Volume 13 Issue 11
Nov.  2023
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Article Navigation >  Journal of Pharmaceutical Analysis  > 2023  >  13(11): 1309-1325
Hui-Nan Zhang, Meng Zhang, Wen Tian, Wei Quan, Fan Song, Shao-Yuan Liu, Xiao-Xiao Liu, Dan Mo, Yang Sun, Yuan-Yuan Gao, Wen Ye, Ying-Da Feng, Chang-Yang Xing, Chen Ye, Lei Zhou, Jing-Ru Meng, Wei Cao, Xiao-Qiang Li. Canonical transient receptor potential channel 1 aggravates myocardial ischemia-and-reperfusion injury by upregulating reactive oxygen species[J]. Journal of Pharmaceutical Analysis, 2023, 13(11): 1309-1325. doi: 10.1016/j.jpha.2023.08.018
Citation: Hui-Nan Zhang, Meng Zhang, Wen Tian, Wei Quan, Fan Song, Shao-Yuan Liu, Xiao-Xiao Liu, Dan Mo, Yang Sun, Yuan-Yuan Gao, Wen Ye, Ying-Da Feng, Chang-Yang Xing, Chen Ye, Lei Zhou, Jing-Ru Meng, Wei Cao, Xiao-Qiang Li. Canonical transient receptor potential channel 1 aggravates myocardial ischemia-and-reperfusion injury by upregulating reactive oxygen species[J]. Journal of Pharmaceutical Analysis, 2023, 13(11): 1309-1325. doi: 10.1016/j.jpha.2023.08.018
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Canonical transient receptor potential channel 1 aggravates myocardial ischemia-and-reperfusion injury by upregulating reactive oxygen species

doi: 10.1016/j.jpha.2023.08.018

  • a. Department of Health Management, Second Affiliated Hospital, Fourth Military Medical University, Xi'an, 710038, China;

  • b. Department of Pharmacology, School of Pharmacy, Fourth Military Medical University, Xi'an, 710032, China;

  • c. Key Laboratory of Gastrointestinal Pharmacology of Chinese Materia Medica of the State Administration of Traditional Chinese Medicine, School of Pharmacy, Fourth Military Medical University, Xi'an, 710032, China;

  • d. Shaanxi Key Laboratory of "Qin Medicine" Research and Development, Shaanxi Administration of Traditional Chinese Medicine, Xi'an, 710032, China;

  • e. Institute of Materia Medica, School of Pharmacy, Fourth Military Medical University, Xi'an, 710032, China;

  • f. Department of Ultrasound Diagnostics, Second Affiliated Hospital, Fourth Military Medical University, Xi'an, 710038, China;

  • g. Department of Pharmacy, School of Chemistry & Pharmacy, Northwest A&F University, Yangling, Shaanxi, 712100, China

Funds:

This work was supported by the National Natural Science Foundation of China (Grant Nos.: 81970245, 82270357, and 81770432), the Scientific Research Project of Shaanxi Administration of Traditional Chinese Medicine, China (Grant Nos.: 2021-04-ZZ-001, 2021-QYPT-003, and 2022-SLRH-YQ-004), the Project of Science and Technology Department of Shaanxi Province in China (Project No.: 2022YWZX-PG-01), and the Natural Science Basic Research Program of Shaanxi Province in China (Grant No.: 2023-JC-JQ-61).

  • Received Date: Apr. 03, 2023
  • Accepted Date: Aug. 29, 2023
  • Rev Recd Date: Aug. 28, 2023
  • Publish Date: Sep. 01, 2023
    Abstract
  • The canonical transient receptor potential channel (TRPC) proteins form Ca2+-permeable cation channels that are involved in various heart diseases. However, the roles of specific TRPC proteins in myocardial ischemia/reperfusion (I/R) injury remain poorly understood. We observed that TRPC1 and TRPC6 were highly expressed in the area at risk (AAR) in a coronary artery ligation induced I/R model. Trpc1-/- mice exhibited improved cardiac function, lower serum Troponin T and serum creatine kinase level, smaller infarct volume, less fibrotic scars, and fewer apoptotic cells after myocardial-I/R than wild-type or Trpc6-/- mice. Cardiomyocyte-specific knockdown of Trpc1 using adeno-associated virus 9 mitigated myocardial I/R injury. Furthermore, Trpc1 deficiency protected adult mouse ventricular myocytes (AMVMs) and HL-1 cells from death during hypoxia/reoxygenation (H/R) injury. RNA-sequencing-based transcriptome analysis revealed differential expression of genes related to reactive oxygen species (ROS) generation in Trpc1-/- cardiomyocytes. Among these genes, oxoglutarate dehydrogenase-like (Ogdhl) was markedly downregulated. Moreover, Trpc1 deficiency impaired the calcineurin (CaN)/nuclear factor-kappa B (NF-κB) signaling pathway in AMVMs. Suppression of this pathway inhibited Ogdhl upregulation and ROS generation in HL-1 cells under H/R conditions. Chromatin immunoprecipitation assays confirmed NF-κB binding to the Ogdhl promoter. The cardioprotective effect of Trpc1 deficiency was canceled out by overexpression of NF-κB and Ogdhl in cardiomyocytes. In conclusion, our findings reveal that TRPC1 is upregulated in the AAR following myocardial I/R, leading to increased Ca2+ influx into associated cardiomyocytes. Subsequently, this upregulates Ogdhl expression through the CaN/NF-κB signaling pathway, ultimately exacerbating ROS production and aggravating myocardial I/R injury.
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