Linking oxysterols and different stages of mild cognitive impairment: insights from gut metabolites and N6-methyladenosine

Abstract Background Oxysterols, gut metabolites, and N6-methyladenosine (m6A) are extensively implicated in the pathogenesis of cognitive dysfunction, while their alterations in different stages of mild cognitive impairment (MCI) have not been elucidated. Therefore, this study was conducted to explo...

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Main Authors: Wenjing Feng, Mengwei Ju, Tao Wang, Shanshan Cui, Kexin Yang, Zhiting Guo, Miao Liu, Jiaxuan Tao, Huiyan Yu, Rong Xiao
Format: Article
Language:English
Published: BMC 2025-05-01
Series:Alzheimer’s Research & Therapy
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Online Access:https://doi.org/10.1186/s13195-025-01743-5
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author Wenjing Feng
Mengwei Ju
Tao Wang
Shanshan Cui
Kexin Yang
Zhiting Guo
Miao Liu
Jiaxuan Tao
Huiyan Yu
Rong Xiao
author_facet Wenjing Feng
Mengwei Ju
Tao Wang
Shanshan Cui
Kexin Yang
Zhiting Guo
Miao Liu
Jiaxuan Tao
Huiyan Yu
Rong Xiao
author_sort Wenjing Feng
collection DOAJ
description Abstract Background Oxysterols, gut metabolites, and N6-methyladenosine (m6A) are extensively implicated in the pathogenesis of cognitive dysfunction, while their alterations in different stages of mild cognitive impairment (MCI) have not been elucidated. Therefore, this study was conducted to explore the associations of oxysterols, gut metabolites, and m6A methylation profiles in early MCI (EMCI) and late MCI (LMCI) individuals. Methods Liquid chromatography-mass spectrometry, untargeted metabolomic analysis, and m6A mRNA Epitranscriptomic Microarray were used to detect the characteristics of serum oxysterols (n = 35/group), fecal gut metabolites (n = 30/group), and m6A in whole blood (n = 4/group) respectively. The concentration of serum β-amyloid (Aβ) was detected with ELISA (n = 25/group). The gene expression of amyloid precursor protein (APP) and its key enzyme β-secretase (BACE1) in whole blood were measured by quantitative real-time PCR (n = 25/group). Results EMCIs and LMCIs, especially LMCIs, exhibited poorer performance in almost all global and multidimensional cognitive tests. Serum 27-hydroxycholesterol (27-OHC) and 24S-hydroxycholesterol (24S-OHC) were elevated in EMCI and LMCI groups. Changes in gut metabolites occurred mainly in the EMCI group, in which several gut metabolites, including Procyanidin dimer B7 and Phorbol myristate, were significantly decreased. The m6A methylation landscape of EMCIs and LMCIs obviously differed from Controls. Hypomethylated mRNAs accounted for the majority and were mainly accompanied by downregulated mRNAs, which was consistent with the downregulated expression of the m6A writer methyltransferase-like 4 (METTL4). 27-OHC and 24S-OHC combined with various gut metabolites significantly distinguished between MCI subgroups from healthy controls (EMCI/Control: AUC = 0.877; LMCI/Control: AUC = 0.952). Heatmap revealed the correlation between Phorbol myristate and differentially m6A-methylated mRNAs. Differentially expressed gut metabolites and methylated mRNAs were commonly enriched in 34 KEGG metabolic pathways, including cholesterol metabolism and neurodegenerative disease-related pathways. Conclusions Our study explored the altered oxysterols, gut metabolites, and m6A methylation and their associations in different stages of MCI. The potential function of aberrant gut metabolites in oxysterols and m6A methylation driving MCI progression warrants further mechanistic investigation.
