Laboratory of Immunology, National Eye Institute, NIH, Bethesda, MD, United States.
Signal Transduction Laboratory, National Institute of Environmental Health Sciences, Research Triangle Park, NC, United States.
Front Immunol. 2021 Jan 25;11:583510. doi: 10.3389/fimmu.2020.583510. eCollection 2020.
Non-infectious uveitis, a common cause of blindness in man, is often mediated by autoimmunity, a process in which cytokines play major roles. The biosynthesis and secretion of pro-inflammatory cytokines are regulated in part by tristetraprolin (TTP), an endogenous anti-inflammatory protein that acts by binding directly to specific sequence motifs in the 3'-untranslated regions of target mRNAs, promoting their turnover, and inhibiting synthesis of their encoded proteins. We recently developed a TTP-overexpressing mouse (TTPΔARE) by deleting an AU-rich element (ARE) instability motif from the TTP mRNA, resulting in increased accumulation of TTP mRNA and protein throughout the animal. Here, we show that homozygous TTPΔARE mice are resistant to the induction of experimental autoimmune uveitis (EAU) induced by interphotoreceptor retinoid-binding protein (IRBP), an established model for human autoimmune (noninfectious) uveitis. Lymphocytes from TTPΔARE mice produced lower levels of the pro-inflammatory cytokines IFN-γ, IL-17, IL-6, and TNFα than wild type (WT) mice. TTPΔARE mice also produced lower titers of antibodies against the uveitogenic protein. In contrast, TTPΔARE mice produced higher levels of the anti-inflammatory cytokine IL-10, and had higher frequencies of regulatory T-cells, which, moreover, displayed a moderately higher per-cell regulatory ability. Heterozygous mice developed EAU and associated immunological responses at levels intermediate between homozygous TTPΔARE mice and WT controls. TTPΔARE mice were able, however, to develop EAU following adoptive transfer of activated WT T-cells specific to IRBP peptide 651-670, and naïve T-cells from TTPΔARE mice could be activated by antibodies to CD3/CD28. Importantly, TTPΔARE antigen presenting cells were significantly less efficient compared to WT in priming naïve T cells, suggesting that this feature plays a major role in the dampened immune responses of the TTPΔARE mice. Our observations demonstrate that elevated systemic levels of TTP can inhibit the pathogenic processes involved in EAU, and suggest the possible use of TTP-based treatments in humans with uveitis and other autoimmune conditions.
非传染性葡萄膜炎是一种常见的致盲性眼病,通常由自身免疫介导,而细胞因子在其中发挥了主要作用。前炎性细胞因子的生物合成和分泌受到 tristetraprolin(TTP)的部分调节,TTP 是一种内源性抗炎蛋白,可通过直接结合靶 mRNA 3'非翻译区中的特定序列基序来发挥作用,促进其周转,并抑制其编码蛋白的合成。我们最近通过从 TTP mRNA 中删除一个富含 AU 的不稳定元件(ARE),开发了一种 TTP 过表达的小鼠(TTPΔARE),导致 TTP mRNA 和蛋白在整个动物体内的积累增加。在这里,我们表明,纯合 TTPΔARE 小鼠对光感受器间视网膜结合蛋白(IRBP)诱导的实验性自身免疫性葡萄膜炎(EAU)的诱导具有抗性,IRBP 是人类自身免疫(非传染性)葡萄膜炎的一种既定模型。与野生型(WT)小鼠相比,TTPΔARE 小鼠的淋巴细胞产生的前炎性细胞因子 IFN-γ、IL-17、IL-6 和 TNFα 水平较低。TTPΔARE 小鼠产生的针对致葡萄膜炎蛋白的抗体滴度也较低。相比之下,TTPΔARE 小鼠产生的抗炎细胞因子 IL-10 水平较高,并且具有更高频率的调节性 T 细胞,此外,这些细胞的每细胞调节能力也略高。杂合子小鼠在 EAU 及其相关免疫反应的发展水平介于纯合 TTPΔARE 小鼠和 WT 对照之间。然而,TTPΔARE 小鼠能够在接受针对 IRBP 肽 651-670 的特异性激活 WT T 细胞的过继转移后发展为 EAU,并且 TTPΔARE 小鼠的幼稚 T 细胞可被抗 CD3/CD28 抗体激活。重要的是,与 WT 相比,TTPΔARE 抗原呈递细胞在刺激幼稚 T 细胞方面的效率明显降低,这表明该特征在 TTPΔARE 小鼠的免疫反应减弱中发挥了主要作用。我们的观察结果表明,全身性 TTP 水平升高可抑制 EAU 中涉及的致病过程,并提示在葡萄膜炎和其他自身免疫性疾病的人类中可能使用 TTP 为基础的治疗方法。