Hydrogen sulfide is neuroprotective in Alzheimer's disease by sulfhydrating GSK3β and inhibiting Tau hyperphosphorylation

Proc Natl Acad Sci U S A. 2021 Jan 26;118(4):e2017225118. doi: 10.1073/pnas.2017225118.

Abstract

Alzheimer's disease (AD), the most common cause of dementia and neurodegeneration in the elderly, is characterized by deterioration of memory and executive and motor functions. Neuropathologic hallmarks of AD include neurofibrillary tangles (NFTs), paired helical filaments, and amyloid plaques. Mutations in the microtubule-associated protein Tau, a major component of the NFTs, cause its hyperphosphorylation in AD. We have shown that signaling by the gaseous molecule hydrogen sulfide (H2S) is dysregulated during aging. H2S signals via a posttranslational modification termed sulfhydration/persulfidation, which participates in diverse cellular processes. Here we show that cystathionine γ-lyase (CSE), the biosynthetic enzyme for H2S, binds wild type Tau, which enhances its catalytic activity. By contrast, CSE fails to bind Tau P301L, a mutant that is present in the 3xTg-AD mouse model of AD. We further show that CSE is depleted in 3xTg-AD mice as well as in human AD brains, and that H2S prevents hyperphosphorylation of Tau by sulfhydrating its kinase, glycogen synthase kinase 3β (GSK3β). Finally, we demonstrate that sulfhydration is diminished in AD, while administering the H2S donor sodium GYY4137 (NaGYY) to 3xTg-AD mice ameliorates motor and cognitive deficits in AD.

Keywords: Alzheimer’s disease; GSK3beta; Tau; hydrogen sulfide; sulfhydration.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease / drug therapy*
  • Alzheimer Disease / genetics
  • Alzheimer Disease / metabolism
  • Alzheimer Disease / pathology
  • Animals
  • Cystathionine gamma-Lyase / genetics*
  • Cystathionine gamma-Lyase / metabolism
  • Disease Models, Animal
  • Glycogen Synthase Kinase 3 beta / genetics*
  • Glycogen Synthase Kinase 3 beta / metabolism
  • HEK293 Cells
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Hippocampus / pathology
  • Humans
  • Hydrogen Sulfide / pharmacology*
  • Mice
  • Mice, Transgenic
  • Morpholines / pharmacology*
  • Mutation
  • Neurofibrillary Tangles / drug effects
  • Neurofibrillary Tangles / metabolism
  • Neurofibrillary Tangles / pathology
  • Neuroprotective Agents / pharmacology*
  • Organothiophosphorus Compounds / pharmacology*
  • Phosphorylation
  • Plaque, Amyloid / genetics
  • Plaque, Amyloid / metabolism
  • Plaque, Amyloid / pathology
  • Plaque, Amyloid / prevention & control
  • Protein Binding
  • Protein Processing, Post-Translational
  • Sulfates / metabolism
  • tau Proteins / genetics*
  • tau Proteins / metabolism

Substances

  • GYY 4137
  • MAPT protein, human
  • Mapt protein, mouse
  • Morpholines
  • Neuroprotective Agents
  • Organothiophosphorus Compounds
  • Sulfates
  • tau Proteins
  • Glycogen Synthase Kinase 3 beta
  • Cystathionine gamma-Lyase
  • Hydrogen Sulfide