miR-302 Attenuates Amyloid-β-Induced Neurotoxicity through Activation of Akt Signaling

J Alzheimers Dis. 2016;50(4):1083-98. doi: 10.3233/JAD-150741.

Abstract

Deficiency of insulin signaling has been linked to diabetes and ageing-related neurodegenerative diseases such as Alzheimer's disease (AD). In this regard, brains exhibit defective insulin receptor substrate-1 (IRS-1) and hence result in alteration of insulin signaling in progression of AD, the most common cause of dementia. Consequently, dysregulation of insulin signaling plays an important role in amyloid-β (Aβ)-induced neurotoxicity. As the derivation of induced pluripotent stem cells (iPSC) involves cell reprogramming, it may provide a means for regaining the control of ageing-associated dysfunction and neurodegeneration via affecting insulin-related signaling. To this, we found that an embryonic stem cell (ESC)-specific microRNA, miR-302, silences phosphatase and tensin homolog (PTEN) to activate Akt signaling, which subsequently stimulates nuclear factor erythroid 2-related factor 2 (Nrf2)/heme oxygenase-1 (HO-1) elevation and hence inhibits Aβ-induced neurotoxicity. miR-302 is predominantly expressed in iPSCs and is known to regulate several important biological processes of anti-oxidative stress, anti-apoptosis, and anti-aging through activating Akt signaling. In addition, we also found that miR-302-mediated Akt signaling further stimulates Nanog expression to suppress Aβ-induced p-Ser307 IRS-1 expression and thus enhances tyrosine phosphorylation and p-Ser 473-Akt/p-Ser 9-GSK3β formation. Furthermore, our in vivo studies revealed that the mRNA expression levels of both Nanog and miR-302-encoding LARP7 genes were significantly reduced in AD patients' blood cells, providing a novel diagnosis marker for AD. Taken together, our findings demonstrated that miR-302 is able to inhibit Aβ-induced cytotoxicity via activating Akt signaling to upregulate Nrf2 and Nanog expressions, leading to a marked restoration of insulin signaling in AD neurons.

Keywords: Alzheimer’s disease; Nanog; amyloid-β; insulin signaling; miR-302; phosphatase and tensin homolog.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Amyloid beta-Peptides / toxicity*
  • Cell Line, Tumor
  • Cell Survival / physiology
  • Female
  • Glycogen Synthase Kinase 3 beta / metabolism
  • Heme Oxygenase-1 / metabolism
  • Humans
  • Insulin / metabolism
  • Male
  • Membrane Potential, Mitochondrial / physiology
  • MicroRNAs / metabolism*
  • NF-E2-Related Factor 2 / metabolism
  • Neurons / metabolism*
  • Oxidative Stress / physiology
  • PTEN Phosphohydrolase / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Reactive Oxygen Species / metabolism
  • Ribonucleoproteins / metabolism

Substances

  • Amyloid beta-Peptides
  • Insulin
  • Larp7 protein, human
  • MIRN302A microRNA, human
  • MicroRNAs
  • NF-E2-Related Factor 2
  • NFE2L2 protein, human
  • Reactive Oxygen Species
  • Ribonucleoproteins
  • HMOX1 protein, human
  • Heme Oxygenase-1
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta
  • Proto-Oncogene Proteins c-akt
  • PTEN Phosphohydrolase
  • PTEN protein, human