Lowering Hippocampal miR-29a Expression Slows Cognitive Decline and Reduces Beta-Amyloid Deposition in 5×FAD Mice

Mol Neurobiol. 2024 Jun;61(6):3343-3356. doi: 10.1007/s12035-023-03791-0. Epub 2023 Nov 22.

Abstract

microRNA-29a (miR-29a) increases with age in humans and mice, and, in the brain, it has a role in neuronal maturation and response to inflammation. We previously found higher miR-29a levels in the human brain to be associated with faster antemortem cognitive decline, suggesting that lowering miR-29a levels could ameliorate memory impairment in the 5×FAD AD mouse model. To test this, we generated an adeno-associated virus (AAV) expressing GFP and a miR-29a "sponge" or empty vector. We found that the AAV expressing miR-29a sponge functionally reduced miR-29a levels and improved measures of memory in the Morris water maze and fear condition paradigms when delivered to the hippocampi of 5×FAD and WT mice. miR-29a sponge significantly reduced hippocampal beta-amyloid deposition in 5×FAD mice and lowered astrocyte and microglia activation in both 5×FAD and WT mice. Using transcriptomic and proteomic sequencing, we identified Plxna1 and Wdfy1 as putative effectors at the transcript and protein level in WT and 5×FAD mice, respectively. These data indicate that lower miR-29a levels mitigate cognitive decline, making miR-29a and its target genes worth further evaluation as targets to mitigate Alzheimer's disease (AD).

Keywords: Beta-amyloid; Cognition; Neuroinflammation; Wdfy1; miR-29a.

MeSH terms

  • Alzheimer Disease / genetics
  • Alzheimer Disease / metabolism
  • Alzheimer Disease / pathology
  • Amyloid beta-Peptides* / metabolism
  • Animals
  • Astrocytes / metabolism
  • Cognitive Dysfunction* / genetics
  • Cognitive Dysfunction* / metabolism
  • Dependovirus / genetics
  • Disease Models, Animal
  • Hippocampus* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism

Substances

  • Amyloid beta-Peptides
  • MicroRNAs
  • MIRN29 microRNA, mouse