Small molecule induces mitochondrial fusion for neuroprotection via targeting CK2 without affecting its conventional kinase activity

Abstract Mitochondrial fusion/fission dynamics plays a fundamental role in neuroprotection; however, there is still a severe lack of therapeutic targets for this biological process. Here, we found that the naturally derived small molecule echinacoside (ECH) significantly promotes mitochondrial fusio...

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Main Authors: Ke-Wu Zeng, Jing-Kang Wang, Li-Chao Wang, Qiang Guo, Ting-Ting Liu, Fu-Jiang Wang, Na Feng, Xiao-Wen Zhang, Li-Xi Liao, Mei-Mei Zhao, Dan Liu, Yong Jiang, Pengfei Tu
Format: Article
Language:English
Published: Nature Publishing Group 2021-02-01
Series:Signal Transduction and Targeted Therapy
Online Access:https://doi.org/10.1038/s41392-020-00447-6
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author Ke-Wu Zeng
Jing-Kang Wang
Li-Chao Wang
Qiang Guo
Ting-Ting Liu
Fu-Jiang Wang
Na Feng
Xiao-Wen Zhang
Li-Xi Liao
Mei-Mei Zhao
Dan Liu
Yong Jiang
Pengfei Tu
author_facet Ke-Wu Zeng
Jing-Kang Wang
Li-Chao Wang
Qiang Guo
Ting-Ting Liu
Fu-Jiang Wang
Na Feng
Xiao-Wen Zhang
Li-Xi Liao
Mei-Mei Zhao
Dan Liu
Yong Jiang
Pengfei Tu
author_sort Ke-Wu Zeng
collection DOAJ
description Abstract Mitochondrial fusion/fission dynamics plays a fundamental role in neuroprotection; however, there is still a severe lack of therapeutic targets for this biological process. Here, we found that the naturally derived small molecule echinacoside (ECH) significantly promotes mitochondrial fusion progression. ECH selectively binds to the previously uncharacterized casein kinase 2 (CK2) α′ subunit (CK2α′) as a direct cellular target, and genetic knockdown of CK2α′ abolishes ECH-mediated mitochondrial fusion. Mechanistically, ECH allosterically regulates CK2α′ conformation to recruit basic transcription factor 3 (BTF3) to form a binary protein complex. Then, the CK2α′/BTF3 complex facilitates β-catenin nuclear translocation to activate TCF/LEF transcription factors and stimulate transcription of the mitochondrial fusion gene Mfn2. Strikingly, in a mouse middle cerebral artery occlusion (MCAO) model, ECH administration was found to significantly improve cerebral injuries and behavioral deficits by enhancing Mfn2 expression in wild-type but not CK2α′+/− mice. Taken together, our findings reveal, for the first time, that CK2 is essential for promoting mitochondrial fusion in a Wnt/β-catenin-dependent manner and suggest that pharmacologically targeting CK2 is a promising therapeutic strategy for ischemic stroke.
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series Signal Transduction and Targeted Therapy
spelling doaj-art-72bc1769597745a39d0d9860b2d08daa2025-08-20T01:56:09ZengNature Publishing GroupSignal Transduction and Targeted Therapy2059-36352021-02-016111310.1038/s41392-020-00447-6Small molecule induces mitochondrial fusion for neuroprotection via targeting CK2 without affecting its conventional kinase activityKe-Wu Zeng0Jing-Kang Wang1Li-Chao Wang2Qiang Guo3Ting-Ting Liu4Fu-Jiang Wang5Na Feng6Xiao-Wen Zhang7Li-Xi Liao8Mei-Mei Zhao9Dan Liu10Yong Jiang11Pengfei Tu12State Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityState Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityState Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityState Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityState Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityState Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityState Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityState Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityState Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityState Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityProteomics Laboratory, Medical and Healthy Analytical Center, Peking University Health Science CenterState Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityState Key Laboratory of Natural and Biomimetic Drugs, School of Pharmaceutical Sciences, Peking UniversityAbstract Mitochondrial fusion/fission dynamics plays a fundamental role in neuroprotection; however, there is still a severe lack of therapeutic targets for this biological process. Here, we found that the naturally derived small molecule echinacoside (ECH) significantly promotes mitochondrial fusion progression. ECH selectively binds to the previously uncharacterized casein kinase 2 (CK2) α′ subunit (CK2α′) as a direct cellular target, and genetic knockdown of CK2α′ abolishes ECH-mediated mitochondrial fusion. Mechanistically, ECH allosterically regulates CK2α′ conformation to recruit basic transcription factor 3 (BTF3) to form a binary protein complex. Then, the CK2α′/BTF3 complex facilitates β-catenin nuclear translocation to activate TCF/LEF transcription factors and stimulate transcription of the mitochondrial fusion gene Mfn2. Strikingly, in a mouse middle cerebral artery occlusion (MCAO) model, ECH administration was found to significantly improve cerebral injuries and behavioral deficits by enhancing Mfn2 expression in wild-type but not CK2α′+/− mice. Taken together, our findings reveal, for the first time, that CK2 is essential for promoting mitochondrial fusion in a Wnt/β-catenin-dependent manner and suggest that pharmacologically targeting CK2 is a promising therapeutic strategy for ischemic stroke.https://doi.org/10.1038/s41392-020-00447-6
spellingShingle Ke-Wu Zeng
Jing-Kang Wang
Li-Chao Wang
Qiang Guo
Ting-Ting Liu
Fu-Jiang Wang
Na Feng
Xiao-Wen Zhang
Li-Xi Liao
Mei-Mei Zhao
Dan Liu
Yong Jiang
Pengfei Tu
Small molecule induces mitochondrial fusion for neuroprotection via targeting CK2 without affecting its conventional kinase activity
Signal Transduction and Targeted Therapy
title Small molecule induces mitochondrial fusion for neuroprotection via targeting CK2 without affecting its conventional kinase activity
title_full Small molecule induces mitochondrial fusion for neuroprotection via targeting CK2 without affecting its conventional kinase activity
title_fullStr Small molecule induces mitochondrial fusion for neuroprotection via targeting CK2 without affecting its conventional kinase activity
title_full_unstemmed Small molecule induces mitochondrial fusion for neuroprotection via targeting CK2 without affecting its conventional kinase activity
title_short Small molecule induces mitochondrial fusion for neuroprotection via targeting CK2 without affecting its conventional kinase activity
title_sort small molecule induces mitochondrial fusion for neuroprotection via targeting ck2 without affecting its conventional kinase activity
url https://doi.org/10.1038/s41392-020-00447-6
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