Department of Critical Care Medicine, Sir Run Run Shaw Hospital, College of Medicine, Zhejiang University, Hangzhou, China.
School of Medical Technology and Information Engineering, Zhejiang Chinese Medical University, Hangzhou, China.
PLoS Negl Trop Dis. 2023 Jul 24;17(7):e0011488. doi: 10.1371/journal.pntd.0011488. eCollection 2023 Jul.
Severe fever with thrombocytopenia syndrome (SFTS) is an emerging tick-borne infection with a high mortality rate in humans, which is caused by Dabie bandavirus (DBV), formerly known as SFTS virus. Clinical manifestations of SFTS are characterized by high fever, thrombocytopenia, leukopenia, hemorrhage, gastrointestinal symptoms, myalgia and local lymph node enlargement with up to 30% case fatality rates in human. Macrophage depletion in secondary lymphoid organs have important roles in the pathogenic process of fatal SFTS, but its exact cell death mechanism remains largely unknown. Here, we showed for the first time that DBV infection induced macrophagic pyroptosis, as evidenced by swollen cells, pore-forming structures, accumulation of gasdermin D N-terminal (GSDMD-NT) as well as the release of lactate dehydrogenase (LDH) and IL-1β in human macrophages. In addition to the upregulation of pyronecrosis genes, the expressions of pyroptosis-related proteins (GSDMD, caspase-1 and IL-1β) were also elevated. To be noted, platelets were found to play a protective role in DBV-derived pyroptosis. Transcriptome analysis and in vitro studies demonstrated that platelets significantly reduced the gene expressions and protein production of pro-pyroptotic markers and inflammatory cytokines in macrophages, whereas platelets conferred a propagation advantage for DBV. Collectively, this study demonstrates a novel mechanism by which DBV invasion triggers pyroptosis as a host defense to remove replication niches in human macrophages and platelets provide an additional layer to reduce cellular death. These findings may have important implications to the pathogenesis of lethal DBV, and provide new ideas for developing novel therapeutics to combat its infection.
严重发热伴血小板减少综合征(SFTS)是一种由大别山病毒(DBV)引起的新兴蜱传感染,具有较高的人类死亡率,以前称为 SFTS 病毒。SFTS 的临床表现为高热、血小板减少、白细胞减少、出血、胃肠道症状、肌痛和局部淋巴结肿大,人类的病死率高达 30%。二级淋巴器官中巨噬细胞的耗竭在致命性 SFTS 的发病机制中具有重要作用,但确切的细胞死亡机制仍在很大程度上未知。在这里,我们首次表明 DBV 感染诱导巨噬细胞发生细胞焦亡,这表现在细胞肿胀、形成孔状结构、gasdermin D N 端(GSDMD-NT)积累以及乳酸脱氢酶(LDH)和 IL-1β 的释放。除了坏死基因的上调外,焦亡相关蛋白(GSDMD、caspase-1 和 IL-1β)的表达也升高。值得注意的是,血小板在 DBV 衍生的细胞焦亡中发挥了保护作用。转录组分析和体外研究表明,血小板显著降低了巨噬细胞中前焦亡标志物和炎症细胞因子的基因表达和蛋白产生,而血小板赋予了 DBV 的增殖优势。总之,这项研究证明了 DBV 入侵引发细胞焦亡的新机制,作为宿主防御机制,以清除人巨噬细胞中的复制龛位,而血小板提供了减少细胞死亡的额外保护层。这些发现可能对致死性 DBV 的发病机制具有重要意义,并为开发新的治疗方法来对抗其感染提供了新的思路。