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Circulating exosomal microRNA profiles in migraine patients receiving acupuncture treatment: A placebo-controlled clinical trial

BACKGROUND: Acupuncture has a long history of being used in Chinese medicine for the treatment of migraine. However, molecular biomarkers for diagnosis and prognosis of migraine and its treatment are lacking. This study aimed to explore whether acupuncture could regulate differentially expressed exo...

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Autores principales: Liu, Lu, Qi, Wenchuan, Wang, Yanan, Ni, Xixiu, Gao, Shan, Zhou, Ziyang, Chen, Daohong, He, Zhenxi, Sun, Mingsheng, Wang, Ziwen, Cai, Dingjun, Zhao, Ling
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9871901/
https://www.ncbi.nlm.nih.gov/pubmed/36704329
http://dx.doi.org/10.3389/fnmol.2022.1098766
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author Liu, Lu
Qi, Wenchuan
Wang, Yanan
Ni, Xixiu
Gao, Shan
Zhou, Ziyang
Chen, Daohong
He, Zhenxi
Sun, Mingsheng
Wang, Ziwen
Cai, Dingjun
Zhao, Ling
author_facet Liu, Lu
Qi, Wenchuan
Wang, Yanan
Ni, Xixiu
Gao, Shan
Zhou, Ziyang
Chen, Daohong
He, Zhenxi
Sun, Mingsheng
Wang, Ziwen
Cai, Dingjun
Zhao, Ling
author_sort Liu, Lu
collection PubMed
description BACKGROUND: Acupuncture has a long history of being used in Chinese medicine for the treatment of migraine. However, molecular biomarkers for diagnosis and prognosis of migraine and its treatment are lacking. This study aimed to explore whether acupuncture could regulate differentially expressed exosomal miRNAs between patients with migraine without aura (MWoA) and healthy controls (HCs) and to identify diagnostic biomarkers that helped differentiate MWoA patients from HCs and identify prognostic biomarkers that helped to predict the effect of acupuncture. METHODS: Here, we isolated serum exosomes from patients with MWoA and HCs before and after true and sham acupuncture treatment. Then, small RNA sequencing and bioinformatics analysis were performed to screen out key miRNAs specifically responding to acupuncture treatment. Pearson’s correlation analysis was used to evaluate the correlation between miRNAs and clinical phenotypes. Finally, we applied a machine learning method to identify diagnostic biomarkers of MWoA patients and identify prognostic biomarkers that helped to predict the effect of acupuncture. RESULTS: Small RNA sequencing identified 68 upregulated and 104 downregulated miRNAs in MWoA patients compared to those in HCs. Further, we identified eight upregulated and four downregulated miRNAs in migraine patients after true acupuncture treatment (trAMWoA), but not in the sham acupuncture treatment (shAMWoA) or HC group. Among them, hsa-miR-378a-5p was positively correlated with time unable to work, study, or do housework due to migraine (p < 0.05), whereas hsa-miR-605-3p was negatively correlated with the restrictive subscale of the migraine-specific quality of life questionnaire (MSQ) (p < 0.05). We then evaluated the diagnostic and prognostic potential of these 12 miRNAs in patients with MWoA. The combination of serum levels of exosomal hsa-miR-369-5p, hsa-miR-145-5p, and hsa-miR-5,010-3p could serve as diagnostic and prognostic biomarkers for MWoA patients following acupuncture treatment. CONCLUSION: This is the first study on the serum exosomal miRNA profiles of migraineurs before and after acupuncture treatment. Our results improve our understanding of the molecular functions of miRNAs in MWoA. More importantly, they expand our view of evaluating the clinical outcomes of migraine patients treated with acupuncture, using exosomal RNA markers. CLINICAL TRIAL REGISTRATION: Chinese Clinical Trial Registry, ChiCTR2000034417, July 2020.
