Yan Chunguang, Chen Jing, Wang Botao, Wang Jingya, Luo Ming, Tong Jingru, Xu Xuanli, Zhang Qi, Wang Ximo
Department of Pathogenic Biology and Immunology, Medical School of Southeast University, Nanjing, 210009, China.
Jiangsu Provincial Key Laboratory of Critical Care Medicine, Zhongda Hospital of Southeast University, Nanjing, 210009, China.
Inflammation. 2024 Aug;47(4):1459-1478. doi: 10.1007/s10753-024-01988-6. Epub 2024 Feb 20.
The role of programmed death ligand 1 (PD-L1) has been extensively investigated in adaptive immune system. However, increasing data show that innate immune responses are also affected by the immune checkpoint molecule. It has been demonstrated that regulation of PD-L1 signaling in macrophages may be a potential therapeutic method for acute respiratory distress syndrome (ARDS). However, the PD-L1 expression pattern in local macrophages and whole lung tissues remains mysterious, hindering optimization of the potential treatment program. Therefore, we aim to determine the PD-L1 expression pattern during ARDS. Our findings show that PD-L1 levels are markedly increased in lipopolysaccharide (LPS)-stimulated lung tissues, which might be attributable to an increase in the gene expression by immune cells, including macrophages and neutrophils. In vitro experiments are performed to explore the mechanism involved in LPS-induced PD-L1 production. We find that PD-L1 generation is controlled by transcription factors early growth response 1 (Egr-1) and CCAAT/enhancer binding protein delta (C/EBPδ). Strikingly, PD-L1 production is enhanced by phosphoinositide-3 kinase (PI3K)-protein kinase B (AKT) signaling pathway via up-regulation of Egr-1 and C/EBPδ expressions. Additionally, we observe that expressions of Egr-1 and C/EBPδ mutually reinforce each other. Moreover, we observe that PD-L1 is protective for ARDS due to its regulatory role in macrophage-associated inflammatory response. In summary, during LPS-induced ARDS, PD-L1 expression, which is beneficial for the disease, is increased via the PI3K-AKT1-Egr-1/C/EBPδ signaling pathway, providing theoretical basis for application of methods controlling PD-L1 signaling in macrophages for ARDS treatment in clinic.
程序性死亡配体1(PD-L1)在适应性免疫系统中的作用已得到广泛研究。然而,越来越多的数据表明,先天免疫反应也受免疫检查点分子的影响。已有研究证明,调节巨噬细胞中PD-L1信号传导可能是治疗急性呼吸窘迫综合征(ARDS)的一种潜在方法。然而,局部巨噬细胞和全肺组织中PD-L1的表达模式仍不清楚,这阻碍了潜在治疗方案的优化。因此,我们旨在确定ARDS期间PD-L1的表达模式。我们的研究结果表明,脂多糖(LPS)刺激的肺组织中PD-L1水平显著升高,这可能归因于包括巨噬细胞和中性粒细胞在内的免疫细胞基因表达的增加。进行体外实验以探索LPS诱导PD-L1产生的机制。我们发现PD-L1的产生受早期生长反应1(Egr-1)和CCAAT/增强子结合蛋白δ(C/EBPδ)转录因子的控制。引人注目的是,磷酸肌醇-3激酶(PI3K)-蛋白激酶B(AKT)信号通路通过上调Egr-1和C/EBPδ的表达增强了PD-L1的产生。此外,我们观察到Egr-1和C/EBPδ的表达相互增强。而且,我们观察到PD-L1对ARDS具有保护作用,因为它在巨噬细胞相关的炎症反应中起调节作用。总之,在LPS诱导的ARDS期间,通过PI3K-AKT1-Egr-1/C/EBPδ信号通路增加了对疾病有益的PD-L1表达,为临床应用控制巨噬细胞中PD-L1信号传导的方法治疗ARDS提供了理论依据。