Department of Pharmacology and Systems Physiology, University of Cincinnati College of Medicine, Cincinnati, OH 45267.
Department of Critical Care Medicine, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, Shandong 250021, China.
J Immunol. 2020 Sep 15;205(6):1633-1643. doi: 10.4049/jimmunol.2000440. Epub 2020 Aug 7.
The inability to effectively control invading bacteria or other pathogens is a major cause of multiple organ dysfunction and death in sepsis. As the first-line defense of the immune system, macrophages play a crucial role in the removal of pathogens during sepsis. In this study, we define secreted and transmembrane 1A (Sectm1a) as a novel ligand of glucocorticoid-induced TNFR (GITR) that greatly boosts macrophage phagocytosis and bactericidal capacity. Using a global Sectm1a knockout (KO) mouse model, we observed that Sectm1a deficiency significantly suppressed phagocytosis and bactericidal activity in both recruited macrophages and tissue-resident macrophages, which consequently aggravated bacterial burden in the blood and multiple organs and further increased systemic inflammation, leading to multiple organ injury and increased mortality during polymicrobial sepsis. By contrast, treatment of septic mice with recombinant Sectm1a protein (rSectm1a) not only promoted macrophage phagocytosis and bactericidal activity but also significantly improved survival outcome. Mechanistically, we identified that Sectm1a could bind to GITR in the surface of macrophages and thereby activate its downstream PI3K-Akt pathway. Accordingly, rSectm1a-mediated phagocytosis and bacterial killing were abolished in macrophages by either KO of GITR or pharmacological inhibition of the PI3K-Akt pathway. In addition, rSectm1a-induced therapeutic effects on sepsis injury were negated in GITR KO mice. Taken together, these results uncover that Sectm1a may represent a novel target for drug development to control bacterial dissemination during sepsis or other infectious diseases.
无法有效控制入侵的细菌或其他病原体是导致脓毒症多器官功能障碍和死亡的主要原因。作为免疫系统的第一道防线,巨噬细胞在脓毒症期间清除病原体方面发挥着至关重要的作用。在这项研究中,我们将分泌型和跨膜蛋白 1A(Sectm1a)定义为糖皮质激素诱导的 TN 受体(GITR)的一种新型配体,它极大地增强了巨噬细胞的吞噬作用和杀菌能力。使用全球 Sectm1a 敲除(KO)小鼠模型,我们观察到 Sectm1a 缺乏显著抑制了募集巨噬细胞和组织驻留巨噬细胞的吞噬作用和杀菌活性,这导致血液和多个器官中的细菌负荷增加,进而增加全身炎症,导致多器官损伤和脓毒性多微生物血症期间死亡率增加。相比之下,用重组 Sectm1a 蛋白(rSectm1a)治疗脓毒症小鼠不仅促进了巨噬细胞的吞噬作用和杀菌活性,而且显著改善了生存结果。从机制上讲,我们发现 Sectm1a 可以与巨噬细胞表面的 GITR 结合,从而激活其下游的 PI3K-Akt 途径。因此,在 GITR KO 巨噬细胞或通过 PI3K-Akt 途径的药理学抑制,rSectm1a 介导的吞噬作用和杀菌作用被消除。此外,rSectm1a 在 GITR KO 小鼠中对脓毒症损伤的治疗作用被否定。总之,这些结果揭示了 Sectm1a 可能代表一种新的药物开发靶点,以控制脓毒症或其他传染病期间的细菌传播。