Dexmedetomidine-induced cardioprotection is mediated by inhibition of high mobility group box-1 and the cholinergic anti-inflammatory pathway in myocardial ischemia-reperfusion injury

PLoS One. 2019 Jul 25;14(7):e0218726. doi: 10.1371/journal.pone.0218726. eCollection 2019.

Abstract

Objectives: Dexmedetomidine (DEX) is a selective α2-adrenoceptor agonist that has anti-inflammatory and cardioprotective effects in myocardial ischemia/reperfusion (I/R) injury. The present study aimed to investigate the underlying mechanism by which DEX protects against myocardial I/R.

Methods: Sprague Dawley rats were subjected to either sham operation or myocardial I/R, which was induced by ligating the left anterior descending coronary artery for 30 min followed by reperfusion for 120 min. Rats were treated with either DEX or saline prior to surgery. We measured heart infarct size, serum cardiac Troponin I (cTnI), cardiac High mobility group box-1 (HMGB1) expression, myocardial apoptosis and cytokine production of interleukin-6 (IL-6) and tumor necrosis factor-α (TNF-α). Besides, we evaluated the heart function at 4 weeks post-reperfusion by echocardiography. Unilateral vagotomy or inhibition of the α7 nicotinic acetylcholine receptor (α7nAChR) with methyllycaconitine (MLA) was applied to investigate whether DEX-induced cardioprotection is mediated via the cholinergic anti-inflammatory pathway. Cardiac-selective overexpression of HMGB1 was administered to further confirm if HMGB1 is a key anti-inflammatory target during DEX-induced cardioprotection.

Results: DEX pretreatment significantly attenuated I/R-induced cardiac damage, as evidenced by decreases in short-term injury indicators including myocardial infarct size, cTnI release, myocardial apoptosis, cardiac HMGB1 expression, IL-6 and TNF-α production, as well as improvement on long-term cardiac function at 4 weeks post-reperfusion. These effects were partially reversed by either unilateral vagotomy or methyllycaconitine treatment. Besides, cardiac HMGB1-overexpression nearly abolished DEX-induced cardioprotection.

Conclusions: DEX pretreatment protects against myocardial I/R by inhibiting cardiac HMGB1 production and activating the cholinergic anti-inflammatory pathway.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cardiotonic Agents / pharmacology*
  • Dexmedetomidine / pharmacology*
  • Gene Expression Regulation / drug effects
  • HMGB1 Protein / antagonists & inhibitors
  • HMGB1 Protein / genetics*
  • Humans
  • Interleukin-6 / genetics
  • Myocardial Reperfusion Injury / drug therapy*
  • Myocardial Reperfusion Injury / genetics
  • Myocardial Reperfusion Injury / pathology
  • Myocardium / pathology
  • Neuroimmunomodulation / drug effects
  • Rats
  • Signal Transduction / drug effects
  • Troponin I / genetics
  • Tumor Necrosis Factor-alpha / genetics
  • Vagotomy

Substances

  • Cardiotonic Agents
  • HMGB1 Protein
  • Interleukin-6
  • Troponin I
  • Tumor Necrosis Factor-alpha
  • Dexmedetomidine

Grants and funding

This study was supported, in part, by grants from the National Natural Science Foundation of China (81601666 to JZ, 81471835 and 81671880 to FJ, 81601659 to KP, 81701098 to XM), the Jiangsu Provincial Medical Youth Talents Program (QNRC2016741 to KP), and the Jiangsu Provincial Medical Innovation Team (CXTDA2017043 to FJ). URL:National Natural Science Foundation of China: https://isisn.nsfc.gov.cn/egrantweb/ Jiangsu Provincial Medical Youth Talents Program &Jiangsu Provincial Medical Innovation Team: http://wskj.jswst.gov.cn; The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.