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Trans Sodium Crocetinate Alleviates Ischemia/Reperfusion-Induced

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Trans Sodium Crocetinate Alleviates Ischemia/Reperfusion-Induced International Immunopharmacology 71 (2019) 361–371 Contents lists available at ScienceDirect International Immunopharmacology journal homepage: www.elsevier.com/locate/intimp Trans sodium crocetinate alleviates ischemia/reperfusion-induced myocardial oxidative stress and apoptosis via the SIRT3/FOXO3a/SOD2 T ☆ signaling pathway ⁎ ⁎⁎ Guodong Changa, , Yingwei Chenb, Hongwei Zhanga, Wen Zhouc, a Department of Cardiovascular Diseases, The First People's Hospital of Shangqiu, Shangqiu City 476100, Henan Province, PR China b Department of Cardiovascular Diseases, The First Affiliated Hospital of Zhengzhou University, Zhengzhou City 450052, Henan Province, PR China c The Second Clinical College of Guangzhou University of Chinese Medicine, Guangzhou 510006, Guangdong Province, PR China ARTICLE INFO ABSTRACT Keywords: Trans sodium crocetinate (TSC) has been reported to exert a protective effect against cerebral ischemia/re- Trans sodium crocetinate perfusion (I/R) injury. However, whether TSC protects against myocardial ischemia/reperfusion (MI/R) injury Ischemia/reperfusion remains unknown. Herein, we found that TSC treatment reduced myocardial infract size and elevated serum LDH Myocardial injury and CK activities of MI/R rats. TSC administration attenuated oxidative stress in MI/R rats and H9C2 cells exposed to oxygen glucose deprivation/reperfusion (OGD/R). TSC administration relieved I/R-induced myo- cardial apoptosis in vivo and in vitro, as evidenced by reduced number of TUNEL positive cells, accompanying with marked decreases in caspase-3 activity and Bax protein level and an increase in Bcl-2 protein level. TSC treatment markedly increased SIRT3 activity and SIRT3 and SOD2 protein levels, and could also diminished the phosphorylation of FOXO3a protein. Additionally, TSC treatment attenuated the acetylation of FOXO3a and SOD2 protein. But, these effects were obviously blocked by SIRT3 knockdown. Besides, SIRT3 knockdown blocked the cardioprotective effect of TSC on OGD/R-induced oxidative stress, apoptosis and mitochondrial dysfunction in vitro. In summary, TSC alleviates I/R-induced myocardial oxidative stress and apoptosis via the SIRT3/FOXO3a/SOD2 signaling pathway. Our study suggests that TSC may become a novel drug for the treatment of MI/R injury. 1. Introduction capable of increasing the movement of oxygen from red blood cells into hypoxic tissues [8] Moreover, TSC treatment promoted cerebral tissue Myocardial infarction (MI), one of the most common cardiovascular oxygenation under conditions of vascular occlusion, whereas, atte- diseases, is hallmarked by coronary obstruction and interruption of nuated cerebral tissue hyperoxygenation during vascular perfusion [9]. blood flow [1,2]. Myocardial ischemia/reperfusion (MI/R) injury in- Additionally, TSC as a radiosensitizer increased the sensitivity of glio- itiates various deleterious cascades such as inflammation, oxidative blastoma cancer cells to radiation therapy and enhanced survival stress, and apoptosis [3,4]. Restoration of blood flow to the heart [10–12]. However, whether TSC could protect heart from MI/R injury without delay is considered as the most effective therapy for myocardial remains unclear. infarction [5]. In most situations, reperfusion therapy produces positive Reactive oxygen species (ROS) are important oxygen derivatives results, but it may also cause additional myocardial damage, known as and function as signaling molecules to participate in various physiology MI/R injury [6]. processes, such as gene expression [13]. Overproduction of ROS pro- Trans sodium crocetinate (TSC) is a derivative compound of the vokes a state of oxidative stress. Oxidative stress results from an im- carotenoid crocetin that can enhance the diffusivity of small molecules balance between accumulation of ROS and biological antioxidant sys- in aqueous solutions by modifying the structure of water [7]. TSC is tems, and is regarded as an important causative factor of MI/R injury ☆ Declarations of interest: None. ⁎ Correspondence to: G. Chang, Department of Cardiovascular Diseases, The First People's Hospital of Shangqiu, No. 292 Kaixuan Nan Road, Suiyang District, Shangqiu City 476100, Henan Province, PR China. ⁎⁎ Correspondence to: W. Zhou, The Second Clinical College of Guangzhou University of Chinese Medicine, Guangzhou City, 510006, Guangdong Province, PR China. E-mail addresses: [email protected] (G. Chang), [email protected] (W. Zhou). https://doi.org/10.1016/j.intimp.2019.03.056 Received 21 December 2018; Received in revised form 26 March 2019; Accepted 27 March 2019 Available online 02 April 2019 1567-5769/ © 2019 Elsevier B.V. All rights reserved. G. Chang, et