Division of Infectious Diseases, Department of Medicine, and.
Department of Infectious Diseases and Microbiology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
JCI Insight. 2023 Jul 24;8(14):e161111. doi: 10.1172/jci.insight.161111.
Resolution of T cell activation and inflammation is a key determinant of the lack of SIV disease progression in African green monkeys (AGMs). Although frequently considered together, T cell activation occurs in response to viral stimulation of acquired immunity, while inflammation reflects innate immune responses to mucosal injury. We dissociated T cell activation from inflammation through regulatory T cell (Treg) depletion with Ontak (interleukin-2 coupled with diphtheria toxin) during early SIV infection of AGMs. This intervention abolished control of T cell immune activation beyond the transition from acute to chronic infection. Ontak had no effect on gut barrier integrity, microbial translocation, inflammation, and hypercoagulation, despite increasing T cell activation. Ontak administration increased macrophage counts yet decreased their activation. Persistent T cell activation influenced SIV pathogenesis, shifting the ramp-up in viral replication to earlier time points, prolonging the high levels of replication, and delaying CD4+ T cell restoration yet without any clinical or biological sign of disease progression in Treg-depleted AGMs. Thus, by inducing T cell activation without damaging mucosal barrier integrity, we showed that systemic T cell activation per se is not sufficient to drive disease progression, which suggests that control of systemic inflammation (likely through maintenance of gut integrity) is the key determinant of lack of disease progression in natural hosts of SIVs.
T 细胞激活和炎症的消退是非洲绿猴(AGM)中缺乏 SIV 疾病进展的关键决定因素。尽管通常将 T 细胞激活和炎症同时考虑,但 T 细胞激活是针对获得性免疫的病毒刺激而发生的,而炎症则反映了对黏膜损伤的固有免疫反应。我们通过在 AGM 感染 SIV 的早期使用 Ontak(白细胞介素 2 与白喉毒素偶联物)耗尽调节性 T 细胞(Treg),将 T 细胞激活与炎症区分开来。这种干预措施消除了从急性感染向慢性感染过渡后对 T 细胞免疫激活的控制。尽管 Ontak 增加了 T 细胞的激活,但它对肠道屏障完整性、微生物易位、炎症和高凝状态没有影响。Ontak 给药增加了巨噬细胞的数量,但减少了其激活。持续的 T 细胞激活影响 SIV 的发病机制,将病毒复制的增加提前到更早的时间点,延长了高水平的复制,并延迟了 CD4+T 细胞的恢复,但在 Treg 耗尽的 AGM 中没有任何疾病进展的临床或生物学迹象。因此,通过诱导 T 细胞激活而不破坏黏膜屏障完整性,我们表明系统 T 细胞激活本身不足以驱动疾病进展,这表明控制全身炎症(可能通过维持肠道完整性)是 SIV 天然宿主中缺乏疾病进展的关键决定因素。