Dusp14-Mediated Dephosphorylation of MLKL Protects Against Cardiomyocyte Necroptosis in Hypothyroidism-Induced Heart Failure

Y Yitian Zheng (Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).) Y Yueyue Cao (Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).) W Wenyao Wang (Key Laboratory of the Ministry of Education for Advanced Catalysis Materials Zhejiang Normal University Jinhua China) Y Yicheng Tong (Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).) S Shuaixing Wang (National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China (S.W.).) C Chen Li (Sibley School of Mechanical and Aerospace Engineering, Cornell University, Ithaca, NY, USA.) M Mingming Zhao Y Yao Song (State Key Laboratory of Catalysis, Collaborative Innovation Center of Chemistry for Energy Materials) Y Yuan-geng-shuo Wang (Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).) J Jiating Qi (Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).) C Chao Wu J Jie Yang J Jilin Zheng J Jun Gao (Qingdao Institute of Bioenergy and Bioprocess Technology) J Jingjia Wang (Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).) Q Qing Yang (Department of Hepatic Surgery and Liver Transplantation Centre) G Gang Liu J Jiajun Zhao Y Yan Zhang H Han Xiao (Department of Chemistry, Rice University, 6100 Main Street, Houston, Texas 77005, United States) Y You-Yi Zhang (Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).) Y Yi-Da Tang (Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).)

Abstract

BACKGROUND: Hypothyroidism leads to multiple organ dysfunction, with the heart the most affected. However, the pathologic mechanism of hypothyroidism-induced heart failure remains to be completely elucidated. Thyroid hormone replacement therapy enhances myocardium systolic function but increases the occurrence of arrythmias. There is an urgent need to explore these mechanisms in detail and to discover and develop drugs that can target and manage heart failure in patients with hypothyroidism. METHODS: In this study, a mouse model of hypothyroidism-induced heart failure was established through the administration of propylthiouracil. Dusp14 knockout mice were generated, and adeno-associated virus–mediated cardiomyocyte-specific overexpression of Dusp14 (dual specificity phosphatase 14) was used in combination with related cellular experiments to investigate the protective effects of Dusp14 on hypothyroidism-induced heart failure. Further analyses confirmed the crucial involvement of necroptosis in the pathogenesis of hypothyroidism-induced heart failure, and demonstrated the protective role of Dusp14 in modulating necroptosis. In addition, a novel small molecule compound that effectively regulates Dusp14 activity in vitro was identified through molecular docking, providing a potential therapeutic avenue. RESULTS: Dusp14 regulates necroptosis and mitigates hypothyroidism-induced heart failure. Myocardial tissue sections from mice in the hypothyroidism group showed positive Evans blue dye staining, and the serum levels of the myocardial injury marker lactate dehydrogenase were significantly higher compared with the euthyroid group (n=8). In addition, phosphorylation levels of the necroptosis marker MLKL (mixed lineage kinase domain-like protein) were significantly elevated, indicating the activation of necroptosis (n=8). These findings suggest that myocardial necroptosis is activated during hypothyroidism. Myocardial-specific overexpression of Dusp14 reduced myocardial necroptosis and improved myocardial contractile function in hypothyroid mice (n=8). In contrast, Dusp14 knockout exacerbated myocardial contractile dysfunction and necroptosis in these mice (n=5–7). These results indicate that Dusp14 alleviates hypothyroidism-induced heart failure by inhibiting necroptosis. P077-0472, a small molecule compound, was identified as an activator of Dusp14, which could inhibit cardiomyocyte necroptosis from hypothyroidism (n=6). CONCLUSIONS: Dusp14 inhibits cardiomyocyte necroptosis from hypothyroidism and consequently rescues damaged cardiomyocytes. P077-0472, a novel small molecule compound that activates the dephosphorylation function of Dusp14, could inhibit cardiomyocyte necroptosis from hypothyroidism.

Article Details

Journal Circulation
Volume / Issue Vol. 151, Issue 25
Published June 24, 2025
Pages 1797-1813
ISSN 0009-7322
Publisher Lippincott Williams & Wilkins

Journal Info

Circulation

Lippincott Williams & Wilkins

ISSN: 0009-7322 Health Sciences

Authors (22)

Y

Yitian Zheng

Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).

Y

Yueyue Cao

Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).

W

Wenyao Wang

Key Laboratory of the Ministry of Education for Advanced Catalysis Materials Zhejiang Normal University Jinhua China

Y

Yicheng Tong

Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).

S

Shuaixing Wang

National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China (S.W.).

C

Chen Li

Sibley School of Mechanical and Aerospace Engineering, Cornell University, Ithaca, NY, USA.

M

Mingming Zhao

Y

Yao Song

State Key Laboratory of Catalysis, Collaborative Innovation Center of Chemistry for Energy Materials

Y

Yuan-geng-shuo Wang

Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).

J

Jiating Qi

Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).

C

Chao Wu

J

Jie Yang

J

Jilin Zheng

J

Jun Gao

Qingdao Institute of Bioenergy and Bioprocess Technology

J

Jingjia Wang

Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).

Q

Qing Yang

Department of Hepatic Surgery and Liver Transplantation Centre

G

Gang Liu

J

Jiajun Zhao

Y

Yan Zhang

H

Han Xiao

Department of Chemistry, Rice University, 6100 Main Street, Houston, Texas 77005, United States

Y

You-Yi Zhang

Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).

Y

Yi-Da Tang

Department of Cardiology and Institute of Vascular Medicine, Peking University Third Hospital, Beijing, China (Y. Zheng, Y.C., W.W., Y.T., C.L., M.Z., Y.S., Y.-g.-s.W., J.Q., C.W., J.Y., J. Zheng, J.G., J.W., Y. Zhang, H.X., Y.-Y.Z., Y.-D.T.).