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spelling doaj-art-ad3cb51d1a8c402bb44dd38197ae09e82025-08-20T02:31:58ZengBMCAlzheimer’s Research & Therapy1758-91932025-05-0117112410.1186/s13195-025-01743-5Linking oxysterols and different stages of mild cognitive impairment: insights from gut metabolites and N6-methyladenosineWenjing Feng0Mengwei Ju1Tao Wang2Shanshan Cui3Kexin Yang4Zhiting Guo5Miao Liu6Jiaxuan Tao7Huiyan Yu8Rong Xiao9School of Public Health, Capital Medical UniversitySchool of Public Health, Capital Medical UniversitySchool of Public Health, Capital Medical UniversitySchool of Public Health, Capital Medical UniversitySchool of Public Health, Capital Medical UniversitySchool of Public Health, Capital Medical UniversitySchool of Public Health, Capital Medical UniversitySchool of Public Health, Capital Medical UniversitySchool of Public Health, Capital Medical UniversitySchool of Public Health, Capital Medical UniversityAbstract Background Oxysterols, gut metabolites, and N6-methyladenosine (m6A) are extensively implicated in the pathogenesis of cognitive dysfunction, while their alterations in different stages of mild cognitive impairment (MCI) have not been elucidated. Therefore, this study was conducted to explore the associations of oxysterols, gut metabolites, and m6A methylation profiles in early MCI (EMCI) and late MCI (LMCI) individuals. Methods Liquid chromatography-mass spectrometry, untargeted metabolomic analysis, and m6A mRNA Epitranscriptomic Microarray were used to detect the characteristics of serum oxysterols (n = 35/group), fecal gut metabolites (n = 30/group), and m6A in whole blood (n = 4/group) respectively. The concentration of serum β-amyloid (Aβ) was detected with ELISA (n = 25/group). The gene expression of amyloid precursor protein (APP) and its key enzyme β-secretase (BACE1) in whole blood were measured by quantitative real-time PCR (n = 25/group). Results EMCIs and LMCIs, especially LMCIs, exhibited poorer performance in almost all global and multidimensional cognitive tests. Serum 27-hydroxycholesterol (27-OHC) and 24S-hydroxycholesterol (24S-OHC) were elevated in EMCI and LMCI groups. Changes in gut metabolites occurred mainly in the EMCI group, in which several gut metabolites, including Procyanidin dimer B7 and Phorbol myristate, were significantly decreased. The m6A methylation landscape of EMCIs and LMCIs obviously differed from Controls. Hypomethylated mRNAs accounted for the majority and were mainly accompanied by downregulated mRNAs, which was consistent with the downregulated expression of the m6A writer methyltransferase-like 4 (METTL4). 27-OHC and 24S-OHC combined with various gut metabolites significantly distinguished between MCI subgroups from healthy controls (EMCI/Control: AUC = 0.877; LMCI/Control: AUC = 0.952). Heatmap revealed the correlation between Phorbol myristate and differentially m6A-methylated mRNAs. Differentially expressed gut metabolites and methylated mRNAs were commonly enriched in 34 KEGG metabolic pathways, including cholesterol metabolism and neurodegenerative disease-related pathways. Conclusions Our study explored the altered oxysterols, gut metabolites, and m6A methylation and their associations in different stages of MCI. The potential function of aberrant gut metabolites in oxysterols and m6A methylation driving MCI progression warrants further mechanistic investigation.https://doi.org/10.1186/s13195-025-01743-5Mild cognitive impairmentOxysterolsGut metabolitesN6-methyladenosineCognitive assessment
spellingShingle Wenjing Feng
Mengwei Ju
Tao Wang
Shanshan Cui
Kexin Yang
Zhiting Guo
Miao Liu
Jiaxuan Tao
Huiyan Yu
Rong Xiao
Linking oxysterols and different stages of mild cognitive impairment: insights from gut metabolites and N6-methyladenosine
Alzheimer’s Research & Therapy
Mild cognitive impairment
Oxysterols
Gut metabolites
N6-methyladenosine
Cognitive assessment
title Linking oxysterols and different stages of mild cognitive impairment: insights from gut metabolites and N6-methyladenosine
title_full Linking oxysterols and different stages of mild cognitive impairment: insights from gut metabolites and N6-methyladenosine
title_fullStr Linking oxysterols and different stages of mild cognitive impairment: insights from gut metabolites and N6-methyladenosine
title_full_unstemmed Linking oxysterols and different stages of mild cognitive impairment: insights from gut metabolites and N6-methyladenosine
title_short Linking oxysterols and different stages of mild cognitive impairment: insights from gut metabolites and N6-methyladenosine
title_sort linking oxysterols and different stages of mild cognitive impairment insights from gut metabolites and n6 methyladenosine
topic Mild cognitive impairment
Oxysterols
Gut metabolites
N6-methyladenosine
Cognitive assessment
url https://doi.org/10.1186/s13195-025-01743-5
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