Hollis Russell, Li Jingsong, Lee Yongchan, Jin Hui, Zhou Mian, Nofi Colleen P, Sfakianos Maria, Coppa Gene, Aziz Monowar, Wang Ping
Center for Immunology and Inflammation, The Feinstein Institutes for Medical Research, Manhasset, New York.
Department of Surgery, Zucker School of Medicine, Manhasset, New York.
Shock. 2025 Jan 1;63(1):101-109. doi: 10.1097/SHK.0000000000002467. Epub 2024 Aug 21.
Introduction: Gut ischemia and reperfusion (I/R) injury promotes the release of damage-associated molecular patterns (DAMPs) such as extracellular cold-inducible RNA-binding protein (eCIRP). Gut I/R often leads to acute lung injury (ALI), a major contributor to mortality. Milk fat globule-epidermal growth factor-factor VIII-derived oligopeptide-3 (MOP3) is a novel peptide that attenuates sepsis by opsonizing eCIRP and facilitating its phagocytic clearance. We hypothesized that MOP3 reduces inflammation, mitigates gut and lung injury, and improves survival in gut I/R injury. Methods: Phagocytosis of FITC-labeled eCIRP by intestinal epithelial cells was determined by confocal microscopy, and the cell supernatant was evaluated for cytokine expression by ELISA. Adult C57BL/6 mice underwent 60 min of gut ischemia via superior mesenteric artery occlusion followed by reperfusion. Mice were treated with MOP3 or vehicle via retro-orbital injection at the time of reperfusion. At 4 h post-I/R, blood, gut, and lungs were harvested for further assay. In additional mice, 36-h survival was assessed. Plasma levels of injury and inflammatory markers were measured with colorimetry and ELISA, respectively. Tissue mRNA expression was measured with qPCR. Myeloperoxidase (MPO), TUNEL, histologic injury, and ZO-1 immunohistochemistry assessments were performed. Results: MOP3 significantly increased eCIRP phagocytosis by intestinal epithelial cells ( P < 0.01) and decreased IL-6 release ( P < 0.001). Gut I/R caused elevated plasma eCIRP levels. MOP3 treatment significantly reduced plasma levels of IL-1β ( P < 0.01), IL-6 ( P < 0.05), and lactate dehydrogenase ( P < 0.05) along with a significant decrease in gut ( P < 0.05) and lung ( P < 0.001) injury scores as well as gut cell death ( P < 0.05). Moreover, MOP3 reduced pulmonary levels of chemokines and the granulocyte activation marker MPO after gut I/R. Mechanistically, ZO-1 expression in the gut was decreased following gut I/R injury, whereas MOP3 significantly reversed the decrease in ZO-1 mRNA expression ( P < 0.001). Finally, mice treated with MOP3 exhibited a significant decrease in mortality ( P < 0.05). Conclusions: Treatment with MOP3 effectively mitigates organ injury induced by gut I/R. This beneficial effect is attributed to the facilitation of eCIRP clearance, directing the potential of MOP3 as an innovative therapeutic approach for this critical and often fatal condition.
肠道缺血再灌注(I/R)损伤会促使损伤相关分子模式(DAMPs)的释放,如细胞外冷诱导RNA结合蛋白(eCIRP)。肠道I/R常导致急性肺损伤(ALI),这是导致死亡的主要因素。乳脂肪球-表皮生长因子-因子VIII衍生寡肽-3(MOP3)是一种新型肽,它通过调理eCIRP并促进其吞噬清除来减轻脓毒症。我们推测MOP3可减轻炎症、缓解肠道和肺部损伤,并改善肠道I/R损伤后的存活率。方法:通过共聚焦显微镜检测肠道上皮细胞对异硫氰酸荧光素(FITC)标记的eCIRP的吞噬作用,并通过酶联免疫吸附测定(ELISA)评估细胞上清液中的细胞因子表达。成年C57BL/6小鼠通过肠系膜上动脉闭塞进行60分钟的肠道缺血,随后进行再灌注。在再灌注时通过眶后注射用MOP3或赋形剂处理小鼠。在I/R后4小时,采集血液、肠道和肺组织用于进一步检测。在另外的小鼠中,评估36小时的存活率。分别用比色法和ELISA测量损伤和炎症标志物的血浆水平。用定量聚合酶链反应(qPCR)测量组织mRNA表达。进行髓过氧化物酶(MPO)、末端脱氧核苷酸转移酶介导的缺口末端标记(TUNEL)、组织学损伤和紧密连接蛋白1(ZO-1)免疫组织化学评估。结果:MOP3显著增加肠道上皮细胞对eCIRP的吞噬作用(P<0.01),并减少白细胞介素-6(IL-6)的释放(P<0.001)。肠道I/R导致血浆eCIRP水平升高。MOP3处理显著降低血浆中IL-1β(P<0.01)、IL-6(P<0.05)和乳酸脱氢酶(P<0.05)的水平,同时肠道(P<0.05)和肺(P<0.001)损伤评分以及肠道细胞死亡(P<0.05)显著降低。此外,MOP3降低了肠道I/R后肺组织中趋化因子水平和粒细胞活化标志物MPO。从机制上讲,肠道I/R损伤后肠道中ZO-1的表达降低,而MOP3显著逆转了ZO-1 mRNA表达的降低(P<0.001)。最后,用MOP3处理的小鼠死亡率显著降低(P<0.05)。结论:MOP3治疗可有效减轻肠道I/R诱导的器官损伤。这种有益作用归因于促进了eCIRP的清除,表明MOP3作为治疗这种危急且往往致命疾病的创新治疗方法具有潜力。