Liu Na, Li Rui, Cao Jinglin, Song Xinyao, Ma Wenmiao, Liu Tengli, Wang Le, Zou Jiaqi, Zhang Boya, Liu Zewen, Liang Rui, Zheng Rongxiu, Wang Shusen
Department of Pediatrics, Tianjin Medical University General Hospital, 300052, Tianjin, People's Republic of China.
Research Institute of Transplant Medicine, Organ Transplant Center, NHC Key Laboratory for Critical Care Medicine, Tianjin First Central Hospital, Nankai University, 300384, Tianjin, People's Republic of China.
Cell Death Discov. 2023 Jul 14;9(1):247. doi: 10.1038/s41420-023-01506-x.
The FK506-binding protein 51 (FKBP51, encoded by FKBP5 gene) has emerged as a critical regulator of mammalian endocrine stress responses and as a potential pharmacological target for metabolic disorders, including type 2 diabetes (T2D). However, in β cells, which secrete the only glucose-lowering hormone-insulin, the expression and function of FKBP5 has not been documented. Here, using human pancreatic tissue and primary human islets, we demonstrated the abundant expression of FKBP5 in β cells, which displayed an responsive induction upon acute inflammatory stress mimicked by in vitro treatment with a cocktail of inflammatory cytokines (IL-1β, IFN-γ, and TNF-α). To explore its function, siRNAs targeting FKBP5 and pharmacological inhibitor SAFit2 were applied both in clonal NIT-1 cells and primary human/mice islets. We found that FKBP5 inhibition promoted β-cell survival, improved insulin secretion, and upregulated β-cell functional gene expressions (MAFA and NKX6.1) in acute-inflammation stressed β cells. In primary human and mice islets, which constitutively suffer from inflammation stress during isolation and culture, FKBP5 inhibition also presented decent performance in improving islet function, in accordance with its protective effect against inflammation. Molecular studies found that FKBP5 is an important regulator for FOXO1 phosphorylation at Serine 256, and silencing of FOXO1 abrogated the protective effect of FKBP5 inhibition, suggesting that it is the key downstream effector of FKBP5 in β cells. At last, in situ detection of FKBP5 protein expression on human and mice pancreases revealed a reduction of FKBP5 expression in β cells in human T2D patients, as well as T2D mice model (db/db), which may indicate a FKBP5-inhibition-mediated pro-survival mechanism against the complex stresses in T2D milieus.
FK506结合蛋白51(FKBP51,由FKBP5基因编码)已成为哺乳动物内分泌应激反应的关键调节因子,也是包括2型糖尿病(T2D)在内的代谢紊乱的潜在药理学靶点。然而,在分泌唯一降糖激素胰岛素的β细胞中,FKBP5的表达和功能尚未见报道。在此,我们利用人胰腺组织和原代人胰岛,证明了FKBP5在β细胞中大量表达,在用炎性细胞因子(IL-1β、IFN-γ和TNF-α)混合物进行体外处理模拟急性炎症应激时,FKBP5表现出反应性诱导。为了探究其功能,针对FKBP5的小干扰RNA(siRNA)和药理学抑制剂SAFit2被应用于克隆NIT-1细胞以及原代人/小鼠胰岛。我们发现,在急性炎症应激的β细胞中,抑制FKBP5可促进β细胞存活、改善胰岛素分泌并上调β细胞功能基因(MAFA和NKX6.1)的表达。在原代人胰岛和小鼠胰岛中,它们在分离和培养过程中持续遭受炎症应激,抑制FKBP5在改善胰岛功能方面也表现出良好效果,这与其对炎症的保护作用一致。分子研究发现,FKBP5是FOXO1丝氨酸256位点磷酸化的重要调节因子,沉默FOXO1可消除抑制FKBP5的保护作用,这表明FOXO1是β细胞中FKBP5的关键下游效应因子。最后,对人和小鼠胰腺中FKBP5蛋白表达的原位检测显示,在人类T2D患者以及T2D小鼠模型(db/db)的β细胞中,FKBP5表达降低,这可能表明FKBP5抑制介导了一种针对T2D环境中复杂应激的促存活机制。