Astrocytic CCAAT/Enhancer Binding Protein δ Regulates Neuronal Viability and Spatial Learning Ability via miR-135a

Mol Neurobiol. 2016 Aug;53(6):4173-4188. doi: 10.1007/s12035-015-9359-z. Epub 2015 Jul 26.

Abstract

The progression of Alzheimer's disease (AD) has been associated with astrocytes-induced neuroinflammation. However, the detailed mechanism of astrocytes associated with learning impairments and neuronal loss in AD is poorly defined. Here, we provide novel evidences that astrocytic miR-135a is critical for neuronal viability and spatial learning ability in vivo. The AppTg/Cebpd (-/-) mice showed a spatial learning improvement compared with the APPswe/PS1/E9 bigenic (AppTg) mice. miR-135a was found to be a CCAAT/enhancer binding protein δ (CEBPD) responsive miRNA and can repress the transcription of thrombospondin 1 (THBS1) / Thbs1 (mouse) via its 3'-untranslated region (3'UTR). We used different experimental approaches to attenuate the expression of CEBPD/Cebpd (mouse) or miR-135a in astrocytes and found the following results: increase in THBS1/Thbs1 expression, decrease in neuronal apoptosis, and increase in growth of neurites. Importantly, injection of miR-135a antagonist (AM135a) into the brain of AppTg mice was found to prevent neuronal apoptosis and improved the spatial learning ability. Together, our findings demonstrate a critical function for the astrocytic CEBPD, and point to miR-135a antagonist as an attractive therapeutic target for the treatment of Alzheimer's disease.

Keywords: Neuroinflammation; Neuronal viability; Neuroprotective factor; Spatial learning ability; miR-135a.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3' Untranslated Regions / genetics
  • Animals
  • Antagomirs / pharmacology
  • Apoptosis / drug effects
  • Astrocytes / cytology*
  • Astrocytes / drug effects
  • Astrocytes / metabolism*
  • CCAAT-Enhancer-Binding Protein-delta / metabolism*
  • Cell Line, Tumor
  • Cell Survival
  • Humans
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Neuronal Outgrowth / drug effects
  • Neurons / cytology*
  • Neurons / metabolism*
  • Spatial Learning* / drug effects
  • Transcription, Genetic / drug effects

Substances

  • 3' Untranslated Regions
  • Antagomirs
  • MIRN135 microRNA, human
  • MicroRNAs
  • Mirn135 microRNA, mouse
  • CCAAT-Enhancer-Binding Protein-delta