Liu Yanan, Wang Zhenglian, Xie Weidang, Gu Zhengtao, Xu Qiulin, Su Lei
Department of Intensive Care Unit, Nanfang Hospital, Southern Medical University, Guangzhou, Guangdong 510515, P.R. China.
Graduate School, Guangzhou University of Chinese Medicine, Guangzhou, Guangdong 510120, P.R. China.
Mol Med Rep. 2017 Sep;16(3):2579-2587. doi: 10.3892/mmr.2017.6859. Epub 2017 Jun 27.
Heat stress and gut‑derived endotoxinemia are common causes of multiple organ dysfunction syndrome in heat stroke patients. Evidence has demonstrated that cell apoptosis in the small intestine serves an important role in the pathogenesis of heatstroke, which leads to increased intestinal permeability to endotoxin or lipopolysaccharides (LPS) from the gut entering the circulation. However, little is known about the potential underlying mechanisms mediating heat stress combined with LPS‑induced intestinal epithelial cell apoptosis. In the present study, LPS combined with heat stress induced production of reactive oxygen species (ROS), mitochondrial membrane potential disruption and cell apoptosis, which eventually led to increased intestinal permeability and reduced epithelial resistance in the IEC‑6 cell line. Inductions in ROS, mitochondrial membrane potential disruption and cell apoptosis were detected by using an ROS assay kit, 5,5',6,6'‑tetrachloro‑1,1',3,3'tetraethylbenzimidazo carbocyanine iodide dye kit and annexin V‑fluorescein isothiocyanate apoptosis kit, respectively. The effect of ROS on mitogen activated protein kinases (MAPKs) and c‑Jun activation was investigated using the antioxidant drug, butylated hydroxyanisole (BHA) by western blotting. The results of the present study demonstrated that ROS is essential to activate p38, extracellular signal‑regulated kinase (ERK) and c‑Jun, but not c‑Jun N‑terminal kinase (JNK), in LPS combined with heat stress treated cells. Furthermore, ROS, and activation of p38, JNK and c‑Jun, were revealed to serve pro‑apoptosis roles which aggravated damage to epithelial barrier integrity, as assessed by flow cytometry using Annexin V‑fluorescein isothiocyanate staining and pretreatment of cells with specific inhibitors of ROS, JNK, p38 and c‑Jun (BHA, SP600125, SB203580 and c‑Jun peptide, respectively). Transepithelial electrical resistance and horseradish peroxidase permeability were detected in cells treated with LPS combined with heat stress, which revealed that ERK serves an anti‑apoptosis role, as determined by pretreatment of cells with PD98059, a specific inhibitor of ERK. In conclusion, these findings suggested a novel role of the ROS signaling pathway which involved activation of MAPKs and c‑Jun, following LPS combined with heat stress‑induced IEC‑6 cell apoptosis and impairment of the epithelial barrier. These results may facilitate understanding of pathological conditions involving ROS, such as heat stroke.
热应激和肠道源性内毒素血症是中暑患者多器官功能障碍综合征的常见病因。有证据表明,小肠中的细胞凋亡在中暑发病机制中起重要作用,这会导致肠道对内毒素或来自肠道进入循环的脂多糖(LPS)的通透性增加。然而,关于介导热应激与LPS诱导的肠上皮细胞凋亡的潜在机制知之甚少。在本研究中,LPS联合热应激诱导活性氧(ROS)生成、线粒体膜电位破坏和细胞凋亡,最终导致IEC-6细胞系的肠道通透性增加和上皮电阻降低。分别使用ROS检测试剂盒、5,5',6,6'-四氯-1,1',3,3'-四乙基苯并咪唑羰花青碘化物染料试剂盒和膜联蛋白V-异硫氰酸荧光素凋亡试剂盒检测ROS生成、线粒体膜电位破坏和细胞凋亡。使用抗氧化剂丁基羟基茴香醚(BHA)通过蛋白质印迹法研究ROS对丝裂原活化蛋白激酶(MAPK)和c-Jun活化的影响。本研究结果表明,在LPS联合热应激处理的细胞中,ROS对于激活p38、细胞外信号调节激酶(ERK)和c-Jun至关重要,但对c-Jun氨基末端激酶(JNK)无此作用。此外,通过使用膜联蛋白V-异硫氰酸荧光素染色的流式细胞术以及用ROS、JNK、p38和c-Jun的特异性抑制剂(分别为BHA、SP600125、SB203580和c-Jun肽)预处理细胞评估,发现ROS以及p38、JNK和c-Jun的活化具有促凋亡作用,加重了对上皮屏障完整性的损害。在用LPS联合热应激处理的细胞中检测跨上皮电阻和辣根过氧化物酶通透性,结果显示,通过用ERK的特异性抑制剂PD98059预处理细胞确定,ERK具有抗凋亡作用。总之,这些发现提示了ROS信号通路的新作用,即在LPS联合热应激诱导IEC-6细胞凋亡和上皮屏障受损后,ROS信号通路涉及MAPK和c-Jun的激活。这些结果可能有助于理解涉及ROS的病理状况,如中暑。