Shanghai Key Laboratory of Regulatory Biology, School of Life Sciences, East China Normal University, Shanghai, China.
Burn Institute of Chinese PLA and Department of Burn Surgery, Changhai Hospital, Second Military Medical University, Shanghai, China.
PLoS Pathog. 2014 Feb 20;10(2):e1003918. doi: 10.1371/journal.ppat.1003918. eCollection 2014 Feb.
Interleukin-33 (IL-33) is associated with multiple diseases, including asthma, rheumatoid arthritis, tissue injuries and infections. Although IL-33 has been indicated to be involved in Staphylococcus aureus (S. aureus) wound infection, little is known about how IL-33 is regulated as a mechanism to increase host defense against skin bacterial infections. To explore the underlying intricate mechanism we first evaluated the expression of IL-33 in skin from S. aureus-infected human patients. Compared to normal controls, IL-33 was abundantly increased in skin of S. aureus-infected patients. We next developed a S. aureus cutaneous infection mouse model and found that IL-33 was significantly increased in dermal macrophages of infected mouse skin. The expression of IL-33 by macrophages was induced by staphylococcal peptidoglycan (PGN) and lipoteichoic acid (LTA) via activation of toll-like receptor 2(TLR2)-mitogen-activated protein kinase (MAPK)-AKT-signal transducer and activator of transcription 3(STAT3) signaling pathway as PGN and LTA failed to induce IL-33 in Tlr2-deficient peritoneal macrophages, and MAPK,AKT, STAT3 inhibitors significantly decreased PGN- or LTA-induced IL-33. IL-33, in turn, acted on macrophages to induce microbicidal nitric oxygen (NO) release. This induction was dependent on inducible nitric oxide synthase (iNOS) activation, as treatment of macrophages with an inhibitor of iNOS, aminoguanidine, significantly decreased IL-33-induced NO release. Moreover, aminoguanidine significantly blocked the capacity of IL-33 to inhibit the growth of S. aureus, and IL-33 silencing in macrophages significantly increased the survival of S. aureus in macrophages. Furthermore, the administration of IL-33-neutralizing antibody into mouse skin decreased iNOS production but increased the survival of S. aureus in skin. These findings reveal that IL-33 can promote antimicrobial capacity of dermal macrophages, thus enhancing antimicrobial defense against skin bacterial infections.
白细胞介素-33 (IL-33) 与多种疾病相关,包括哮喘、类风湿性关节炎、组织损伤和感染。尽管已经表明白细胞介素-33参与了金黄色葡萄球菌 (S. aureus) 伤口感染,但对于白细胞介素-33如何作为一种增强宿主对皮肤细菌感染防御能力的机制调节知之甚少。为了探索潜在的复杂机制,我们首先评估了金黄色葡萄球菌感染患者皮肤中 IL-33 的表达。与正常对照组相比,金黄色葡萄球菌感染患者的皮肤中 IL-33 大量增加。接下来,我们建立了金黄色葡萄球菌皮肤感染小鼠模型,发现感染小鼠皮肤的真皮巨噬细胞中 IL-33 显著增加。金黄色葡萄球菌的肽聚糖 (PGN) 和脂磷壁酸 (LTA) 通过激活 Toll 样受体 2 (TLR2)-丝裂原活化蛋白激酶 (MAPK)-AKT-信号转导和转录激活因子 3 (STAT3) 信号通路诱导巨噬细胞表达 IL-33,因为 PGN 和 LTA 不能诱导 TLR2 缺陷型腹腔巨噬细胞表达 IL-33,而 MAPK、AKT、STAT3 抑制剂则显著降低了 PGN 或 LTA 诱导的 IL-33。IL-33 反过来作用于巨噬细胞诱导杀菌性一氧化氮 (NO) 释放。这种诱导依赖于诱导型一氧化氮合酶 (iNOS) 的激活,因为用 iNOS 抑制剂氨基胍处理巨噬细胞会显著降低 IL-33 诱导的 NO 释放。此外,氨基胍显著阻断了 IL-33 抑制金黄色葡萄球菌生长的能力,并且巨噬细胞中 IL-33 的沉默显著增加了金黄色葡萄球菌在巨噬细胞中的存活。此外,将 IL-33 中和抗体注入小鼠皮肤会降低 iNOS 的产生,但会增加皮肤中金黄色葡萄球菌的存活。这些发现表明,IL-33 可以增强真皮巨噬细胞的抗菌能力,从而增强对皮肤细菌感染的抗菌防御。