Flavonoid-Derived Human Phenyl-γ-Valerolactone Metabolites Selectively Detoxify Amyloid-β Oligomers and Prevent Memory Impairment in a Mouse Model of Alzheimer's Disease

Mol Nutr Food Res. 2020 Mar;64(5):e1900890. doi: 10.1002/mnfr.201900890. Epub 2020 Jan 16.

Abstract

Scope: Amyloid-β oligomers (AβO) are causally related to Alzheimer's disease (AD). Dietary natural compounds, especially flavonoids and flavan-3-ols, hold great promise as potential AD-preventive agents but their host and gut microbiota metabolism complicates identification of the most relevant bioactive species. This study aims to investigate the ability of a comprehensive set of phenyl-γ-valerolactones (PVL), the main circulating metabolites of flavan-3-ols and related dietary compounds in humans, to prevent AβO-mediated toxicity.

Methods and results: The anti-AβO activity of PVLs is examined in different cell model systems using a highly toxic β-oligomer-forming polypeptide (β23) as target toxicant. Multiple PVLs, and particularly the monohydroxylated 5-(4'-hydroxyphenyl)-γ-valerolactone metabolite [(4'-OH)-PVL], relieve β-oligomer-induced cytotoxicity in yeast and mammalian cells. As revealed by atomic force microscopy (AFM) and other in vitro assays, (4'-OH)-PVL interferes with AβO (but not fibril) assembly and actively remodels preformed AβOs into nontoxic amorphous aggregates. In keeping with the latter mode of action, treatment of AβOs with (4'-OH)-PVL prior to brain injection strongly reduces memory deterioration as well as neuroinflammation in a mouse model of AβO-induced memory impairment.

Conclusion: PVLs, which have been validated as biomarkers of the dietary intake of flavan-3-ols, lend themselves as novel AβO-selective, candidate AD-preventing compounds.

Keywords: Alzheimer's disease prevention; amyloid oligomer detoxification; flavan 3-ol flavonoids; phenyl-γ-valerolactones; polyphenols.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Disease / etiology
  • Alzheimer Disease / prevention & control
  • Amyloid beta-Peptides / genetics
  • Amyloid beta-Peptides / metabolism*
  • Amyloid beta-Peptides / toxicity
  • Animals
  • Disease Models, Animal
  • Flavonoids / chemistry
  • HEK293 Cells
  • Humans
  • Lactones / metabolism
  • Lactones / pharmacology*
  • Male
  • Memory Disorders / prevention & control*
  • Mice, Inbred C57BL
  • Peptide Fragments / metabolism
  • Yeasts / drug effects

Substances

  • (-)-5-(3',4'-dihydroxyphenyl)-valerolactone
  • Amyloid beta-Peptides
  • Flavonoids
  • Lactones
  • Peptide Fragments
  • amyloid beta-protein (1-42)