OGA Inhibition Alters Energetics and Nutrient Sensing in Alzheimer's Disease Cytoplasmic Hybrids

J Alzheimers Dis. 2020;78(4):1743-1753. doi: 10.3233/JAD-200996.

Abstract

Background: Alzheimer's disease (AD) features reductions in key bioenergetic fluxes and perturbed mitochondrial function. Cytoplasmic hybrids (cybrids) generated through the transfer of AD subject mitochondria to mtDNA-depleted SH-SY5Y neuroblastoma cells recapitulate some of these features in an in vitro setting.

Objective: For this study, we used the AD cybrid model to assess the impact of a nutrient-excess like-state via increasing O-GlcNAcylation on whole cell and mitochondrial homeostasis.

Methods: We induced increased O-GlcNAc by treating AD and control cybrid cell lines with Thiamet G (TMG), an inhibitor of the O-GlcNAcase enzyme that mediates removal of the nutrient-dependent O-GlcNAc modification.

Results: Relative to control cybrid cell lines, AD cybrid lines showed a blunted response to TMG-induced O-GlcNAcylation. At baseline, AD cybrid cell line mitochondria showed partial activation of several proteins that help maintain bioenergetic homeostasis such as AMP-Regulated Kinase suggesting that AD mitochondria initiate a state of nutrient stress promoting energetic compensation; however, this compensation reduces the capacity of cells to respond to additional nutrient-related stresses such as TMG treatment. Also, TMG caused disruptions in acetylation and Sirtuin 3 expression, while lowing total energetic output of the cell.

Conclusion: Together, these findings suggest that modulation of O-GlcNAc is essential for proper energetic function of the mitochondria, and AD mitochondrial capacity to handle nutrient-excess is limited.

Keywords: Acetylation; O-GlcNAc; O-GlcNAc transferase (OGT); O-GlcNAcase (OGA); SIRT3; cybrids; mitochondria; oxidative phosphorylation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acetylation
  • Acetylglucosamine / metabolism*
  • Aged
  • Aged, 80 and over
  • Alzheimer Disease / metabolism*
  • Cell Line, Tumor
  • Cell Respiration
  • Energy Metabolism / drug effects
  • Energy Metabolism / physiology*
  • Enzyme Inhibitors / pharmacology
  • Female
  • Glycolysis
  • Humans
  • Hybrid Cells
  • In Vitro Techniques
  • Male
  • Mitochondria / drug effects
  • Mitochondria / metabolism*
  • Mitochondria / transplantation
  • Neurons / drug effects
  • Neurons / metabolism*
  • Pyrans / pharmacology
  • Sirtuin 3 / drug effects
  • Sirtuin 3 / metabolism
  • Stress, Physiological / drug effects
  • Stress, Physiological / physiology
  • Thiazoles / pharmacology
  • beta-N-Acetylhexosaminidases / antagonists & inhibitors

Substances

  • Enzyme Inhibitors
  • Pyrans
  • Thiazoles
  • thiamet G
  • hexosaminidase C
  • beta-N-Acetylhexosaminidases
  • Sirtuin 3
  • Acetylglucosamine