Center for Infectious Medicine, Department of Medicine, Karolinska Institutet, Karolinska University Hospital, 141 52 Huddinge, Sweden.
Department of Microbiology and Immunology, Western University, London, ON N6A 5C1, Canada.
Proc Natl Acad Sci U S A. 2019 Dec 17;116(51):25923-25931. doi: 10.1073/pnas.1910883116. Epub 2019 Nov 26.
Streptococcal toxic shock syndrome (STSS) is a rapidly progressing, life-threatening, systemic reaction to invasive infection caused by group A streptococci (GAS). GAS superantigens are key mediators of STSS through their potent activation of T cells leading to a cytokine storm and consequently vascular leakage, shock, and multiorgan failure. Mucosal-associated invariant T (MAIT) cells recognize MR1-presented antigens derived from microbial riboflavin biosynthesis and mount protective innate-like immune responses against the microbes producing such metabolites. GAS lack de novo riboflavin synthesis, and the role of MAIT cells in STSS has therefore so far been overlooked. Here we have conducted a comprehensive analysis of human MAIT cell responses to GAS, aiming to understand the contribution of MAIT cells to the pathogenesis of STSS. We show that MAIT cells are strongly activated and represent the major T cell source of IFNγ and TNF in the early stages of response to GAS. MAIT cell activation is biphasic with a rapid TCR Vβ2-specific, TNF-dominated response to superantigens and a later IL-12- and IL-18-dependent, IFNγ-dominated response to both bacterial cells and secreted factors. Depletion of MAIT cells from PBMC resulted in decreased total production of IFNγ, IL-1β, IL-2, and TNFβ. Peripheral blood MAIT cells in patients with STSS expressed elevated levels of the activation markers CD69, CD25, CD38, and HLA-DR during the acute compared with the convalescent phase. Our data demonstrate that MAIT cells are major contributors to the early cytokine response to GAS, and are therefore likely to contribute to the pathological cytokine storm underlying STSS.
链球菌中毒性休克综合征(STSS)是由 A 组链球菌(GAS)引起的侵袭性感染导致的一种快速进展、危及生命的全身性反应。GAS 超抗原通过其对 T 细胞的强烈激活,导致细胞因子风暴,从而导致血管渗漏、休克和多器官衰竭,是 STSS 的关键介质。黏膜相关不变 T(MAIT)细胞识别由微生物核黄素生物合成衍生的 MR1 呈递的抗原,并对产生这些代谢物的微生物产生保护性先天样免疫反应。GAS 缺乏从头合成核黄素,因此 MAIT 细胞在 STSS 中的作用迄今为止一直被忽视。在这里,我们对人类 MAIT 细胞对 GAS 的反应进行了全面分析,旨在了解 MAIT 细胞对 STSS 发病机制的贡献。我们表明,MAIT 细胞被强烈激活,并代表 GAS 早期反应中 IFNγ 和 TNF 的主要 T 细胞来源。MAIT 细胞的激活是双相的,对超抗原具有快速的 TCR Vβ2 特异性、TNF 主导的反应,对细菌细胞和分泌因子具有后期的 IL-12 和 IL-18 依赖性、IFNγ 主导的反应。从 PBMC 中耗尽 MAIT 细胞会导致 IFNγ、IL-1β、IL-2 和 TNFβ 的总产生减少。与恢复期相比,STSS 患者的外周血 MAIT 细胞在急性期表达高水平的激活标志物 CD69、CD25、CD38 和 HLA-DR。我们的数据表明,MAIT 细胞是 GAS 早期细胞因子反应的主要贡献者,因此可能有助于 STSS 中潜在的病理性细胞因子风暴。