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spelling pubmed-98719012023-01-25 Circulating exosomal microRNA profiles in migraine patients receiving acupuncture treatment: A placebo-controlled clinical trial Liu, Lu Qi, Wenchuan Wang, Yanan Ni, Xixiu Gao, Shan Zhou, Ziyang Chen, Daohong He, Zhenxi Sun, Mingsheng Wang, Ziwen Cai, Dingjun Zhao, Ling Front Mol Neurosci Molecular Neuroscience BACKGROUND: Acupuncture has a long history of being used in Chinese medicine for the treatment of migraine. However, molecular biomarkers for diagnosis and prognosis of migraine and its treatment are lacking. This study aimed to explore whether acupuncture could regulate differentially expressed exosomal miRNAs between patients with migraine without aura (MWoA) and healthy controls (HCs) and to identify diagnostic biomarkers that helped differentiate MWoA patients from HCs and identify prognostic biomarkers that helped to predict the effect of acupuncture. METHODS: Here, we isolated serum exosomes from patients with MWoA and HCs before and after true and sham acupuncture treatment. Then, small RNA sequencing and bioinformatics analysis were performed to screen out key miRNAs specifically responding to acupuncture treatment. Pearson’s correlation analysis was used to evaluate the correlation between miRNAs and clinical phenotypes. Finally, we applied a machine learning method to identify diagnostic biomarkers of MWoA patients and identify prognostic biomarkers that helped to predict the effect of acupuncture. RESULTS: Small RNA sequencing identified 68 upregulated and 104 downregulated miRNAs in MWoA patients compared to those in HCs. Further, we identified eight upregulated and four downregulated miRNAs in migraine patients after true acupuncture treatment (trAMWoA), but not in the sham acupuncture treatment (shAMWoA) or HC group. Among them, hsa-miR-378a-5p was positively correlated with time unable to work, study, or do housework due to migraine (p < 0.05), whereas hsa-miR-605-3p was negatively correlated with the restrictive subscale of the migraine-specific quality of life questionnaire (MSQ) (p < 0.05). We then evaluated the diagnostic and prognostic potential of these 12 miRNAs in patients with MWoA. The combination of serum levels of exosomal hsa-miR-369-5p, hsa-miR-145-5p, and hsa-miR-5,010-3p could serve as diagnostic and prognostic biomarkers for MWoA patients following acupuncture treatment. CONCLUSION: This is the first study on the serum exosomal miRNA profiles of migraineurs before and after acupuncture treatment. Our results improve our understanding of the molecular functions of miRNAs in MWoA. More importantly, they expand our view of evaluating the clinical outcomes of migraine patients treated with acupuncture, using exosomal RNA markers. CLINICAL TRIAL REGISTRATION: Chinese Clinical Trial Registry, ChiCTR2000034417, July 2020. Frontiers Media S.A. 2023-01-10 /pmc/articles/PMC9871901/ /pubmed/36704329 http://dx.doi.org/10.3389/fnmol.2022.1098766 Text en Copyright © 2023 Liu, Qi, Wang, Ni, Gao, Zhou, Chen, He, Sun, Wang, Cai and Zhao. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Molecular Neuroscience
Liu, Lu
Qi, Wenchuan
Wang, Yanan
Ni, Xixiu
Gao, Shan
Zhou, Ziyang
Chen, Daohong
He, Zhenxi
Sun, Mingsheng
Wang, Ziwen
Cai, Dingjun
Zhao, Ling
Circulating exosomal microRNA profiles in migraine patients receiving acupuncture treatment: A placebo-controlled clinical trial
title Circulating exosomal microRNA profiles in migraine patients receiving acupuncture treatment: A placebo-controlled clinical trial
title_full Circulating exosomal microRNA profiles in migraine patients receiving acupuncture treatment: A placebo-controlled clinical trial
title_fullStr Circulating exosomal microRNA profiles in migraine patients receiving acupuncture treatment: A placebo-controlled clinical trial
title_full_unstemmed Circulating exosomal microRNA profiles in migraine patients receiving acupuncture treatment: A placebo-controlled clinical trial
title_short Circulating exosomal microRNA profiles in migraine patients receiving acupuncture treatment: A placebo-controlled clinical trial
title_sort circulating exosomal microrna profiles in migraine patients receiving acupuncture treatment: a placebo-controlled clinical trial
topic Molecular Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9871901/
https://www.ncbi.nlm.nih.gov/pubmed/36704329
http://dx.doi.org/10.3389/fnmol.2022.1098766
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