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A Novel Role of Claudin-5 in Prevention of Mitochondrial Fission Against Ischemic/Hypoxic Stress in Cardiomyocytes

  • Tao Luo
  • , Haiqiong Liu
  • , Baihe Chen
  • , Han Liu
  • , Ahmed Abdel-Latif
  • , Masafumi Kitakaze
  • , Xianbao Wang
  • , Yuanzhou Wu
  • , Dylan Chou
  • , Jin Kyung Kim

Research output: Contribution to journalArticlepeer-review

19 Citations (SciVal)

Abstract

Background: Downregulation of claudin-5 in the heart is associated with the end-stage heart failure. However, the underlying mechanism ofclaudin-5 is unclear. Here we investigated the molecular actions of claudin-5 in perspective of mitochondria in cardiomyocytes to better understand the role of claudin-5 in cardioprotection during ischemia. Methods: Myocardial ischemia/reperfusion (I/R; 30 min/24 h) and hypoxia/reoxygenation (H/R; 24 h/4 h) were used in this study. Confocal microscopy and transmission electron microscope (TEM) were used to observe mitochondrial morphology. Results: Claudin-5 was detected in murine heart tissue and neonatal rat cardiomyocytes (NRCM). Its protein level was severely decreased after myocardial I/R or H/R. Confocal microscopy showedclaudin-5 presented in the mitochondria of NRCM. H/R-induced claudin-5 downregulation was accompanied by mitochondrial fragmentation. The mitofusin 2 (Mfn2) expressionwas dramatically decreased while the dynamin-related protein (Drp) 1 expression was significantly increased after H/R. The TEM indicatedH/R-induced mitochondrial swelling and fission. Adenoviral claudin-5 overexpression reversed these structural disintegration of mitochondria. The mitochondria-centered intrinsic pathway of apoptosis triggered by H/R and indicated by the cytochrome c and cleaved caspase 3 in the cytoplasm of NRCMs was also reduced by overexpressing claudin-5. Claudin-5 overexpression in mouse heart also significantly decreased cleaved caspase 3 and the infarct size in ischemic heart with improved systolic function. Conclusion: We demonstrated for the first time the presence of claudin-5 in the mitochondria in cardiomyocytes and provided the firm evidence for the cardioprotective role of claudin-5 in the preservation of mitochondrial dynamics and cell fate against hypoxia- or ischemia-induced stress.

Original languageEnglish
Pages (from-to)1593-1606
Number of pages14
JournalCanadian Journal of Cardiology
Volume37
Issue number10
DOIs
StatePublished - Oct 2021

Bibliographical note

Publisher Copyright:
© 2021 Canadian Cardiovascular Society

Funding

This work was supported by a grant from the National Natural Science Foundation of China (grant no. 82060045 to Dr Luo), 2 Funded Projects from Zunyi Medical University (grant no. [2018]5772-025 to Dr Luo and [2018]5772-026 to Dr Chou), a grant from Guizhou province of China (grant no. [2021]224 to Dr Luo), 2 grants from the National Heart, Lung, and Blood Institute of the National Institutes of Health (R01 HL111180 to Dr Kim and R01 HL138488 to Dr Abdel-Latif), and a grant from the University of Kentucky COBRE Early Career Program (P20 GM103527 to Dr Abdel-Latif).

FundersFunder number
Guizhou province of China[2021]224
University of Kentucky COBREP20 GM103527
Zunyi Medical University5772-026, [2018]5772-025
National Institutes of Health (NIH)R01 HL111180, R01 HL138488
National Institutes of Health (NIH)
National Heart, Lung, and Blood Institute Family Blood Pressure ProgramR56HL124266
National Heart, Lung, and Blood Institute Family Blood Pressure Program
National Natural Science Foundation of China (NSFC)82060045
National Natural Science Foundation of China (NSFC)

    ASJC Scopus subject areas

    • Cardiology and Cardiovascular Medicine

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