al. International Immunopharmacology 71 (2019) 361–371 [14]. Myocardial ischemic causes the depletion of ATP, the accumula- incubated under normal conditions for 24 h. tion of H+ and Ca2+ and the opening of the mitochondrial permeability transition pore, leading to the superfluous generation of ROS and 2.4. Determination of myocardial infarct size thereby activating the apoptosis cascade [15]. Excessive ROS genera- tion induces oxidative damage to proteins, lipids and DNA, resulting in The myocardial infarct size was determined using 2,3,5-triphe- cell death [16]. nyltetrazolium chloride triazole (TTC; Solarbio) staining. At 24 h after Sirtuin-3 (SIRT3), located in the mitochondrial matrix, belongs to MI/R surgery, rats were sacrificed and the hearts were excised, frozen the sirtuin family and is highly expressed in cardiac myocytes [17]. Of and cut into slices. The slices were incubated with 2% TTC in PBS for note, SIRT3 has been postulated to be implicated in the pathological 15 min at 37 °C in the dark, followed by fixation with 10% formalin mechanism of MI/R injury [18]. FOXO3a, also known as FKHRL1, is a solution for 12 h. The infarct area (white) and non-infract area (red) forkhead transcription factor and belongs to the FOXO family. FOXO3a were analyzed using Image J software (NIH, Rockville, MD, USA). is capable of regulating the expression of genes involved in cellular development, longevity, autophagy, apoptosis and stress resistance 2.5. Detection of cardiac marker enzymes [19]. Superoxide dismutase (SOD), also known as manganese-depen- dent superoxide dismutase, belongs to the iron/manganese superoxide At 24 h after MI/R surgery, blood samples were collected and stored dismutase family and is a superoxide scavenger enzyme that plays a at −80 °C. Myocardium damage was assessed by determining serum vital role in maintenance of cellular redox balance [20]. lactate dehydrogenase (LDH) and creatine kinase (CK) activities. Serum In this study, we explored the cardioprotective effect of TSC in MI/R LDH and CK activities were determined using the LDH assay kit rats and H9C2 cells exposed to oxygen glucose deprivation/reperfusion (Jiancheng, Nanjing, China) and the CK assay kit (Jiancheng), ac- (OGD/R) injury. Further, the exact molecular mechanism underlying cording to the manufacturer's instructions. the anti-oxidative and anti-apoptosis effects of TSC was investigated in vitro. 2.6. Detection of ROS, GSH, SOD and MDA levels 2. Materials and methods The levels of ROS, glutathione (GSH), SOD and methane di- carboxylic aldehyde (MDA) in vitro and in vivo were determined using 2.1. Animal the ROS assay kit (Jiancheng), total glutathione assay kit (Beyotime, Shanghai, China), total superoxide dismutase assay kit with wst-8 Male Wistar rats (weighing 180–230 g) were supplied by Vital River (Beyotime) and MDA assay kit (Jiancheng), respectively. Lab Animal Technology Co., Ltd. (Beijing, China). Rats were penned individually, kept under a specific pathogen-free condition and had free 2.7. Terminal deoxynucleotidyl transferase dUTP nick end labeling access to standard pellet diet. Rats were randomized into sham + saline group (n = 8), MI/R + saline group (n = 8), MI/R + TSC (25 μg/kg; Terminal deoxynucleotidyl transferase dUTP nick end labeling n = 8) group, MI/R + TSC (50 μg/kg; n = 8) group and MI/R + TSC (TUNEL; Roche, Penzberg, Germany) assay was performed to evaluate (100 μg/kg; n = 8) group. TSC (ChemFaces, Wuhan, China) or vehicle cell apoptosis. Tissue slices or adherent cells were fixed in formalin (saline) was administered to rats with myocardial ischemia via the fe- solution for 30 min, followed by permeation with 0.3% Triton X-100 for moral vein at 10 min prior to reperfusion. All experimental procedures 5 min. After washing with PBS, tissue slices or cell smears were in- were approved by the Ethics Committee of The First People's Hospital of cubated with TUNEL reaction mixture for 1 h at 37 °C in darkness, Shangqiu. followed by staining with DAPI or hematoxylin. 2.2. Rat model of MI/R injury 2.8. Detection of caspase-3 activity To establish an in vivo model of MI/R injury, rats were fasted The activity of caspase-3 was measured using a Caspase-3 assay kit overnight and anesthetized by an intraperitoneal injection of sodium (Beyotime). Tissues or cells were homogenized or lysed in ice-cold lysis pentobarbital (40 mg/kg; Sigma, St. Louis, USA). During the operation, buffer and then incubated with Ac-DEVD-pNA (2 mM) for 1 h at 37 °C. rectal temperature was maintained at 37.0 ± 0.5 °C. The heart was The activity of caspase-3 was measured at 405 nm using a microplate exposed with a left thoracotomy, and a 4–0 silk suture slipknot was spectrophotometer (SpectraMax M5, Molecular Devices, and placed at the distal 1/3 of the left anterior descending coronary artery Sunnyvale, CA, USA). (LAD) origin. After 30 min
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