Silencing of PCK1 mitigates the proliferation and migration of vascular smooth muscle cells and vascular intimal hyperplasia by suppressing STAT3/DRP1-mediated mitochondrial fission

The pathological proliferation and migration of vascular smooth muscle cells (VSMCs) are key processes during vascular neointimal hyperplasia (NIH) and restenosis. Phosphoenolpyruvate carboxy kinase 1 (PCK1) is closely related to a variety of malignant proliferative diseases. However, the role of PC...

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Main Authors: Zhang Li, Chen Yingmei, Pan Quanrong, Fang Shizheng, Zhang Zhongjian, Wang Jia, Yang Yongjian, Yang Dachun, Sun Xiongshan
Format: Article
Language:English
Published: China Science Publishing & Media Ltd. 2024-09-01
Series:Acta Biochimica et Biophysica Sinica
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Online Access:https://www.sciengine.com/doi/10.3724/abbs.2024154
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author Zhang Li
Chen Yingmei
Pan Quanrong
Fang Shizheng
Zhang Zhongjian
Wang Jia
Yang Yongjian
Yang Dachun
Sun Xiongshan
author_facet Zhang Li
Chen Yingmei
Pan Quanrong
Fang Shizheng
Zhang Zhongjian
Wang Jia
Yang Yongjian
Yang Dachun
Sun Xiongshan
author_sort Zhang Li
collection DOAJ
description The pathological proliferation and migration of vascular smooth muscle cells (VSMCs) are key processes during vascular neointimal hyperplasia (NIH) and restenosis. Phosphoenolpyruvate carboxy kinase 1 (PCK1) is closely related to a variety of malignant proliferative diseases. However, the role of PCK1 in VSMCs has rarely been investigated. This study aims to examine the role of PCK1 in the proliferation and migration of VSMCs and vascular NIH after injury. In vivo, extensive NIH and increased expression of PCK1 within the neointima are observed in injured arteries. Interestingly, the administration of adeno-associated virus-9 (AAV-9) carrying Pck1 short hairpin RNA (shPck1) significantly attenuates NIH and stenosis of the vascular lumen. In vitro, Pck1 small interfering RNA (siPck1)-induced PCK1 silencing inhibits VSMC proliferation and migration. Additionally, silencing of PCK1 leads to reduced expression of dynamin-related protein 1 (DRP1) and attenuated mitochondrial fission. Lentivirus-mediated DRP1 overexpression markedly reverses the inhibitory effects of PCK1 silencing on VSMC proliferation, migration, and mitochondrial fission. Finally, PCK1 inhibition attenuates the phosphorylation of signal transducer and activator of transcription 3 (STAT3). Activation of STAT3 abolishes the suppressive effects of PCK1 silencing on DRP1 expression, mitochondrial fission, proliferation, and migration in VSMCs. In conclusion, PCK1 inhibition attenuates the mitochondrial fission, proliferation, and migration of VSMCs by inhibiting the STAT3/DRP1 axis, thereby suppressing vascular NIH and restenosis.
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publisher China Science Publishing & Media Ltd.
