National Key Laboratory for Innovation and Transformation of Luobing Theory, The Key Laboratory of Cardiovascular Remodeling and Function Research, Chinese Ministry of Education, Chinese National Health Commission and Chinese Academy of Medical Sciences, Department of Cardiology, Qilu Hospital of Shandong University, Jinan, China; Department of Medicine, Division of Cardiovascular Disease, University of Alabama at Birmingham, Birmingham, AL 35233, USA.
Department of Medicine, Division of Cardiovascular Disease, University of Alabama at Birmingham, Birmingham, AL 35233, USA.
J Mol Cell Cardiol. 2024 Jan;186:31-44. doi: 10.1016/j.yjmcc.2023.11.001. Epub 2023 Nov 16.
Ischemia/reperfusion (I/R) injury after revascularization contributes ∼50% of infarct size and causes heart failure, for which no established clinical treatment exists. β-hydroxybutyrate (β-OHB), which serves as both an energy source and a signaling molecule, has recently been reported to be cardioprotective when administered immediately before I/R and continuously after reperfusion. This study aims to determine whether administering β-OHB at the time of reperfusion with a single dose can alleviate I/R injury and, if so, to define the mechanisms involved. We found plasma β-OHB levels were elevated during ischemia in STEMI patients, albeit not to myocardial protection level, and decreased after revascularization. In mice, compared with normal saline, β-OHB administrated at reperfusion reduced infarct size (by 50%) and preserved cardiac function, as well as activated autophagy and preserved mtDNA levels in the border zone. Our treatment with one dose β-OHB reached a level achievable with fasting and strenuous physical activity. In neonatal rat ventricular myocytes (NRVMs) subjected to I/R, β-OHB at physiologic level reduced cell death, increased autophagy, preserved mitochondrial mass, function, and membrane potential, in addition to attenuating reactive oxygen species (ROS) levels. ATG7 knockdown/knockout abolished the protective effects of β-OHB observed both in vitro and in vivo. Mechanistically, β-OHB's cardioprotective effects were associated with inhibition of mTOR signaling. In conclusion, β-OHB, when administered at reperfusion, reduces infarct size and maintains mitochondrial homeostasis by increasing autophagic flux (potentially through mTOR inhibition). Since β-OHB has been safely tested in heart failure patients, it may be a viable therapeutic to reduce infarct size in STEMI patients.
再灌注后的缺血/再灌注(I/R)损伤约占梗死面积的 50%,并导致心力衰竭,目前尚无有效的临床治疗方法。β-羟丁酸(β-OHB)既是一种能量来源,也是一种信号分子,最近有报道称,在 I/R 前立即给予并在再灌注后持续给予β-OHB 具有心脏保护作用。本研究旨在确定在再灌注时给予单次剂量的β-OHB 是否可以减轻 I/R 损伤,如果可以,确定相关机制。我们发现 STEMI 患者在缺血期间血浆β-OHB 水平升高,尽管未达到心肌保护水平,但再灌注后降低。在小鼠中,与生理盐水相比,再灌注时给予β-OHB 可减少梗死面积(减少 50%)并保持心脏功能,同时在边缘区激活自噬并保持 mtDNA 水平。我们的单剂量β-OHB 治疗达到了禁食和剧烈运动可达到的水平。在经历 I/R 的新生大鼠心室肌细胞(NRVMs)中,生理水平的β-OHB 可降低细胞死亡、增加自噬、保持线粒体质量、功能和膜电位,同时减轻活性氧(ROS)水平。ATG7 敲低/敲除消除了β-OHB 在体外和体内观察到的保护作用。从机制上讲,β-OHB 的心脏保护作用与抑制 mTOR 信号有关。总之,β-OHB 在再灌注时通过增加自噬通量(可能通过抑制 mTOR)来减少梗死面积并维持线粒体稳态。由于β-OHB 已在心力衰竭患者中进行了安全测试,因此它可能是一种可行的治疗方法,可减少 STEMI 患者的梗死面积。