Homocysteine Promotes the Pathogenesis of Atherosclerosis through the Circ‐PIAS1‐5/miR‐219a‐2‐3p/TEAD1 Axis

Abstract Previous studies have established a possible link between hyperhomocysteinemia (HHcy) and dyslipidemia. Circular RNAs (circRNAs) play important regulatory roles in the development of atherosclerosis. However, the biological functions and potential molecular mechanisms of circRNAs in HHcy‐in...

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Main Authors: Shengchao Ma, Fei Ma, Ning Ding, Lin Xie, Anning Yang, Jiangyong Shen, Yun jiao, Kai Wu, YueE Chai, Zhigang Bai, Jiantuan Xiong, Nan Li, Huiping Zhang, Yideng Jiang
Format: Article
Language:English
Published: Wiley 2025-05-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202415563
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author Shengchao Ma
Fei Ma
Ning Ding
Lin Xie
Anning Yang
Jiangyong Shen
Yun jiao
Kai Wu
YueE Chai
Zhigang Bai
Jiantuan Xiong
Nan Li
Huiping Zhang
Yideng Jiang
author_facet Shengchao Ma
Fei Ma
Ning Ding
Lin Xie
Anning Yang
Jiangyong Shen
Yun jiao
Kai Wu
YueE Chai
Zhigang Bai
Jiantuan Xiong
Nan Li
Huiping Zhang
Yideng Jiang
author_sort Shengchao Ma
collection DOAJ
description Abstract Previous studies have established a possible link between hyperhomocysteinemia (HHcy) and dyslipidemia. Circular RNAs (circRNAs) play important regulatory roles in the development of atherosclerosis. However, the biological functions and potential molecular mechanisms of circRNAs in HHcy‐induced lipid accumulation leading to atherosclerosis are still unclear. In this study, it is determined that homocysteine (Hcy) downregulates the expression of circ‐PIAS1‐5 by global circRNA expression profiling and that circ‐PIAS1‐5 inhibits Hcy‐mediated lipid accumulation in foam cells and the pathogenesis of atherosclerosis by acting as a sponge for miR‐219a‐2‐3p. Circ‐PIAS1‐5 is identified as a potential diagnostic biomarker of HHcy‐associated atherosclerosis in male “apolipoprotein E knockout (ApoE−/−)” mice. Mechanistically, circ‐PIAS1‐5 activates the adenosine 5‘‐monophosphate (AMP)‐activated protein kinase pathway by regulating TEAD1 through miR‐219a‐2‐3p, and Hcy mediates the m6A modification and nuclear export of circ‐PIAS1‐5 via YTHDC1 to increase lipid accumulation in foam cells and accelerate the pathogenesis of atherosclerosis. Taken together, these results highlight the role of circ‐PIAS1‐5 in the Hcy‐mediated pathogenesis of atherosclerosis and suggest its potential application as a prognostic biomarker of atherosclerosis induced by HHcy.
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issn 2198-3844
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publishDate 2025-05-01
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spelling doaj-art-301676eab1ae4baf9943983f9b046bde2025-08-20T03:11:14ZengWileyAdvanced Science2198-38442025-05-011218n/an/a10.1002/advs.202415563Homocysteine Promotes the Pathogenesis of Atherosclerosis through the Circ‐PIAS1‐5/miR‐219a‐2‐3p/TEAD1 AxisShengchao Ma0Fei Ma1Ning Ding2Lin Xie3Anning Yang4Jiangyong Shen5Yun jiao6Kai Wu7YueE Chai8Zhigang Bai9Jiantuan Xiong10Nan Li11Huiping Zhang12Yideng Jiang13NHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaNHC Key Laboratory of Metabolic Cardiovascular Diseases Research Ningxia Medical University Yinchuan 750004 ChinaAbstract Previous studies have established a possible link between hyperhomocysteinemia (HHcy) and dyslipidemia. Circular RNAs (circRNAs) play important regulatory roles in the development of atherosclerosis. However, the biological functions and potential molecular mechanisms of circRNAs in HHcy‐induced lipid accumulation leading to atherosclerosis are still unclear. In this study, it is determined that homocysteine (Hcy) downregulates the expression of circ‐PIAS1‐5 by global circRNA expression profiling and that circ‐PIAS1‐5 inhibits Hcy‐mediated lipid accumulation in foam cells and the pathogenesis of atherosclerosis by acting as a sponge for miR‐219a‐2‐3p. Circ‐PIAS1‐5 is identified as a potential diagnostic biomarker of HHcy‐associated atherosclerosis in male “apolipoprotein E knockout (ApoE−/−)” mice. Mechanistically, circ‐PIAS1‐5 activates the adenosine 5‘‐monophosphate (AMP)‐activated protein kinase pathway by regulating TEAD1 through miR‐219a‐2‐3p, and Hcy mediates the m6A modification and nuclear export of circ‐PIAS1‐5 via YTHDC1 to increase lipid accumulation in foam cells and accelerate the pathogenesis of atherosclerosis. Taken together, these results highlight the role of circ‐PIAS1‐5 in the Hcy‐mediated pathogenesis of atherosclerosis and suggest its potential application as a prognostic biomarker of atherosclerosis induced by HHcy.https://doi.org/10.1002/advs.202415563atherosclerosiscirc‐PIAS1‐5homocysteinemiR‐219a‐2‐3pYTHDC1
spellingShingle Shengchao Ma
Fei Ma
Ning Ding
Lin Xie
Anning Yang
Jiangyong Shen
Yun jiao
Kai Wu
YueE Chai
Zhigang Bai
Jiantuan Xiong
Nan Li
Huiping Zhang
Yideng Jiang
Homocysteine Promotes the Pathogenesis of Atherosclerosis through the Circ‐PIAS1‐5/miR‐219a‐2‐3p/TEAD1 Axis
Advanced Science
atherosclerosis
circ‐PIAS1‐5
homocysteine
miR‐219a‐2‐3p
YTHDC1
title Homocysteine Promotes the Pathogenesis of Atherosclerosis through the Circ‐PIAS1‐5/miR‐219a‐2‐3p/TEAD1 Axis
title_full Homocysteine Promotes the Pathogenesis of Atherosclerosis through the Circ‐PIAS1‐5/miR‐219a‐2‐3p/TEAD1 Axis
title_fullStr Homocysteine Promotes the Pathogenesis of Atherosclerosis through the Circ‐PIAS1‐5/miR‐219a‐2‐3p/TEAD1 Axis
title_full_unstemmed Homocysteine Promotes the Pathogenesis of Atherosclerosis through the Circ‐PIAS1‐5/miR‐219a‐2‐3p/TEAD1 Axis
title_short Homocysteine Promotes the Pathogenesis of Atherosclerosis through the Circ‐PIAS1‐5/miR‐219a‐2‐3p/TEAD1 Axis
title_sort homocysteine promotes the pathogenesis of atherosclerosis through the circ pias1 5 mir 219a 2 3p tead1 axis
topic atherosclerosis
circ‐PIAS1‐5
homocysteine
miR‐219a‐2‐3p
YTHDC1
url https://doi.org/10.1002/advs.202415563
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