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series Acta Biochimica et Biophysica Sinica
spelling doaj-art-911a319d9ea745d7a2c92a9563ab6cf72025-08-20T02:26:59ZengChina Science Publishing & Media Ltd.Acta Biochimica et Biophysica Sinica1672-91452024-09-015763364510.3724/abbs.202415420d259ccSilencing of PCK1 mitigates the proliferation and migration of vascular smooth muscle cells and vascular intimal hyperplasia by suppressing STAT3/DRP1-mediated mitochondrial fissionZhang Li0Chen Yingmei1Pan Quanrong2Fang Shizheng3Zhang Zhongjian4Wang Jia5Yang Yongjian6Yang Dachun7Sun Xiongshan8["Department of Cardiology, the General Hospital of Western Theater Command, Chengdu 610083, China"]["Department of Cardiology, the General Hospital of Western Theater Command, Chengdu 610083, China"]["Department of General Practice, the General Hospital of Western Theater Command, Chengdu 610083, China"]["Department of Critical Care Medicine, the General Hospital of Western Theater Command, Chengdu 610083, China"]["Department of Cardiology, the General Hospital of Western Theater Command, Chengdu 610083, China"]["Department of Cardiology, the General Hospital of Western Theater Command, Chengdu 610083, China"]["Department of Cardiology, the General Hospital of Western Theater Command, Chengdu 610083, China"]["Department of Cardiology, the General Hospital of Western Theater Command, Chengdu 610083, China"]["Department of Cardiology, the General Hospital of Western Theater Command, Chengdu 610083, China"]The pathological proliferation and migration of vascular smooth muscle cells (VSMCs) are key processes during vascular neointimal hyperplasia (NIH) and restenosis. Phosphoenolpyruvate carboxy kinase 1 (PCK1) is closely related to a variety of malignant proliferative diseases. However, the role of PCK1 in VSMCs has rarely been investigated. This study aims to examine the role of PCK1 in the proliferation and migration of VSMCs and vascular NIH after injury. In vivo, extensive NIH and increased expression of PCK1 within the neointima are observed in injured arteries. Interestingly, the administration of adeno-associated virus-9 (AAV-9) carrying Pck1 short hairpin RNA (shPck1) significantly attenuates NIH and stenosis of the vascular lumen. In vitro, Pck1 small interfering RNA (siPck1)-induced PCK1 silencing inhibits VSMC proliferation and migration. Additionally, silencing of PCK1 leads to reduced expression of dynamin-related protein 1 (DRP1) and attenuated mitochondrial fission. Lentivirus-mediated DRP1 overexpression markedly reverses the inhibitory effects of PCK1 silencing on VSMC proliferation, migration, and mitochondrial fission. Finally, PCK1 inhibition attenuates the phosphorylation of signal transducer and activator of transcription 3 (STAT3). Activation of STAT3 abolishes the suppressive effects of PCK1 silencing on DRP1 expression, mitochondrial fission, proliferation, and migration in VSMCs. In conclusion, PCK1 inhibition attenuates the mitochondrial fission, proliferation, and migration of VSMCs by inhibiting the STAT3/DRP1 axis, thereby suppressing vascular NIH and restenosis.https://www.sciengine.com/doi/10.3724/abbs.2024154phosphoenolpyruvate carboxyl kinase 1vascular smooth muscle cellsmitochondrial fissionneointimal hyperplasiadynamin-related protein 1
spellingShingle Zhang Li
Chen Yingmei
Pan Quanrong
Fang Shizheng
Zhang Zhongjian
Wang Jia
Yang Yongjian
Yang Dachun
Sun Xiongshan
Silencing of PCK1 mitigates the proliferation and migration of vascular smooth muscle cells and vascular intimal hyperplasia by suppressing STAT3/DRP1-mediated mitochondrial fission
Acta Biochimica et Biophysica Sinica
phosphoenolpyruvate carboxyl kinase 1
vascular smooth muscle cells
mitochondrial fission
neointimal hyperplasia
dynamin-related protein 1
title Silencing of PCK1 mitigates the proliferation and migration of vascular smooth muscle cells and vascular intimal hyperplasia by suppressing STAT3/DRP1-mediated mitochondrial fission
title_full Silencing of PCK1 mitigates the proliferation and migration of vascular smooth muscle cells and vascular intimal hyperplasia by suppressing STAT3/DRP1-mediated mitochondrial fission
title_fullStr Silencing of PCK1 mitigates the proliferation and migration of vascular smooth muscle cells and vascular intimal hyperplasia by suppressing STAT3/DRP1-mediated mitochondrial fission
title_full_unstemmed Silencing of PCK1 mitigates the proliferation and migration of vascular smooth muscle cells and vascular intimal hyperplasia by suppressing STAT3/DRP1-mediated mitochondrial fission
title_short Silencing of PCK1 mitigates the proliferation and migration of vascular smooth muscle cells and vascular intimal hyperplasia by suppressing STAT3/DRP1-mediated mitochondrial fission
title_sort silencing of pck1 mitigates the proliferation and migration of vascular smooth muscle cells and vascular intimal hyperplasia by suppressing stat3 drp1 mediated mitochondrial fission
topic phosphoenolpyruvate carboxyl kinase 1
vascular smooth muscle cells
mitochondrial fission
neointimal hyperplasia
dynamin-related protein 1
url https://www.sciengine.com/doi/10.3724/abbs.2024154
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