disease-initiating mechanism is known. Aβ deposits and neuronal tangles composed of hyperphosphorylated tau are characteristic for AD. Here, we analyze the contribution of microRNA-125b (miR-125b), which is elevated in AD. In primary neurons, overexpression of miR-125b causes tau hyperphosphorylation and an upregulation of p35, cdk5, and p44/42-MAPK signaling. In parallel, the phosphatases DUSP6 and PPP1CA and the anti-apoptotic factor Bcl-W are downregulated as direct targets of miR-125b. Knockdown of these phosphatases induces tau hyperphosphorylation, and overexpression of PPP1CA and Bcl-W prevents miR-125b-induced tau phosphorylation, suggesting that they mediate the effects of miR-125b on tau. Conversely, suppression of miR-125b in neurons by tough decoys reduces tau phosphorylation and kinase expression/activity. Injecting miR-125b into the hippocampus of mice impairs associative learning and is accompanied by downregulation of Bcl-W, DUSP6, and PPP1CA, resulting in increased tau phosphorylation in vivo. Importantly, DUSP6 and PPP1CA are also reduced in AD brains. These data implicate miR-125b in the pathogenesis of AD by promoting pathological tau phosphorylation.

Keywords: Alzheimer's disease; kinases; microRNA‐125b; phosphatases; tau phosphorylation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease / genetics
  • Alzheimer Disease / metabolism*
  • Animals
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism
  • Cells, Cultured
  • Cognition Disorders / genetics
  • Down-Regulation
  • Dual Specificity Phosphatase 6 / genetics
  • Dual Specificity Phosphatase 6 / metabolism
  • Gene Knockout Techniques
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Humans
  • Memory / physiology
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • MicroRNAs / pharmacology
  • Neurons / metabolism
  • Phosphorylation
  • Protein Phosphatase 1 / genetics
  • Protein Phosphatase 1 / metabolism
  • tau Proteins / metabolism*

Substances

  • Apoptosis Regulatory Proteins
  • BCL2L2 protein, human
  • MAPT protein, human
  • MIRN125 microRNA, human
  • MicroRNAs
  • tau Proteins
  • PPP1CA protein, human
  • Protein Phosphatase 1
  • DUSP6 protein, human
  • Dual Specificity Phosphatase 6