Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Canada.
University of Ottawa Centre for Infection, Immunity, and Inflammation (CI3), University of Ottawa, Ottawa, Canada.
PLoS Pathog. 2023 Jun 22;19(6):e1011455. doi: 10.1371/journal.ppat.1011455. eCollection 2023 Jun.
XIAP is an endogenous inhibitor of cell death and inactivating mutations of XIAP are responsible for X-linked lymphoproliferative disease (XLP-2) and primary immunodeficiency, but the mechanism(s) behind these contradictory outcomes have been unclear. We report that during infection of macrophages and dendritic cells with various intracellular bacteria, XIAP restricts cell death and secretion of IL-1β but promotes increased activation of NFκB and JNK which results in elevated secretion of IL-6 and IL-10. Poor secretion of IL-6 by Xiap-deficient antigen presenting cells leads to poor expansion of recently activated CD8 T cells during the priming phase of the response. On the other hand, Xiap-deficient CD8 T cells displayed increased proliferation and effector function during the priming phase but underwent enhanced contraction subsequently. Xiap-deficient CD8 T cells underwent skewed differentiation towards short lived effectors which resulted in poor generation of memory. Consequently Xiap-deficient CD8 T cells failed to provide effective control of bacterial infection during re-challenge. These results reveal the temporal impact of XIAP in promoting the fitness of activated CD8 T cells through cell extrinsic and intrinsic mechanisms and provide a mechanistic explanation of the phenotype observed in XLP-2 patients.
XIAP 是细胞死亡的内源性抑制剂,XIAP 的失活突变导致 X 连锁淋巴组织增生性疾病(XLP-2)和原发性免疫缺陷,但这些矛盾结果的机制尚不清楚。我们报告称,在各种细胞内细菌感染巨噬细胞和树突状细胞期间,XIAP 限制细胞死亡和 IL-1β 的分泌,但促进 NFκB 和 JNK 的激活增加,从而导致 IL-6 和 IL-10 的分泌增加。抗原呈递细胞中缺乏 Xiap 导致 IL-6 分泌不良,导致在反应的初始阶段新激活的 CD8 T 细胞扩增不良。另一方面,Xiap 缺陷的 CD8 T 细胞在初始阶段表现出增殖和效应功能增强,但随后经历了增强的收缩。Xiap 缺陷的 CD8 T 细胞向短命效应器的分化偏向,导致记忆生成不良。因此,Xiap 缺陷的 CD8 T 细胞在再次受到挑战时无法有效控制细菌感染。这些结果揭示了 XIAP 通过细胞外和内在机制促进激活的 CD8 T 细胞适应性的时间影响,并为 XLP-2 患者观察到的表型提供了机制解释。