D-Methionine Improves Spatial Navigation and Attenuates Oxidative Stress and Amyloid Pathology in a Sex-Specific Manner

D-蛋氨酸以性别特异性方式改善空间导航能力并减轻氧化应激和淀粉样蛋白病理

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Abstract

BACKGROUND: Oxidative stress and maladaptive neuroimmune activation contribute to cognitive decline in Alzheimer's disease (AD) and represent therapeutic targets beyond amyloid-centered approaches. OBJECTIVE: To determine whether oral D-methionine (D-Met), a redox-active amino acid, reduces amyloid pathology and lipid peroxidation and confers disease-modifying benefits in AD mouse models. METHODS: Male and female APP/PS1 and APP(NL-F) mice with advanced AD pathology received oral D-Met or vehicle. Behavioral assessments included locomotor activity and hippocampal-dependent spatial learning and memory. Amyloid burden, lipid peroxidation, peripheral metabolic and inflammatory markers, and hippocampal microglial phenotypes were evaluated using biochemical and histological analyses. RESULTS: D-Met did not alter locomotor or exploratory behavior but improved spatial memory recall in both sexes of APP/PS1 mice and in female APP(NL-F) mice. APP(NL-F) males exhibited improved learning during Morris water maze (MWM) acquisition. Amyloid pathology was modestly and region-specifically reduced, including decreased hippocampal plaque size in male APP(NL-F) mice, reduced cortical plaque size in female APP/PS1 mice, and lower soluble amyloid-β (Aβ)(42) in male APP/PS1 mice. Lipid peroxidation, assessed by malondialdehyde, was reduced only in female APP(NL-F) mice. D-Met induced pronounced sex-dependent peripheral effects, increasing adiposity and pro-inflammatory adipose signaling in males, while reducing perigonadal white adipose tissue (pgWAT) IL-6 expression in female APP(NL-F) mice. In the hippocampus, D-Met remodeled microglial signatures, with female APP(NL-F) mice showing reduced Iba1 and disease-associated microglial (DAM) markers and increased Axl expression. CONCLUSION: Short-term D-Met acts as a metabolic and redox modulator with modest amyloid-lowering effects mediated by improved microglial function. Therapeutic efficacy is strongly sex- and model-dependent, with the greatest benefit observed in female APP(NL-F) mice.

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