Department of Inflammation and Immunity, Lerner Research Institute, Cleveland, OH 44195.
Gastroenterology and Hepatology, Lerner Research Institute, Cleveland, OH 44195.
Proc Natl Acad Sci U S A. 2024 Jul 30;121(31):e2314760121. doi: 10.1073/pnas.2314760121. Epub 2024 Jul 25.
Transceptors, solute transporters that facilitate intracellular entry of molecules and also initiate intracellular signaling events, have been primarily studied in lower-order species. Ammonia, a cytotoxic endogenous metabolite, is converted to urea in hepatocytes for urinary excretion in mammals. During hyperammonemia, when hepatic metabolism is impaired, nonureagenic ammonia disposal occurs primarily in skeletal muscle. Increased ammonia uptake in skeletal muscle is mediated by a membrane-bound, 12 transmembrane domain solute transporter, Rhesus blood group-associated B glycoprotein (RhBG). We show that in addition to its transport function, RhBG interacts with myeloid differentiation primary response-88 (MyD88) to initiate an intracellular signaling cascade that culminates in activation of NFκB. We also show that ammonia-induced MyD88 signaling is independent of the canonical toll-like receptor-initiated mechanism of MyD88-dependent NFκB activation. In silico, in vitro, and in situ experiments show that the conserved cytosolic J-domain of the RhBG protein interacts with the Toll-interleukin-1 receptor (TIR) domain of MyD88. In skeletal muscle from human patients, human-induced pluripotent stem cell-derived myotubes, and myobundles show an interaction of RhBG-MyD88 during hyperammonemia. Using complementary experimental and multiomics analyses in murine myotubes and mice with muscle-specific RhBG or MyD88 deletion, we show that the RhBG-MyD88 interaction is essential for the activation of NFkB but not ammonia transport. Our studies show a paradigm of substrate-dependent regulation of transceptor function with the potential for modulation of cellular responses in mammalian systems by decoupling transport and signaling functions of transceptors.
转导蛋白是一种能促进分子进入细胞内并启动细胞内信号事件的溶质转运体,主要在低等物种中进行研究。氨是一种细胞毒性内源性代谢物,在哺乳动物中被肝细胞转化为尿素进行尿液排泄。在肝代谢受损的高氨血症期间,非尿素生成氨的处置主要发生在骨骼肌中。骨骼肌中氨的摄取增加是由一种膜结合的 12 个跨膜结构域溶质转运体,即恒河猴血型相关 B 糖蛋白(RhBG)介导的。我们表明,除了其转运功能外,RhBG 还与髓样分化初级反应-88(MyD88)相互作用,启动一个细胞内信号级联反应,最终导致 NFκB 的激活。我们还表明,氨诱导的 MyD88 信号传导独立于经典的 Toll 样受体启动的 MyD88 依赖性 NFκB 激活机制。计算机模拟、体外和原位实验表明,RhBG 蛋白保守的细胞质 J 结构域与 MyD88 的 Toll-白细胞介素-1 受体(TIR)结构域相互作用。在人类患者的骨骼肌、人诱导多能干细胞衍生的肌管和肌束中,在高氨血症期间观察到 RhBG-MyD88 相互作用。使用鼠肌管和肌肉特异性 RhBG 或 MyD88 缺失小鼠的补充实验和多组学分析,我们表明 RhBG-MyD88 相互作用对于 NFkB 的激活是必不可少的,但对于氨的转运不是必需的。我们的研究表明了一种转导蛋白功能的底物依赖性调节范例,有可能通过分离转导蛋白的转运和信号功能来调节哺乳动物系统中的细胞反应。