Possible Involvement of Hippocampal miR-539-3p/Lrp6/Igf1r Axis for Diminished Working Memory in Mice Fed a Low-Carbohydrate and High-Protein Diet

Mol Nutr Food Res. 2025 Jan;69(2):e202400648. doi: 10.1002/mnfr.202400648. Epub 2024 Dec 20.

Abstract

A low-carbohydrate and high-protein (LC-HP) diet demonstrates favorable impacts on metabolic parameters, albeit it leads to a decline in hippocampal function with the decreased expression of hippocampal insulin-like growth factor-1 receptor (IGF-1R) among healthy mice. However, the precise mechanisms underlying this phenomenon remain unexplored. Eight-week-old male C57BL/6 mice were divided into the LC-HP diet-fed group (25.1% carbohydrate, 57.2% protein, and 17.7% fat as percentages of calories; n = 10) and the control diet-fed group (58.9% carbohydrate, 24.0% protein, and 17.1% fat; n = 10). After 4 weeks, all mice underwent the Y-maze test, followed by analyses of hippocampal mRNA and miRNA expressions. We revealed that feeding the LC-HP diet suppressed working memory function and hippocampal Igf1r mRNA levels in mice. Sequencing of hippocampal miRNA demonstrated 17 upregulated and 27 downregulated miRNAs in the LC-HP diet-fed mice. Notably, we found decreased hippocampal mRNA levels of low-density lipoprotein receptor-related protein 6 (Lrp6), a gene modulated by miR-539-3p, in mice fed the LC-HP diet. Furthermore, a significant positive correlation was observed between Lrp6 and Igf1r mRNA levels in the hippocampus. These findings suggest that LC-HP diets may suppress hippocampal function via the miR-539-3p/Lrp6/Igf1r axis.

Keywords: Igf1r; carbohydrate; hippocampus; miRNA; protein; working memory.

MeSH terms

  • Animals
  • Diet, Carbohydrate-Restricted* / methods
  • Dietary Proteins / administration & dosage
  • Dietary Proteins / pharmacology
  • Hippocampus* / metabolism
  • Low Density Lipoprotein Receptor-Related Protein-6* / genetics
  • Low Density Lipoprotein Receptor-Related Protein-6* / metabolism
  • Male
  • Maze Learning
  • Memory, Short-Term* / physiology
  • Mice
  • Mice, Inbred C57BL*
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Receptor, IGF Type 1* / genetics
  • Receptor, IGF Type 1* / metabolism

Substances

  • MicroRNAs
  • Receptor, IGF Type 1
  • Igf1r protein, mouse
  • Low Density Lipoprotein Receptor-Related Protein-6
  • Dietary Proteins