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CircNSD1 promotes cardiac fibrosis through targeting the miR-429-3p/SULF1/Wnt/β-catenin signaling pathway

Acta Pharmacologica Sinica volume 45, pages 2092–2106 (2024)Cite this article

Abstract

Cardiac fibrosis is a detrimental pathological process, which constitutes the key factor for adverse cardiac structural remodeling leading to heart failure and other critical conditions. Circular RNAs (circRNAs) have emerged as important regulators of various cardiovascular diseases. It is known that several circRNAs regulate gene expression and pathological processes by binding miRNAs. In this study we investigated whether a novel circRNA, named circNSD1, and miR-429-3p formed an axis that controls cardiac fibrosis. We established a mouse model of myocardial infarction (MI) for in vivo studies and a cellular model of cardiac fibrogenesis in primary cultured mouse cardiac fibroblasts treated with TGF-β1. We showed that miR-429-3p was markedly downregulated in the cardiac fibrosis models. Through gain- and loss-of-function studies we confirmed miR-429-3p as a negative regulator of cardiac fibrosis. In searching for the upstream regulator of miR-429-3p, we identified circNSD1 that we subsequently demonstrated as an endogenous sponge of miR-429-3p. In MI mice, knockdown of circNSD1 alleviated cardiac fibrosis. Moreover, silence of human circNSD1 suppressed the proliferation and collagen production in human cardiac fibroblasts in vitro. We revealed that circNSD1 directly bound miR-429-3p, thereby upregulating SULF1 expression and activating the Wnt/β-catenin pathway. Collectively, circNSD1 may be a novel target for the treatment of cardiac fibrosis and associated cardiac disease.

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Fig. 1: MiR-429-3p participates in the regulation of cardiac fibrosis in vitro.
Fig. 2: MiR-429-3p serve as the target of circNSD1.
Fig. 3: Silencing of circNSD1 improves cardiac function and suppresses cardiac fibrosis in vivo.
Fig. 4: CircNSD1 regulates production of collagen and fibronectin and CFs proliferation in vitro.
Fig. 5: H-circNSD1 regulates fibrotic phenotype of HCFs.
Fig. 6: CircNSD1 promotes fibrotic phenotype of CFs by inhibiting miR-429-3p.
Fig. 7: MiR-429-3p participates in regulating cardiac fibrosis through SULF1.
Fig. 8: CircNSD1/miR-429-3p/SULF1/Wnt/β-catenin axis plays an important role in cardiac fibrosis.
Fig. 9: The underlying mechanism of circNSD1 regulating cardiac fibrosis.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (82070240, 82270246, 82073844, 82070236 and 82073838), and Harbin Medical University Marshal Initiative Funding (HMUMIF-21026).

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  1. These authors contributed equally: Dong-ni Ji, Sai-di Jin, Yuan Jiang

Authors and Affiliations

  1. Department of Pharmacology, State-Province Key Laboratories of Biomedicine-Pharmaceutics of China, Key Laboratory of Cardiovascular Medicine Research, Ministry of Education, College of Pharmacy, Harbin Medical University, Harbin, 150081, China

    Dong-ni Ji, Sai-di Jin, Yuan Jiang, Fei-yong Xu, Shu-wei Fan, Yi-lin Zhao, Xin-qi Liu, Hao Sun, Wen-zheng Cheng, Xin-yue Zhang, Xiao-xiang Guan, Bo-wen Zhang, Ning Wang, Rong Zhang, Ming-yu Zhang & Chao-qian Xu

  2. National Key Laboratory of Frigid Zone Cardiovascular Diseases, Harbin Medical University, Harbin, 150081, China

    Dong-ni Ji, Sai-di Jin, Yuan Jiang, Fei-yong Xu, Yi-lin Zhao, Xin-qi Liu, Hao Sun, Wen-zheng Cheng, Xin-yue Zhang, Xiao-xiang Guan, Bo-wen Zhang, Ning Wang, Rong Zhang, Ming-yu Zhang & Chao-qian Xu

  3. Institute of Clinical Pharmacy, The Second Affiliated Hospital of Harbin Medical University, Harbin, 150081, China

    Bo-wen Zhang & Zhi-min Du

  4. Center of Chronic Diseases and Drug Research of Mudanjiang Medical University, Mudanjiang, 157011, China

    Ying Wang

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Contributions

C-qX, M-yZ and RZ conceived the research, contributed to the manuscript revision, and jointly supervised this work. D-nJ and S-dJ contributed significantly to data analyses and manuscript preparation. D-nJ, F-yX and S-wF performed experiments and wrote the manuscript. YJ edited the manuscript. Y-lZ, X-qL, HS, W-zC, X-yZ, XxG and B-wZ contributed animal studies and manuscript revision. Z-mD, YW and NW provided technical support.

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Correspondence to Rong Zhang, Ming-yu Zhang or Chao-qian Xu.

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Ji, Dn., Jin, Sd., Jiang, Y. et al. CircNSD1 promotes cardiac fibrosis through targeting the miR-429-3p/SULF1/Wnt/β-catenin signaling pathway. Acta Pharmacol Sin 45, 2092–2106 (2024). https://doi.org/10.1038/s41401-024-01296-7

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