National Key Laboratory of Immunity and Inflammation, Institute of Immunology, Naval Medical University, Shanghai, China.
Department of Immunology, Institute of Basic Medical Research, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China.
Nat Metab. 2024 Nov;6(11):2118-2137. doi: 10.1038/s42255-024-01149-x. Epub 2024 Oct 18.
Cellular metabolism modulates dendritic cell (DC) maturation and activation. Migratory dendritic cells (mig-DCs) travelling from the tissues to draining lymph nodes (dLNs) are critical for instructing adaptive immune responses. However, how lipid metabolites influence mig-DCs in autoimmunity remains elusive. Here, we demonstrate that farnesyl pyrophosphate (FPP), an intermediate of the mevalonate pathway, accumulates in mig-DCs derived from mice with systemic lupus erythematosus (SLE). FPP promotes mig-DC survival and germinal centre responses in the dLNs by coordinating protein geranylgeranylation and mitochondrial remodelling. Mechanistically, FPP-dependent RhoA geranylgeranylation promotes mitochondrial fusion and oxidative respiration through mitochondrial RhoA-MFN interaction, which subsequently facilitates the resolution of endoplasmic reticulum stress in mig-DCs. Simvastatin, a chemical inhibitor of the mevalonate pathway, restores mitochondrial function in mig-DCs and ameliorates systemic pathogenesis in SLE mice. Our study reveals a critical role for FPP in dictating mig-DC survival by reprogramming mitochondrial structure and metabolism, providing new insights into the pathogenesis of DC-dependent autoimmune diseases.
细胞代谢调节树突状细胞 (DC) 的成熟和激活。从组织迁移到引流淋巴结 (dLNs) 的迁移树突状细胞 (mig-DC) 对于指导适应性免疫反应至关重要。然而,脂质代谢物如何影响自身免疫中的 mig-DC 仍然难以捉摸。在这里,我们证明法呢基焦磷酸 (FPP),甲羟戊酸途径的中间产物,在系统性红斑狼疮 (SLE) 小鼠来源的 mig-DC 中积累。FPP 通过协调蛋白质香叶基香叶基化和线粒体重塑促进 dLN 中的 mig-DC 存活和生发中心反应。在机制上,FPP 依赖性 RhoA 香叶基香叶基化通过线粒体 RhoA-MFN 相互作用促进线粒体融合和氧化呼吸,从而促进 mig-DC 中内质网应激的解决。他汀类药物,甲羟戊酸途径的化学抑制剂,可恢复 mig-DC 中的线粒体功能,并改善 SLE 小鼠的全身发病机制。我们的研究揭示了 FPP 通过重编程线粒体结构和代谢来决定 mig-DC 存活的关键作用,为 DC 依赖性自身免疫疾病的发病机制提供了新的见解。